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Running head: SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
Scratching as a Behavioral Indicator
of Positive and Negative Arousal in Common Marmosets (Callithrix jacchus)
Sarah Neal
California State University San Marcos
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SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
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Abstract
Negative emotional arousal is associated with a pattern of physiological and behavioral
responses, such as increases in heart rate, blood pressure, and locomotion. In captive Old World
monkeys and apes, self-directed scratching is a well-known behavioral indicator of negative
arousal, with increased rates of scratching occurring in conjunction with simulated predation
threats, social competition, cognitive challenge, and interactions with dominant conspecifics.
Additionally, scratching in the context of negative arousal has also been found to be lateralized
(i.e., scratching is directed to one side of the body or the other). For example, chimpanzees tend
to prefer to use the right hand to scratch the left side of the body during anxiety-provoking
circumstances. I tested the prediction that scratching in response to negative arousal generalizes
to a sample of naturally-housed New World primates (common marmosets; Callithrix jacchus).
The second aim of my thesis was to determine if contexts of positive arousal (play, food
anticipation, and foraging) are also associated with increased rates of scratching, a question that
has not yet been addressed in the literature. Finally, I predicted that subjects would scratch more
with the left hand than the right during negative arousal, and examined with which hand subjects
would scratch more during positive arousal. Contrary to the first prediction, and contrary to the
widely accepted assumption that there is a positive relationship between anxiety and scratching
in primates, my results showed that scratching significantly decreased in response to all three
negative arousal contexts. Contexts within positive arousal showed varying patterns of scratching
between baseline, manipulation, and post-manipulation periods. There were no differences
between the frequency of left and right limb scratches during negative arousal manipulations.
There was a bias for right hand scratching in the positive arousal conditions, but the overall rates
of scratching in all manipulations were too low to adequately address the prediction about
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
lateralized scratching. Overall, data from this study point to the conclusion that the anxietyscratching relationship may be more complex than is generally accepted in the literature.
Keywords: scratching, arousal, marmoset, anxiety, laterality
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Scratching as a Behavioral Indicator of Positive and Negative Arousal
in Common Marmosets (Callithrix jacchus)
The term “arousal” is used in different ways in the psychological and neuroscience
literature. At the most basic level, arousal refers to the on-off state of the brain (e.g., conscious
versus unconscious), which is controlled by the reticular activating system (RAS) (Berlyne,
1960). Arousal is also used to describe the activation of the autonomic nervous system. When
humans experience a stressful or exciting situation, the hypothalamus triggers activation of the
sympathetic nervous system, which, among other reactions, increases heart rate and blood
pressure (Berlyne, 1960; Comer, 2010). Additionally, the RAS, which exhibits EEG activation
patterns, works with the sympathetic nervous system and inhibits parasympathetic activity to
increase arousal (Berlyne, 1960).
In human studies, investigators can induce arousal, measure the resulting behavioral and
physiological responses, and simultaneously ask participants to label what they are feeling. We
assume that the physiological responses that accompany self-reported feelings of anxiousness in
humans, including increased heart rate, blood pressure, breathing, and muscular tension (Comer,
2010), can be generalized to non-human animals. Furthermore, when animals engage in
behaviors that humans exhibit during states of anxiety, such as increased agitation and
vigilance/visual scanning (Koenig, 1998), we assume the animal is experiencing something
equivalent to anxiety.
In humans, the physiological and behavioral correlates of arousal may look very similar
for positive and negative arousal, but the self-reported emotional and cognitive correlates differ.
For example, a person might exhibit increased heart rate, blood pressure, muscular tension, and
agitation, but, depending on the circumstances, describe that arousal as either excitement
(positive arousal) or anxiety (negative arousal). In non-human animals, there are some external
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indications as to whether the arousal may be positive or negative, including the presence of
context-specific vocalizations, approach/avoidance behaviors, and signs of pain. For example,
non-human primates issue alarm calls and contact calls in anxiety-provoking situations, such as
confrontation with a predator or separation from the social group (Norcross & Newman, 1999).
Additionally, like humans, animals tend to avoid unpleasant circumstances and approach or
actively seek pleasant circumstances or stimuli (Clara et al., 2008; Mellou, 2006). In the absence
of these indicators of negative arousal (i.e., alarm calls, avoidance, and pain), we can assume that
the exhibited arousal is positive.
Understanding the neural substrates and behavioral correlates of arousal not only
contributes to the body of knowledge in behavioral neuroscience, but also has important
implications for improving the well-being of captive animals in research laboratories and zoos.
Successful animal husbandry reduces stress (which can lead to negative arousal) and provides
opportunities for enrichment (which can produce positive arousal). Thus, successful husbandry is
dependent on a thorough understanding of the nature and indices of positive and negative
arousal.
Positive Arousal
Positive arousal is less commonly studied than negative arousal, and, as described above,
the distinction between positive and negative arousal is complicated by the fact that they share
some physiological and behavioral correlates (Jacob et al., 1999; Schwartz, Weinberger, &
Singer, 1981). For example, in comparing cardiovascular differences between the induced
emotional states of happiness and fear, Schwartz et al. (1981) found that human subjects
exhibited similar increases in blood pressure during fear and happiness. The authors also found
an increase in heart rate during fear and happiness, although the increases were higher during
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fear than happiness. This pattern of findings is consistent with other research that has found
increases in heart rate and blood pressure during both positive and negative mood in humans
(Jacob et al., 1991; Waldstein et al., 2000). In nonhuman animals, positive arousal is assumed to
arise when there are indications of excitement (increased locomotion and attention) in the
absence of aggression, fear-related vocalizations/postures/facial expressions, stereotypies, or
pain.
Play as Positive Arousal in Nonhuman Primates
Play is widely considered to be an expression of positive arousal and well-being (Biben
& Campoux, 1999; Lancy, 1980; Mellou, 2006). Animals often seek opportunities to play and
will play for long periods of time (Mellou, 2006). Many studies of primates have shown that
rates of play are greatly reduced during stressful situations (e.g., in the presence of predatory
threat or food deprivation), leading to the conclusion that play is a good indicator of
psychological well-being (Baldwin & Baldwin, 1974; Biben & Champoux, 1999; Lancy, 1980;
Loy, 1970; Mellou, 2006; O’Neill-Wagner, Bolig, & Price, 1994; Spinka, Newberry, & Bekoff,
2001). There is even evidence that the mere observation of play is arousing. Parr and Hopkins
(2000) had chimpanzees (Pan troglodytes) view a video of intense play and measured resulting
tympanic membrane thermometry (tty) to assess overall brain temperature (higher brain
temperature is indicative of higher arousal). They found that left tty increased while viewing the
play videos. The inhibition of aggression and absence of injury during play (Poirier, Bellisari, &
Haines, 1978) suggests that, despite its “rough and tumble” nature, the arousal associated with
play is of a positive nature.
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Positive Arousal in Feeding Contexts
Researchers have also examined positive arousal in appetitive contexts (i.e., contexts in
which an animal anticipates and/or consumes highly desirable foods). Braesicke et al. (2005) had
common marmosets (Callithrix jacchus) view preferred (marshmallows, raisins, and grapes) and
non-preferred (laboratory pellets) foods through a small hole in a food box during two phases: an
anticipation period, in which the subjects could only view the food, and a consumption period, in
which the subjects were allowed to eat the food. The authors found that heart rate and blood
pressure were higher when viewing and consuming preferred rather than non-preferred foods.
Additionally, there is evidence for a dissociation between the pleasure caused by the anticipatory
period and the consumption period in these appetitive contexts. The anticipatory period, or the
“wanting,” activates the dopamine system; in fact, simply searching for food, or foraging, (i.e.,
the “wanting” of food) is sufficient to activate the dopamine neurotransmitter system. On the
other hand, the consumption period, or “liking,” activates the opioid system (Boissy et al., 2007).
Other research using the anticipatory period of food rewards has found increases in locomotor
activity (an indication of arousal) in various species of captive animals, including mink, pigs, and
rats (Boissy et al., 2007).
Negative Arousal
Unlike positive arousal, negative arousal (usually referred to as anxiety in primates) has
been given a great deal of empirical attention, especially in nonhuman primates, in part because
it is used to assess well-being in captivity. Researchers have identified a number of
physiological and behavioral indicators of anxiety, including stereotypies (Koolhaus et al.,
1999), increased cortisol levels (Clara, Tommasi, & Rogers, 2008; Elder & Menzel, 2001;
Higham, Maclarnon, Hesitermann, & Semple, 2009), increased heart rate (Boccia, Reite, &
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Laundenslager, 1988), increased blood pressure (Parr, 2001; Parr & Hopkins, 2000), piloerection
(De Almeida, De Paula, & Tavora, 2006; Dettling, Pryce, Martin, & Dobeli, 1998; Omedes,
1981), lowered skin temperature (Tomaz, Verburg, Boere, Pianta, & Belo, 2003), and selfdirected behaviors (Diezinger & Anderson, 1986; Elder & Menzel, 2001; Maestripieri, Schino,
Aureli, & Troisi, 1991; Leavens, Aureli, & Hopkins, 2004; Mason & Perry, 2000; Troisi et al.,
1991). Of most importance for the proposed study is the literature on anxiety and a prominent
form of self-directed behavior: self-scratching.
Scratching as an Indicator of Negative Arousal
Self-directed behaviors (SDBs), including scratching, grooming, yawning, body shaking,
and rubbing, occur during anxiety-provoking situations, and are thought to reflect feelings of
uncertainty, threat, or danger (Elder & Menzel, 2001; Leavens, Aureli, & Hopkins, 2004; Mason
& Perry, 2000). Self-scratching (hereafter, “scratching”), defined as movement of the fingers in a
repetitive, parallel scraping or raking motion across a body part or fur (Mootnick, Cunningham,
& Baker, 2012; Troisi et al., 1991), is one of the most commonly used behavioral indicators of
anxiety among nonhuman primates. Although scratching can occur in the context of selfgrooming, many researchers believe that scratching as grooming and scratching as an indicator
of anxiety are separate behaviors. For example, Mootnick et al. (2012) were able to distinguish
grooming from scratching by more clearly defining the two behaviors. The authors defined selfgrooming as manipulation of the fur using the thumb, with gaze directed at the groomed body
part, whereas scratching does not include these specifications. In using these definitions, they
were able to exclude self-grooming from their analyses of self-scratching across various primate
species. Diezinger & Anderson (1986) concluded that skin care scratching and scratching as a
SDB are causally different, and may have different determinants as indicated by the finding that
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animals differentially direct these two activities across their bodies. Specifically, rhesus monkeys
(Macaca mulatta) directed most scratching toward the legs, back, and thighs, whereas most selfgrooming was directed toward the arms and legs, with the least amount of self-grooming directed
toward the thighs.
Scratching in social contexts. Much of the research on scratching and anxiety in non­
human primates has focused on social contexts because of the inherent tension resulting from the
potential for conflict. Scratching rates increase with (the risk of) intra- and inter-group
aggression, whereas rates of scratching decrease when social tension is reduced via allogrooming
(Maestripieri et al., 1991; Schino, Maestripieri, Scucchi, & Turillazzi, 1990). Research from
social contexts has primarily focused on anxiety and scratching in relation to dominance rank
and risk of threat or aggression from conspecifics.
Pavani et al. (1991) examined scratching rates in response to inter-individual proximity
(passive contact, close proximity, and solitariness) in conjunction with dominance rank in longtailed macaques (M. fascicularis). They found that subordinate animals had higher scratching
rates in general, and that females scratched more when in close proximity to a male. The authors
reasoned that the increased scratching was indicative of anxiety stemming from conflicting
motivation to approach and withdraw from the more dominant conspecific.
Diezinger and Anderson (1986) found that a sample of rhesus macaques of intermediate
rank scratched nearly twice as frequently as dominant and low ranking individuals during
feeding time. Low-ranking individuals did not attempt to obtain food until all higher-ranking
individuals had already done so, thus reducing the potential for anxiety in that context.
Intermediate-ranking monkeys, however, vacillated between approach to and avoidance of the
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food in the presence of a higher-ranking group mate, thus increasing anxiety due to conflicting
motivations.
Viewing or hearing conspecifics in a state of anxiety also induces scratching in great
apes. For example, Japanese macaques (M. fuscata) are known to increase scratching (and other
SDB) rates in response to viewing a strange conspecific in an alert posture. Nakayama (2004)
called this a “contagion of scratching,” representing a transmission of arousal between the
animals. Furthermore, chimpanzees need not see conspecifics in their physical environment in
order for arousal transmission to occur. Even hearing a neighbor’s vocalizations (hooting,
screaming, or banging/drumming) (Baker & Aureli, 1997) or viewing a video of agonistic
encounters between a group of unknown chimpanzees (Hopkins et al., 2006) is effective in
increasing scratching rates in chimpanzee subjects. Lastly, close proximity to an unknown
conspecific can induce scratching. Schino et al. (1990) found that female long-tailed macaques
increased overall rates of SDBs, including scratching, when placed near an unfamiliar rather than
familiar conspecific. The authors conclude that this increased scratching was indicative of
anxiety resulting from uncertainty and risk of aggression from the unknown conspecific.
Scratching in non-social contexts. Cognitive challenges can cause negative arousal,
which has been correlated with rates of SDBs. Leavens et al. (2001) used a computerized match­
to-sample (MTS) task, in which the subject was required to match a given symbol to a sample
symbol using a joystick in both easy (simple discrimination between the symbols) and hard
(difficult discrimination between the symbols) conditions. Subjects that transitioned from the
easy to the difficult task exhibited more scratching overall than subjects that transitioned from
the hard to the easy task. Using a very similar procedure, Leavens et al. (2004) also found that
increased scratching rates in chimpanzees occurred with more incorrect responses in a MTS task.
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Elder and Menzel (2001) had a female orangutan (Pongo pygmaeus) use a joystick to
move a cursor on a computer screen. This task included three conditions varying in difficulty
level: the subject had to (a) solve four problems at a time with a fast-moving cursor to receive a
reward, (b) solve one problem with a slow-moving cursor to receive a reward, or (c) solve one
problem with a fast-moving cursor with a delay inserted between solving the problem and
receiving the reward. The subject exhibited the highest rates of SDBs during the inserted delay
condition, suggesting that the subject was negatively aroused when an expected reward was not
provided.
Pharmacological evidence of the relationship between anxiety and scratching.
Pharmacological studies also connect scratching to anxiety. The majority of these studies use
anxiolytic and anxiogenic drugs to reduce or induce scratching or other SDBs. Barros et al.
(2000) studied scratching and anxiety in Cerrado marmosets (C. penicillata) by creating a
predator model of anxiety called the Marmoset Predator Confrontation Test (MPCT). In this
model, the subject is placed into an eight-figure maze after administration of diazepam (valium)
or saline, and subsequently confronted with a taxidermied model of a cat (Felis tigrina), a
predator common to the marmoset’s natural environment. The authors found that 2 and 3 mg/kg
doses were effective in reducing overall scratching rates compared to the saline control. These
doses also increased the amount of time spent in the section closest to the model predator. This
implies that the marmosets that received the anxiolytic drug were less anxious, as indicated by
decreased rates of scratching as well as increased amount of time spent near what would
normally be an anxiety-inducing stimulus. Furthermore, the Barros et al. data show that rates of
scratching in the absence of arousal (i.e., when medicated with diazepam) are very low,
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averaging less than 1 scratch per hour. This is an important indication of the extent to which
scratching is related to arousal.
Cilia and Piper (1996) found similar results to Barros et al. (2000). Their sample of
common marmosets exhibited decreased rates of scratching after 1.0 and 3.5 mg/kg doses of
diazepam in response to an unknown conspecific. Furthermore, they found that the anxiolytic
drug doses also decreased rates of other anxiety-related behaviors, such as aggression and selfgrooming. Schino et al. (1996) examined the effects of both anxiogenic (FG 7142) and anxiolytic
(lorazepam) drugs on the frequency of scratching and other anxiety-related behaviors (i.e.,
autogrooming and body shaking) in female macaques (M. fasicularis). They found dose
dependent increases in scratching and other anxiety-related behaviors in response to the
anxiogenic drug, and dose dependent decreases in scratching and anxiety-related behaviors in
response to the anxiolytic drug. Schino et al. (1991) also demonstrated that lorazepam decreased
scratching in female macaques, particularly those of low rank. These authors showed that
lorazepam did not change the baseline rates of grooming, locomotion, and passive aggression,
suggesting that possible sedation from the drug was not responsible for the changes in rates of
scratching. Thus, the authors concluded that the decreases in anxiety due to administration of
lorazepam were responsible for the observed reductions in scratching.
Taken together, the results of the aforementioned pharmacological studies suggest that
scratching is associated with the internal state of anxiety. Drugs that are used to induce and
reduce anxiety in humans are effective at inducing and reducing anxiety-related behaviors in
non-human primates with concurrent productions and reductions in scratching.
Physiological evidence of the relationship between anxiety and scratching. Few
researchers have attempted to correlate scratching with physiological indicators of anxiety such
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as heart rate, blood pressure, and circulating levels of catecholamines and corticosteroids
(Maestripieri et al., 1991). In fact, no studies have investigated correlations between scratching
and blood pressure or circulating catecholamines, and only one study has indirectly examined
heart rate in relation to scratching. As in humans, increased heart rate is suggestive of the internal
state of anxiety in primates. Consistent with research linking scratching to anxiety in social
agonistic encounters, Boccia, Reite, and Laudenslager (1988) found that the heart rate of a pigtail
macaque (M. leonina) increased during agonistic encounters and decreased upon initiation of
allogrooming. Because heart rate is a well-established indicator of anxiety, and because heart
rate increases during agonistic encounters, researchers assume that agonistic encounters induce
anxiety in the animal. Consequently, because scratching increases during agonistic encounters,
the assumption can be made that scratching is an indicator of anxiety in the animal during these
types of situations (Maestripieri et al., 1991; Manson & Perry, 2000; Pavani et al., 1991; Schino
et al., 1990).
The level of circulating cortisol is another physiological indicator of anxiety that has been
investigated in the literature on self-scratching. Cortisol is often called the “stress hormone”
because it is released during times of increased physiological or psychological demand (Axelrod
& Reisine, 1984). In humans, increased cortisol levels are associated with high levels of anxiety
and/or stress. However, research concerning cortisol levels, anxiety, and scratching in primates is
inconclusive. In inducing frustration in a male orangutan, Elder and Menzel (2001) found lower
cortisol levels during testing (computer tasks) days than during non-testing (baseline) days,
whereas scratching rates were higher during testing than non-testing days. The authors
mentioned the possibility that engaging in scratching may serve as a behavioral release of
anxiety, consequently lowering cortisol levels and acting as a coping mechanism. Higham,
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Maclarnon, Heistermann, Ross, and Semple (2009) also found no correlation between scratching
rates and fecal glucocorticoid levels in female wild olive baboons (Papio hamadryas nubis).
These authors speculated that scratching may serve as an effective coping mechanism for anxiety
or stress (although it is entirely unclear how it could do so), and that scratching may be more
related to low-level anxiety than chronic stress. Maestripieri et al. (1991) also stated that
scratching (and other displacement activities) may function to regulate the animal’s
psychological state. This regulation would consist of reducing anxiety by either redirecting
attention to the body and away from noxious stimuli, or causing actual physiological changes,
such as increased catecholamine release. In any case, research that simultaneously examines
physiological correlates of anxiety and scratching is needed to further understand the source of
the scratching-anxiety relationship in non-human primates.
The Neurological Basis of the Arousal-Scratch Association: Evidence from Lateralization.
There is ample evidence that scratching is related to anxiety, but the reason for this
association is unclear. Hopkins et al. (2006) write that arousal may cause histamine release
and/or piloerection, which, in turn, makes individuals feels “itchy.” These or other explanations
await empirical confirmation. But data from studies of lateralized preferences for scratching
have implicated the right hemisphere in the scratch response.
Lateralization refers to the specialization of the cerebral hemispheres for certain
biological functions, including behavior. Two popular theories propose that the left and right
hemispheres are equally, but differently, involved in emotions (Demaree, Everhart, Youngstrom,
& Harrison, 2005). There is good evidence that the medial pre-frontal cortex (and some other
regions) of the right hemisphere are selectively involved in autonomic responsiveness to stress in
rats and humans (Denenberg & Yutzey, 1985; Wittling, 1997). The emotional-valence
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hypothesis (Silbermann & Weingartner, 1986) posits that the right hemisphere controls responses
to negative arousal, such as anxiety, and the left hemisphere controls responses to positive
arousal, such as excitement. The approach-withdrawal hypothesis, put forth by Davidson (1992),
states that approach-related behaviors (positive arousal) are associated with greater activity in the
left hemisphere, whereas withdrawal behaviors (negative arousal) are associated with greater
activity in the right hemisphere. Combined, these two theories have led to the assumption that
animals placed in positively arousing situations (i.e., situations that induce happiness, approach,
and excitement) should exhibit increases in left-hemisphere activity (Berlyne, 1960). Animals
placed in negatively arousing situations (i.e., situations that induce anxiety or fear and
avoidance) should exhibit increased activity in the right hemisphere.
Behavioral evidence supporting emotional lateralization and the valence and approachwithdrawal hypotheses includes data showing that fish, reptiles, and mammals, including non­
human primates, prefer to view threatening stimuli with the left eye (Bisazza, Rogers, &
Vallortigara, 1998; Bracinni et al., 2012; Rogers, 2010). Non-human primates have
approximately 50% decussation of the optic fibers (Brooks, Komaromy, & Kallberg, 1999);
however, the contralateral fibers are larger in diameter, and thus conduct more quickly than the
ipsilateral fibers (Rogers, Ward, & Stafford, 1994). Thus, a left eye preference is indicative of
greater activity in the right hemisphere. Studies have also investigated emotional lateralization in
the form of motor biases. Austin and Rogers (2007) found that horses (Equus caballus) move
farther away when confronted with an inanimate threatening stimulus from the left. Furthermore,
Hook-Costigan and Rogers (1998) found that common marmosets display larger left-mouth
movements than right-mouth movements when issuing alarm calls. These studies suggest that the
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right hemisphere is more active during anxiety-provoking or stressful situations, that is, when
animals are negatively aroused.
Leavens et al. (2004) found that a single chimpanzee subject preferentially scratched the
left side of his body during poorer performance on a difficult cognitive task. Moreover, Hopkins
et al. (2006) found that chimps who viewed videos of agonistic encounters of unknown
conspecifics directed self-scratches toward the left side of the body. Both Leavens et al. (2001,
2004) and Hopkins et al. (2006) explained their findings in terms of nervous system
organization. First, as explained above, the right hemisphere shows increased activity during
negative emotional arousal. Second, ipsilaterally descending fibers traveling through the dorsal
horns of the spinal cord inhibit pain and itch. If the right hemisphere is more active, sensation in
the right cutaneous hemispace is more inhibited, causing the perception of increased sensitivity
in the left hemispace. As such, animals in anxiety-provoking situations may scratch their left side
more because of perceived greater arousal and sensitivity in the left hemispace.
However, the conclusions drawn by Leavens et al. (2004) are speculative. Hopkins et al.
(2006) point to the need for more research in this area, stating that there are many physiological
models that could account for the observed left-side scratching bias. Indeed, studies conducted
with common marmosets present a perplexing case of lateralized scratching, as side and hand
preferences during scratching are confounded. Neal, Rice, Ritzer, Wombolt, and Caine (2013)
examined hand preferences during scratching in common marmosets with the specific aim of
replicating the left side scratching bias in a different species. We found that subjects scratched
significantly more with their left hand and on the left side of the body, regardless of overall hand
preferences. If we focus solely on the findings of increased left hand scratching, it seems that
scratching may be a result of contralateral motor biases under conditions of arousal. That is,
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because the brain controls the limbs in a contralateral manner, and because the right hemisphere
is more active during anxiety-provoking situations, the result may be increased motor activity on
the left side (i.e., a left motor bias in the form of left hand scratching). However, if we focus
solely on the left side scratching preferences, the data seem to support the Leavens et al.
hypothesis of increased cutaneous sensitivity on the left side of the body during arousal.
However, our data were collected without manipulating arousal in the marmosets.
Summary
In summary, scratching as a behavioral indicator of arousal in nonhuman primates is
evidenced by behavioral and pharmacological research findings. However, all of these studies
examine scratching in relation to negative arousal (i.e., anxiety). Although positive and negative
arousal are assumed to be accompanied by different cognitive and emotional states, there are
many physiological similarities between positive and negative arousal. For example, both
positive and negative arousal involve increases in heart rate and blood pressure, as well as
increases in locomotion (Engel et al., 2009). Some research has found that self-reported,
experimentally induced levels of itchiness in humans are greater in response to negative than
positive mood. Unfortunately, the authors did not compare the positive mood condition to a
neutral emotion condition (van Laarhoven et al., 2012). If scratching is a result of general
physiological arousal, it should be seen in both positive and negative contexts. However, if the
right hemisphere is less engaged during positive than negative arousal, there might not be the
same autonomic mechanisms at play, and hence less scratching. Finally, the different cognitive
correlates of positive (excited) and negative (anxious) arousal might influence the behavior in as
yet unexplored ways.
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Furthermore, studies of scratching are primarily limited to laboratory housed apes and
Old World monkeys. Even small differences in neuroanatomy and physiology may change the
nature and behavioral correlates of arousal across species, and stressors used to cause arousal in
laboratory settings (which are highly artificial in many ways) may be perceived and reacted to in
ways that are not typical of free-living primates. Therefore, we need additional research to
understand the scratching-arousal relationship.
Current Study
In my thesis I tested the prediction that negative arousal would be positively related to
scratching in naturalistically-housed common marmosets. This prediction was based on studies
of primates that have found this relationship. Because previous literature has examined
scratching caused by arousal in relation only to negatively arousing stimuli (i.e., anxiety) in
laboratory housed monkeys and apes, I extended the findings on scratching as a behavioral
indicator of anxiety to naturalistically-housed common marmosets. I employed previously used
negative arousal paradigms that have successfully induced scratching in laboratory monkeys and
apes, including predation threat, food competition, and social isolation, to determine if previous
findings concerning scratching generalize to naturally housed New World monkeys. I
hypothesized that, consistent with previous research, marmosets would exhibit increases in
scratching rates in negative arousal contexts as compared to baseline scratching rates (H1).
Additionally, I examined scratching under conditions of positive arousal to determine if
scratching is specific to anxiety (i.e., negative arousal), a question that has not yet been
addressed in the literature. If scratching is primarily a function of the fact that there is greater
right hemisphere activation under conditions of negative (but not positive) arousal (Leavens et
al., 2006), then there would be no reason to expect increased scratching under conditions of
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
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positive arousal. However, if scratching is primarily a function of general physiological arousal,
which occurs in both positive and negative contexts, then scratching might also increase during
positive arousal (RQ1).
Because previous literature has found evidence for lateralized scratching (Hopkins et al.,
2006; Leavens et al., 2004), and because previous studies in our lab have found that subjects
scratch significantly more with their left hand and on their left side in everyday (i.e., not
experimentally controlled) circumstances (Neal et al., 2013), I also examined hand and side
preferences for scratching during both positive and negative arousal conditions. I predicted that
subjects would exhibit greater left hand than right hand scratching during negative arousal (H2).
I had no directional prediction about lateralized preferences in the positive arousal condition
(RQ2).
Lastly, should both negative and positive arousal show increases in scratching, I
predicted that increases in scratching during negative arousal would be greater than increases
during positive arousal (H3). There are greater physiological responses to negative rather than
positive arousal (Jacob et al., 1991; Waldstein et al., 2000), and as such, subjects may exhibit a
similar pattern concerning scratching in negatively versus positively arousing contexts.
Methods
Subjects and Study Site
Subjects were eleven common marmosets (see Table 1 for ages and sexes) housed in
outdoor enclosures at Animal Educators in rural Valley Center, California. One family group
consisted of a mated pair and their offspring, while the other family group consisted of six
siblings. The two family groups were housed separately in 25’x20’x7’ enclosures containing tree
branches, shrubs, platforms, and enrichment items. The marmosets had free access to a heated
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
20
“bedroom,” approximately 2’x3’, that was connected to the main enclosure. A varied diet of
commercial primate food, fruits, and vegetables was provided twice daily along with continually
available fresh water. The marmosets were also supplemented with live invertebrate prey (e.g.,
meal worms) four to five times weekly.
General Procedure
To assess the relationship between scratching and arousal, I observed the marmosets
under three contexts of positive arousal (play, introduction of widely-dispersed high-incentive
foods for foraging and consumption, and anticipation of high-incentive foods) and three contexts
of negative arousal (predation threat, food competition, and social isolation). Using three
different manipulations within the positive and negative arousal conditions allowed me to avoid
habituation and pseudoreplication. I observed the monkeys for 10 minutes prior to any data
collection to ensure that there were no extraneous arousing events (e.g., a coyote in the area)
within 10 minutes of the initiation of a trial.
Prior to the experimental manipulation, I recorded all occurrences of scratching
(including the hand used and the side scratched) by the focal animal for 15 minutes. This served
as the baseline measure. I then recorded all instances of scratching for four minutes in the
presence of the arousing stimulus/event (eight minutes for the social isolation condition—see
below). Based on pilot data and experience with the marmosets, a four-minute time frame
allowed me to record scratching during maximal arousal without either frustrating or habituating
the animals to the manipulation. Following the manipulation period in five of the six contexts, I
recorded all instances of scratching in the focal animal during a 10-minute post-manipulation
period (hereafter referred to as the “post” period). Although no predictions were made
concerning scratching rates during the post period, I was interested in knowing if the scratching
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
21
rates quickly returned to baseline, if in fact the rates did change during manipulation. However,
the post period was not appropriate and was not collected for the food anticipation context (see
explanation below). See Figure 1 for condition breakdown.
A randomized list of focal subjects was developed, and trials were randomized within
focal subjects, although it was not always possible to follow the randomized orders because
various husbandry-related circumstances sometimes prevented a subject or manipulation from
being used that day. Play was recorded opportunistically (see below). Trials took place four-five
days per week, with one or two trials per day per group. When two trials were scheduled for a
given day, one was conducted in the morning and one was conducted in the afternoon. Note that
all of the arousing manipulations are common to the everyday experiences of these subjects. As
such, my methodology did not generate excessive distress. Data collection took place from
August 2013 to March 2014.
Positive Arousal Contexts
Play. I recorded scratching rates during naturally occurring play bouts. In this sense, the
play trials were not “manipulations” but will be referred to as such for ease of description.
Because breeding pairs in marmoset social groups rarely play, I excluded the breeding pair from
play trials. Once a play bout began, I recorded scratching by the focal animal for four minutes,
excluding the time during which the subjects were wrestling, which is incompatible with
scratching due to motor demands. Each subject served as a focal animal in three play bouts.
Because I could not predict when play bouts would occur, pre-play bout scratching
baselines were impossible to obtain. Instead, I recorded scratching using focal all-occurrences
sampling in 15-minute increments on days when no trials were scheduled and when there were
no obvious sources of positive or negative arousal in the groups. Each subject was observed in
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
22
three 15-minute baseline sessions, with each session being on a different day. The average rate of
scratching across these three baseline periods served as the baselines for scratching rates during
play.
High-incentive food foraging/consumption. Kix, Coco Puffs, and Cheerios are highly
palatable and highly sought after food items for the marmosets. To avoid competition for food, I
used a large quantity (the same quantity on each trial) of one of these food items in each trial. I
dispersed the foods throughout the enclosure and all occurrences of scratching exhibited by the
focal animal were recorded. Pilot testing showed that most of the food was found within four
minutes. Each subject served as a focal animal three times.
Food anticipation. A research assistant prepared the subjects’ afternoon meal in front of
the enclosure in view of the subjects. Prior to this experiment, the subjects had learned that, in
the presence of certain cues (the key to unlock the enclosure, a certain food tray, gloves, etc.),
they are about to receive their meal. The presence of these cues during the experimental
manipulation ensured that the marmosets indeed anticipated that I was about to give them the
food, thus eliminating any potential frustration (negative arousal) caused by the inability to
obtain the food. All occurrences of scratching exhibited by the focal animal were recorded for
four minutes. Each subject was observed as a focal animal twice using this manipulation.
During the time that data would have been collected for the post period, the focal was
consuming its meal. Food consumption is a positively arousing context and we would not expect
a return to baseline levels of scratching in that circumstance. Therefore, post period scratching
rates for this context are not considered.
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
23
Negative Arousal Contexts
Predation threat. Common marmosets respond with antipredator behavior to models of
cats (Barros, Boere, Huston, & Tomaz, 2000) and snakes (Clara, Tomasi, & Rogers, 2008;
Hook-Costigan & Rogers, 1998). In addition, we have found in pilot studies that our colonies
respond to models of owls.
A research assistant placed a predator model approximately five feet from the enclosure,
where it was in view of either one or both family groups. I began recording scratching as soon as
the first alarm call was issued. Data were collected for four minutes. Each subject served as a
focal animal three times, one for each predator type (cat, snake, owl).
Food competition. Previous research has found that scratching resulting from social
competition is induced when a limited amount of food is available to a social group (Diezinger,
& Anderson, 1986). Highly palatable food items (roaches, crickets) were held in view of the
focal animal and fed to other members of the family group to induce competition for this limited
food item. Because these foods are highly desirable, competition between group members was
inevitable. The manipulation began as soon as an agonistic vocalization associated with social
competition was issued by any member of the family. All occurrences of scratching exhibited by
the focal animal within the four minute period were recorded. Each subject was observed as a
focal animal three times using this manipulation.
Social isolation. To induce anxiety due to social isolation, one research assistant lured
the focal subject into the bedroom, which was then closed to create full physical and visual
isolation, but not auditory isolation, from groupmates. All occurrences of scratching by the
isolated subject were recorded in real time by a research assistant sitting unobtrusively near the
bedroom enclosure. Focal subjects were isolated for an eight-minute manipulation period, as
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
24
pilot testing had shown that in the first few minutes the focal was unlikely to show signs of
distress such as contact calling. After eight minutes the focal animal was then released back into
the larger enclosure and reunited with the family group. Post manipulation scratching was
recorded for 10 minutes following this initial reunion with the family group. Each subject was
observed as the isolated individual on two occasions using this manipulation.
Analyses
Scratching Rates. Scratching rates are expressed as a number per minute. To obtain this
rate, the total number of scratches was divided by the number of minutes in each period.
Scratching rates were determined for each individual by averaging across trials in all of the
contexts within the positive and negative conditions. That is, for the statistical analyses, each
subject had a scratching rate for positive arousal that consisted of the average rate of scratching
across the play, foraging, and food anticipation contexts in the baseline, manipulation, and post
periods. The same was true for the negative arousal scratching rates, calculated from the
predatory threat, food competition, and social isolation trials. No predictions were made about
possible differences among the three contexts within the positive and negative conditions and
thus post-hoc comparisons were not made unless descriptive statistics revealed meaningful
variability across contexts, which was the case in the positive arousal condition but not the
negative arousal condition (see below).
Statistical tests. Due to a small sample size and non-normal distributions for scratching
rates, bootstrapped paired samples t-tests were used to analyze differences between scratching
rates during baseline, manipulation, and post periods under negative and positive arousal.
Bootstrapped paired t-tests were also used to analyze the difference between the number of left
and right hand scratches under positive and negative arousal.
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
25
Results
See Table 2 for a list of comparisons, mean differences, p values, and confidence
intervals.
H1: Subjects will exhibit increased scratching rates in response to negative arousal as
compared to baseline scratching rates.
Bootstrapped paired samples t-tests were used to analyze the difference between average
baseline, manipulation, and post scratching rates under contexts of negative arousal. Results
showed that subjects exhibited significantly lower scratching rates during the manipulation
period (M = .13, SE = .03) than during baseline (M = .26, SE = .04), p = .002, or during the post
period (M = .29, SE = .04), p = .005. There were no significant differences between baseline and
post scratching rates, p = .125. As Figure 2 shows, subjects showed the same change in
scratching patterns across all three negative arousal contexts. Piloerection (an indication of
arousal due to sympathetic nervous system activity) was recorded as a manipulation check using
a yes/no tally. Results showed that subjects exhibited piloerection in 87% of trials during
manipulation periods in the negative arousal condition. Anecdotally, subjects also exhibited high
rates of locomotion during manipulations, alarm calls were consistently issued by all group
members during predation threat, all focal subjects issued long calls (contact calls) during social
isolation, and chattering was consistently issued during food competition.
H2: Subjects will exhibit more left hand scratching than right hand scratching in response
to negative arousal.
The number of scratches using only the hand during the manipulation period were too
low for statistical analyses (N manipulation = 0 – 14), so hand and foot scratches were
combined, creating a “limb” scratching measure. Total numbers of left and right limb scratches
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
26
were compared in two bootstrapped paired samples t-tests: one for right vs. left limb scratches
during baseline and one for right vs. left limb scratches during manipulation. There were no
significant differences between the numbers of right vs. left limb scratches during either the
manipulation (M right limb = .47, SE = .11; M left limb = .25, SE = .12, p = .11), or the baseline
period (M right limb = 1.80, SE = .30; M left limb= 1.76, SE = .21, p = .83).
It was originally planned that analyses based on computed z-scores for each individual
under the negative arousal condition would be used to further assess differences in left and right
hand/limb scratching. Z-scores for binomial data (z = r(.5N) / √. 25𝑁) reflect the strength of a
left or right bias, with positive numbers indicating a right bias and negative scores reflecting a
left bias. Differences between an individual’s z-scores at baseline and during manipulation might
suggest different patterns of neural activity. However, the low rates of scratching in the
manipulation periods made z-scores unreliable estimates of preference. These scores are
presented in Figure 3.
Research Question 1: Do subjects exhibit higher scratching rates in response to positive
arousal as compared to baseline?
Descriptive statistics revealed that each context under the positive arousal condition
showed a different pattern of results (see Figure 4), and that the data in the play manipulation
were possibly driving the results of the t-tests. Thus, results for each manipulation are presented
separately.
Play. Bootstrapped paired samples t-tests were used to analyze differences in scratching
rates during baseline, manipulation, and post periods. Results showed that rates during the
manipulation (M = 1.15, SE = .19) were significantly higher than rates during both baseline (M =
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
27
.28, SE = .05, p = .008) and post periods (M = .41, SE = .08, p = .001). There was no significant
difference between scratching rates during the baseline and post periods, p = .16.
Foraging. Bootstrapped paired t-tests were used to analyze differences in scratching
rates between baseline, manipulation, and post periods. Results showed that the manipulation
rates (M = .03, SE = .02) were significantly lower than rates during baseline (M = .24, SE = .05),
p = .02. A second bootstrapped paired t-test showed a trend toward lower scratching rates during
the manipulation period than during the post period (M = .27, SE = .08, p = .07). There was not a
significant difference in scratching rates between baseline and post periods, p = .695.
Food Anticipation. A bootstrapped paired t-test was used to determine the difference in
scratching rates between baseline and manipulation. Results showed that manipulation rates (M =
.33, SE = .06) were not significantly different from baseline rates (M = .31, SE = .04), p = .779.
Recall that, during the time that data would have been collected for the post period, the focal was
consuming its meal. Food consumption is a positively arousing context and we would not expect
a return to baseline levels of scratching in that circumstance. Therefore, post period scratching
rates for this context are not considered.
Research Question 2: Do marmosets show a lateralized hand preference for scratching
during positive arousal?
Descriptive statistics showed that the number of scratches using only the hand were too
low for statistical analyses (N manipulation = 0 – 26), so hand and foot scratches were combined
to create a limb scratching measure. Total numbers of left and right limb scratches for each
individual were compared in two bootstrapped paired samples t-tests: one for right vs. left limb
scratches during baseline and one for right vs. left limb scratches during manipulation. Results
showed that subjects exhibited significantly more right than left limb scratches during the
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
28
manipulation period (M right limb = .98, SE = .24; M left limb = .63, SE = .19, p = .025). There
was not a significant difference between left and right limb scratches during the baseline period
(M right limb = 1.98, SE = .26; M left limb= 1.67, SE = .15, p = .30) in the positive arousal
condition.
As was the case with negative arousal, total numbers of scratches with the left and right
limbs were too low to calculate valid z-scores (see Figure 5).
H3: Should subjects show significant increases from baseline in both the positive and
negative condition, I predict that the change will be greater in magnitude in the negative
than positive arousal condition.
In none of the three negative arousal contexts did the subjects show increases in
scratching during the manipulations. In the positive arousal contexts there was an increase in
scratching while playing, a decrease in scratching rates from baseline to manipulation in the
foraging context, and no change from baseline to manipulation in the food anticipation context.
Therefore, no further analyses relative to H3 are warranted.
Discussion
The purposes of the current study were to: 1) generalize previous findings of increased
scratching during negative arousal in laboratory-housed marmosets, Old World monkeys, and
apes to a sample of naturally-housed common marmosets; 2) examine scratching under
conditions of positive arousal to determine if scratching is specific to negative arousal or if it
may be the result of general physiological arousal; and 3) examine hand preferences during
scratching in hopes of elucidating the underlying neural control of scratching. The results are
surprising and provocative.
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
29
Scratching and Negative Arousal
The prediction that subjects would exhibit increases in scratching rates from baseline to
manipulation during the negative arousal condition was unsupported. In fact, data were in direct
contradiction with the hypothesis: subjects from the current study exhibited significant decreases
in scratching rates compared to baseline during all three negative arousal contexts. The facts that:
1) decreases occurred in all three negative contexts; 2) I used manipulations that have been used
in other research; 3) 10 of the 11 subjects demonstrated these decreases; and 4) the monkeys
demonstrated other signs of arousal such as piloerection and agitation, make it unlikely that my
results reflect a statistical aberration, a failure of the manipulations to produce anxiety, or a
methodological flaw.
The discrepancies between previous and current findings raise questions that led me to
re-examine the literature that uses scratching as a measure of arousal or anxiety. One issue that
emerged from this re-examination is that some studies that cite increases in scratching in relation
to anxiety used composite behavioral scores, labeled “self-directed behavior” or “displacement
activity” scores, that lump scratching together with other anxiety-related behaviors (e.g., scentmarking, self-grooming, rubbing, yawning) (Barros et al., 2004, 2007; Dettmer, Novak, Suomi,
& Meyer, 2012; Elder & Menzel, 2001; Judge, Evans, Schroepfer, & Gross, 2011; Leavens et al.,
2004; Manson & Perry, 2000; Schino et al., 1990, 1996). It is possible that one behavioral
measure may have increased while others within the composite score did not change. This can
make it difficult to differentiate between behaviors that are or are not related to anxiety.
When considering only those published studies that explicitly report scratching rates
rather than a composite measure (N= 12 studies), we see that scratching may not have a simple
relationship with arousal (see Table 3). Surprisingly, only six of these twelve studies show
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30
explicit increases in scratching during anxiety-provoking circumstances (video of agonistic
encounters: Hopkins et al., 2006; neighbor vocalizations: Baker & Aureli, 1997; behavioral
transitions: Buckley & Semple, 2012; viewing conspecific in alert posture: Nakayama, 2004;
inter-individual proximity and dominance rank: Pavani et al., 1991; MTS task: Leavens et al.,
2001). Of the other six studies, one shows evidence of increases in scratching in some contexts
but not in others (Diezinger & Anderson, 1986). Three studies show no changes in scratching
during anxiety-inducing circumstances (social crowding: Judge, Griffaton, & Finke, 2006;
intragroup conflict: Aureli, 1997; Duboscq, Agil, & Engelhardt, 2014). Another shows that
common marmosets exhibited no changes in scratching during social isolation or during
administration of an anxiogenic drug even though subjects exhibited concurrent increases in tsik­
eggs calls, which are indicative of anxiety (Kato et al., 2014). Furthermore, although non­
significant, subjects showed decreases in scratching (but increases in tsik and tsik-eggs calls)
during visual presentation of fear-inducing photographs of predatory stimuli (leopard and cat)
compared to the habituation session and sessions of non-picture (gray rectangles) stimuli.
Finally, one study shows increases in scratching during grooming bouts, despite the fact that
grooming is generally associated with states of low anxiety (Semple, Harrison, & Lehman,
2013).
The authors of these particular studies explain their unexpected scratching data in
different ways. For example, Judge et al. (2006) found that hamadryas baboons (Papio
hamadryas) showed no changes in post-crowding rates of scratching compared to baseline rates;
however, rates of other displacement activities (i.e., yawn, self-groom, and pace) did increase
significantly during post-crowding compared to baseline. The authors stated that the behavioral
mechanisms used by subjects during crowding were effective in reducing social tension to the
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
31
point that scratching did not increase. Aureli (1997) found that post-conflict scratching rates in
long-tailed macaques did not differ from matched control rates when analyzed across the full
duration of the experimental timeline. However, the authors noted that there were certain time
periods within the full trial where scratching increased. By focusing on those time periods that
showed the predicted relationship between scratching and anxiety, they rescued the expected
effect. Similarly, Diezinger & Anderson (1986) found that dominant, subordinate, and immature
macaques exhibited no changes in scratching between baseline and feeding competition, but
because the monkeys of intermediate rank did show the expected effect, the other data were
largely ignored in the conclusion. Duboscq, Agil, & Engelhardt (2014) examined natural
agonistic encounters between female crested macaques (M. nigra) and found no difference
between baseline and post-conflict mean scratching frequency. They explained their findings by
stating that the anxiety-scratching relationship may be weak in such a “tolerant” species. Lastly,
Semple, Harrison, & Lehmann (2013) found that scratching rates after grooming bouts in female
Barbary macaques (M. sylvanus) dramatically increased compared to baseline. As mentioned
above, grooming typically reduces anxiety and has been shown to correlate with decreases in
self-scratching in other studies (Maestripieri, Schino, Aureli, & Troisi, 1991; Troisi, 2002). The
authors stated that certain unmeasured conditions in the study (e.g., signaling of relationships to
group members though grooming, termination of grooming, behavioral transitions) may have
increased anxiety, causing increases in scratching rather than decreases.
A handful of studies with marmosets show very distinct increases in scratching when
subjects are given anxiogenic drugs (but see Kato et al., 2014) and decreases in scratching when
subjects are given anxiolytics (Barros et al. 2000; Cilia and Piper, 1996; Schino et al., 1991,
1996). However, we should be circumspect in our interpretation of these results, as the
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
32
physiological and cognitive side effects of such drugs may influence scratching independently of
changes in anxiety. It has been argued that decreases in scratching are not simply a by-product
of the muscle-relaxing and sedative properties of benzodiazepines because some studies have
found decreases in scratching during administration of anxiolytics without concurrent decreases
in locomotor activity (Schino et al., 1991, 1996). However, decreases in scratching have also
been observed with concurrent and significant decreases in locomotor activity during
administration of diazepam (Barros et al., 2000; Cilia & Piper, 1996). Side effects of
benzodiazepines, such as alterations in cutaneous sensitivity, behavioral inhibition, and
avoidance responses, may also influence scratching rates. In short, caution should be applied
when examining and interpreting the anxiety-scratching relationship found in drug studies.
The failure to reliably uncover a positive relationship between scratching and anxiety is
also reflected in the literature on scratching and cortisol. For example, Higham et al. (2009)
observed overall levels of SBDs (including scratching) and found no correlation with fecal
glucocorticoid levels in female baboons. Additionally, Elder and Menzel (2001) found a negative
correlation between SDBs and cortisol levels in orangutans during computerized tasks. The
authors explain this by stating that engaging in SDBs may have released the frustration caused
by the task, thus reducing cortisol release, or possibly that there may be a distinction between
stress and anxiety, such that cortisol release is related to stress, whereas SDBs are related to
anxiety. However, they also point out that the frustration may not act on brain regions associated
with the HPA axis, and thus, SDBs may not be related to cortisol levels in general.
It is possible that the widespread belief in primatology that scratching is a very reliable
measure of negative arousal/anxiety has made that relationship a foregone conclusion, such that
any empirical deviations from that relationship are either ignored or explained away. My data,
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
33
and data in published studies that, upon close examination, fail to confirm the relationship,
suggest that scratching does not always increase with arousal, and that the assumption of the
relationship prevents us from asking a much more interesting set of questions about what
scratching tells us about underlying physical and emotional states. Furthermore, using scratching
as a de facto indication of anxiety could lead to incorrect conclusions that misinform not only
theory, but also decisions about captive animal welfare.
Accounting for the variability. Assuming that the manipulations did indeed cause
arousal in the studies cited above and in my own study, what might be the factors that account
for the variability we see in the scratching-arousal relationship? One possibility is that degree or
intensity of arousal is important, but studies have not reported (and probably have no way to
measure) the extent to which their subjects were aroused. In fact, Troisi et al. (1991) suggested
that scratching and anxiety may be related in an inverse-U fashion, with high levels of scratching
being expressed only during moderate levels of anxiety, and low levels of scratching being
expressed during low and high levels of anxiety. Additionally, it could be that any change in
scratching from baseline is important; that is, the specific direction of change is not as important
as the change itself. Indeed, any alteration in the cortisol response (a measure of stress) is
considered detrimental on health outcomes, regardless of the direction of the alteration (e.g.,
whether the cortisol pattern is blunted or highly increased compared to baseline patterns)
(D’Anna et al., 2012). It may also be important to examine the possibility of transient changes in
scratching throughout manipulation periods by examining scratching minute-by-minute during
anxiety-provoking circumstances, as different rates of scratching can be exhibited throughout
exposure to a stressor (Aureli, 1997). Additionally, Barros et al. (2004) point out that it may be
especially important to dissociate fear and anxiety when measuring scratching, as anxiety-related
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
34
behaviors, including scratching, tend to decrease when fear-related behaviors increase (freezing,
withdrawal). A second possibility is species differences in the physiological mechanisms (see
below) that underlie the arousal-itch-scratch pathway. Third, monkeys tested in social groups
may experience and therefore express arousal differently than monkeys tested alone. There is
evidence for a social buffering effect that reduces HPA activity in marmosets (Cross & Rogers
2006; Smith, McGreer-Whitworth, & French 1998), but whether or not it affects how anxiety is
expressed is not known. Similarly, housing conditions (indoor, outdoor, pair housing, natural
social groups, etc.) and the subjects’ experience with experimental manipulations of various sorts
may influence scratching in ways we do not yet understand. Furthermore, the type of
circumstance used to create arousal might be of importance in explaining the variability across
studies. Studies showing increased arousal-related scratching in great apes often utilized non­
social contexts, including cognitive challenges such as match-to-sample tasks, to induce anxiety
or frustration in subjects (Elder & Menzel, 2001; Leavens et al., 2001, 2004). These types of
computerized tasks are very different from the more naturally-occurring situations used in the
current study to induce negative arousal, such as food competition, social isolation, and predation
threat. It is intriguing that the studies reported above that showed no change or a decrease
(including the current study) in scratching took place in more naturally-occurring contexts, such
as crowding (Judge et al., 2006), agonistic encounters (Aureli, 1997; Duboscq et al., 2014), and
competition for food (Diezinger & Anderson, 1986).
Lateralized preferences while scratching in negative arousal. Because scratching
decreased to such low levels during manipulations, there was not an adequate number of left and
right limb scratches to calculate valid z-scores. Therefore, it is not possible to speculate about
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
35
lateralized scratching preferences, and thus, emotional lateralization during negative arousal,
using data derived from this study.
Scratching and Positive Arousal
To examine if scratching is related to both negative and positive arousal, I recorded
scratching rates during three positive arousal contexts. Each of the three positive arousal contexts
showed a different pattern of scratching rate results. During the play condition, subjects
exhibited significantly higher rates of scratching during the manipulation period than during
baseline and post periods. Subjects showed no significant changes in scratching rates during food
anticipation condition, and significantly lowered their scratching rates during the foraging
manipulation.
Given the surprising result regarding scratching and negative arousal, and the fact that
those data call into question some basic assumptions about scratching and arousal, the data for
the positive arousal condition do not allow for simple interpretation. Nonetheless, to the extent
that scratching has a (complicated) relationship with arousal, the observed variability of
scratching rates across the three positive arousal conditions suggest different types or levels of
excitement in each of the three contexts. The one context, whether it be positive or negative, that
elicited significantly higher rates of scratching during manipulation was social play. Play is a
highly energetic, explicitly social, and cognitively challenging event whose causes and long-term
consequences are not well understood. It is also the case that play was the one condition in my
study that was not manipulated experimentally. Therefore, it is not clear if play represents a
truly unique context with regard to understanding arousal and scratching, but future studies
might benefit from exploring this possibility.
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
36
Lateralized preferences while scratching in positive arousal. As a second research
question, I examined scratching hand preferences during positive arousal. Because the positive
arousal contexts showed a different pattern of scratching rate results, the positive arousal data
concerning lateralized scratching should be interpreted with caution. Additionally, although
scratching rates under the positive arousal condition did not decrease significantly, overall
numbers of scratches were low, and thus, z-scores computed may not be valid. In any case, four
individuals exhibited a number of scratches that may yield valid z-scores. Three of these
individuals exhibited no significant change in their z-scores from baseline to manipulation, and
one subject exhibited a switch from significantly right handed scratching during baseline to
significantly left handed scratching during manipulation. However, the low overall number of
subjects as well as low numbers of scratches makes it difficult to draw conclusions concerning
lateralized scratching during positive arousal.
Underlying Mechanisms that May Produce Scratching
If we are to fully understand the relationship between scratching and arousal, we must
identify the physiological mechanisms that underlie scratching as a self-directed behavior. These
mechanisms have not been identified. It is difficult to explain why subjects do not scratch when
we do not understand why they do scratch.
There are a number of well-known neurochemicals that are associated with pain, itch,
anxiety, and/or stress that might help us understand the pathway to the scratch response. For
instance, Substance P (SP) is involved in pain and itch, as well as anxiety regulation. Studies
have found that, depending on the dose and brain area, injection of SP can have either anxiogenic
or anxiolytic effects, while other studies have found that anxiety-provoking stimuli can cause
increases in SP in various brain areas (Barros et al., 2002; Ebner & Singewald, 2006). Given SPs
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
37
importance in both anxiety regulation and pain and itch transmission, and the fact that it can have
differential effects on anxiety, it is possible that SP has a role in regulating different levels or
types of anxiety, and this may be reflected in the expression of anxiety-related behaviors.
Second, oxytocin is related to social bonding and affiliative behavior, and has been
implicated both agonistically and antagonistically with anxiety and the HPA axis. Recent studies
have found that increases in oxytocin can increase stress-enhanced fear responses in mice and
humans (Guzman et al., 2013; Theodoridou, Penton-Voak, & Rowe, 2013), whereas others have
found that oxytocin administration reduces anxiety behavior in rats when tested in an unfamiliar
environment (Windle, Shanks, Lightman, & Ingram, 1997). When highly social species
experience the stressor in the social group, oxytocin may be found in higher concentrations
relative to other species used in previous studies, which may change fear and anxiety-related
responses (such as scratching).
Lastly, enkephalins are involved in pain inhibition, and possibly itch induction.
Enkephalin is largely involved in inhibiting pain messages both centrally and peripherally.
Additionally, pain and itch have an antagonistic relationship, such that increasing pain messages
inhibits itch, and decreasing pain messages (e.g., taking opioids) often has the side effect of
increasing itch (Ikoma, Steinhoff, Yosipovitch, & Schmelz, 2006; Ward, Wright, & McMahon,
1996). However, other studies have posited that the same inhibition pathway for pain (involving
enkephalins) may also be involved in inhibiting itch (Mochizuki et al., 2003). Given that we do
not understand the full extent of the physiological relationship between inhibition of pain and
itch, it is difficult to say whether enkephalin (which, again, is involved in pain inhibition) may
increase or decrease itch. It is possible, and even likely, that SP, oxytocin, and enkephalins are
all involved in itch and anxiety-related scratching, but how these might fit together to explain
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
38
species and context-dependent differences in anxiety-induced scratching remains to be
determined. Furthermore, it is unclear if anxiety-related scratching in primates reflects a
perception of “itchiness” at all; scratching may be independent of the “itch” sensation and thus
may not benefit from an understanding of a true “itch” sensation.
Conclusion
The current study showed that common marmosets did not exhibit the same pattern (in
fact, an opposite pattern) of scratching as has been commonly reported in nonhuman primates
under conditions of negative arousal. My data, and patterns that are revealed in a careful
examination of the literature, suggest that the anxiety-scratching relationship may be more
complex than typically reported and assumed. Furthermore, the relationship between scratching
and states of positive arousal need further investigation, both to elucidate the similarities and
differences between these two emotional states and to further examine the scratch-arousal
association. In addition to the theoretical questions they pose, my results raise a potential concern
about the use of scratching as an unqualified indicator of anxiety and well-being in captive non­
human primates, with important implications for captive management.
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
39
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SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
52
Figures and Tables
Table 1
Name, Age, Sex, and Group Number for Individual Subjects
Name
Age (months)
Sex
Ringo
12
M
George
12
M
William
30
M
Harry
30
F
Beatrice
18
F
Genie
18
M
Alfred
60
M
Annie
56
F
Achilles
30
M
Athena
30
F
Apollo
18
M
Group
1
1
1
1
1
1
2
2
2
2
2
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
Positive Arousal
Condition
Food Anticipation
Foraging
Contexts
Trials
Play
Kix
Cheerios
Coco
Puffs
Trial 1
Trial 2
Trial 1
Trial 2
Trial 3
Base.,
Manip.,
Base.,
Manip.,
Base.,
Manip.,
Base.,
Manip.
Base.,
Manip.
Base.,
Manip.,
Base.,
Manip.,
Base.,
Manip.,
Post
Post
Post
Post
Post
Post
Negative Arousal
Condition
Contexts
Trials
53
Predation Threat
Social
Isolation
Food competition
Snake
Owl
Cat
Roaches
Crickets
Mealworms
Trial 1
Trial 2
Base.,
Manip.,
Base.,
Manip.,
Base.,
Manip.,
Base.,
Manip.,
Base.,
Manip.,
Base.,
Manip.,
Post
Post
Post
Base.,
Manip.,
Post
Post
Post
Base.,
Manip.,
Post
Post
Figure 1: Breakdown of positive and negative arousal conditions.
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
54
Table 2
Comparisons and Respective Statistics from the Current Study
Comparison
H1: Negative arousal
scratching rates
H2: Negative arousal right
vs. left limb scratching
Food
anticipation
Foraging
RQ1: Positive
arousal
scratching
rates
Baseline vs.
Manipulation
Manipulation vs.
Post
Baseline vs. Post
Baseline right vs.
left
Manipulation right
vs. left
Baseline vs.
Manipulation
Baseline vs.
Manipulation
Manipulation vs.
Post
Baseline vs. Post
Mean
difference
p
95 % CI of Mean
difference
0.13
.002
[0.06 , 0.19]
-0.16
.005
[-0.27, -0.06]
-0.04
0.05
.125
.83
[-0.09, 0.01]
[-0.41, 0.51]
0.22
.11
[-0.6, 0.51]
-0.02
.779
[-0.14, 0.10]
.21
.02
[0.13, 0.29]
-0.24
.074
[-0.41, -0.10]
-0.04
.695
[-0.20, 0.08]
Baseline vs.
-0.87
.008
[-1.25, -0.46]
Manipulation
Play
Manipulation vs.
0.73
.001
[0.42, 1.04]
Post
Baseline vs. Post
-0.13
.16
[-0.29, 0.03]
RQ2: Positive arousal right
Baseline right vs.
.31
.30
[-0.32, 0.94]
vs. left limb scratching
left
Manipulation right
0.36
.025
[0.06, 0.66]
vs. left
Note. df (degrees of freedom), t (t-value), p (p-value), 95% CI of the Mean difference (95%
Confidence Interval of the Mean difference).
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
55
0.4
Scratching rate / minute
0.35
0.3
0.25
Predation Threat
0.2
Food Competition
0.15
Social Isolation
0.1
0.05
0
Baseline
Manipulation
Time Period
Post
Figure 2: Baseline, manipulation, and post scratching rates for the three negative arousal
conditions.
2.5
2
1.5
1
0.5
0
(-) baseline
(-) manipulation
-0.5
-1
-1.5
-2
Figure 3: Scratching z-scores for each individual during baseline and manipulation time periods
in negative arousal. Apollo, Beatrice, and George had z-scores of 0 (equal numbers of
scratches by the left and right limbs) during manipulation. Two subjects did not scratch
during the manipulation period, and are therefore not included on this figure.
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
56
Scratching rate / minute
1.4
1.2
1
0.8
Food Anticipation
0.6
Food Forage
0.4
Play
0.2
0
Baseline
Manipulation
Time Period
Post
Figure 4: Scratching rates during baseline, manipulation, and post periods in the three positive
arousal conditions.
2.5
2
1.5
1
0.5
0
-0.5
(+) baseline
(+) manipulation
-1
-1.5
-2
-2.5
Figure 5: Scratching z-scores for each individual during baseline and manipulation time periods
in positive arousal. George had a z-score of 0 (equal numbers of left and right limb
scratches) during baseline, and Ringo had a z-score of 0 during manipulation. One
subject (Annie) exhibited no scratching during manipulation, and thus does not appear on
this figure. Because the positive arousal contexts showed a different pattern of scratching
rate results, these positive arousal data concerning lateralized scratching should be
interpreted with caution.
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
57
Table 3
Studies that Explicitly Report Scratching in a Non-Composite Measure
Authors
N and
Manipulation
Results
Authors’ Explanation of
(year)
Species
and Measures
Results
Baker &
Aureli
(1997)
Buckley &
Semple
(2012)
81
chimpanzees
Scratching
assessed before
and after
anxietyinducing
neighbor
vocalizations.
17 ring-tailed Scratching
lemurs
assessed before
and after
anxiety caused
by behavioral
transitions*.
Rough and gentle
scratching
increased after
vocalizations
compared to before
vocalizations.
Authors state that results
are consistent with
previous research
showing that anxiety
and scratching are
related.
Scratching
increased both
before and after
behavioral
transitions.
Displacement activities
(e.g., scratching) may
serve as method to allow
animals to divert
attention from previous
activity to next
activity/stimulus.
1) Behavioral transitions
are anxiety-provoking,
as evidenced by
increased scratching
rates. 2) During feeding
contexts, scratching may
be considered a
displacement activity, as
an increase in scratching
in intermediates may be
due to frustration from
attempts to obtain food,
whereas dominant and
subordinate individuals
do not experience this
frustration, and thus, do
not scratch.
Authors addressed
results in context of
lateralized preferences.
Diezinger
&
Anderson
(1986)
14 rhesus
macaques
Scratching
assessed at
baseline and
after 1)
behavioral
changes*, and
2) feeding
contexts.
Scratching 1)
increased during
behavioral changes,
and 2) was higher
only in
intermediates
during feeding
times compared to
baseline (i.e., no
change in
scratching from
baseline to feeding
contexts in
dominants,
subordinates, or
immature subjects).
Hopkins,
Russell,
Freeman,
Reynolds,
Griffis, &
Leavens
(2006)
89
chimpanzees
Scratching
assessed at
baseline and
while subjects
watched video
of conspecific
agonistic
encounters.
Scratching
increased while
watching video
compared to
baseline.
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
Judge,
Griffaton,
& Fincke
(2006)
9 Hamadryas
baboons
Scratching
assessed at
baseline,
during induced
crowding, and
post crowding.
No difference in
scratching between
baseline,
manipulation, and
post measures.
Duboscq,
Agil, &
Engelhardt
(2014)
140 female
crested
macaques
Scratching
assessed at
baseline and
post conflict
and
reconciliation.
No difference in
scratching between
baseline and post­
conflict.
58
Authors stated that
behavioral mechanisms
used by subjects during
crowding were effective
in reducing social
tension to the point that
scratching did not
increase.
Three possibilities were
presented in the
discussion. 1) This is a
“tolerant” species of
macaque. Post-conflict
interactions may serve a
different function
compared to other
macaques/other species
with despotic
individuals, and thus, it
is possible that
scratching-anxiety
relationship is weak in
tolerant species.
2) Subjects were “too
busy” to scratch. 3)
Conflict must not have
been perceived by
subjects as very risky or
costly given their lack of
expression of anxietyrelated behaviors.
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
Semple,
12 female
Harrison, & Barbary
Lehman
macaques
(2013)
Scratching
assessed at
baseline and
while subjects
gave or
received
grooming.
Scratching
increased after
grooming bouts.
59
Authors rejected idea
that self-scratching may
not be indicator of
anxiety due to results
from previous studies
with the same
population of subjects
showing increases in
scratching. They explain
the findings by stating
that other situations that
cause increases in
scratching (e.g.,
behavioral transitions)
may have been present
to the extent that they
overrode any decreases
in scratching caused by
grooming. Grooming
may also be anxietyprovoking because it
signals to other
members certain
preferences for
individuals and
relationships, and may
also represent ending of
a rewarding experience,
which would cause
frustration/anxiety.
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
Aureli
(1997)
31 longtailed
macaques
Scratching
assessed postconflict and in
matched
control
observations.
Kato et al.
(2014)
6 common
marmosets
Grooming
(episodes of
scratching)
assessed in
three fear and
anxietyinducing
paradigms:
isolation,
anxiogenic
administration,
visual
presentation of
predator
pictures.
Post-conflict
scratching did not
differ from
scratching in
matched control
observations when
assessed during the
entire time period.
However, when
first the three
minutes were
analyzed
separately, postconflict rates were
higher than
matched control
rates.
No differences in
scratching across
five isolation
sessions, no
significant
difference in
scratching in the
anxiogenic
administration
sessions, non­
significant decrease
in scratching during
presentations of
pictures of
predators.
However, subjects
did show increased
tsik-eggs calling in
each condition,
indicative of
anxiety.
60
Authors stated that the
disturbance of a
valuable relationship
due to previous conflict
is the major cause of
post-conflict anxiety.
Authors did not address
findings concerning no
changes in scratching.
Scratching results were
not addressed in the
discussion, as the focus
of the study was
vocalizations.
SCRATCHING IN POSITIVE AND NEGATIVE AROUSAL
Leavens et
al. (2001)
8
chimpanzees
Nakayama
(2004)
5 Japanese
macaques
Pavani et
al. (1991)
8 long-tailed
macaques
Gentle and
rough
scratching
assessed
during Match­
to-Sample
(MTS) task in
easy and hard
conditions.
Scratching
assessed while
subjects
watched a
monkey
monitoring a
third monkey
that was a
stranger to all
other monkeys:
stranger, and
no stranger
conditions.
Scratching
assessed
during interindividual
proximity and
measured in
relation to
dominance
rank.
Gentle scratching
increased when
subjects were
presented with easy
condition first
compared to when
subjects were
presented with hard
condition first.
Subjects who
viewed the
monitoring monkey
in an alert state
(i.e., during the
stranger viewing
condition) were
more likely to
scratch than during
no stranger
condition.
Monitoring monkey
also showed
increased
scratching in
stranger than no
stranger condition.
Scratching was
higher during close
proximity to males
compared to alone.
Scratching was also
higher in
subordinates than
high-ranking
individuals.
61
Authors state that these
results are consistent
with the idea that
scratching increases
when subjects are
anxious or frustrated.
Authors state that this
shows a contagion of
scratching in conspecific
observers who
experience negative
arousal along with the
monitoring monkey.
This is indicative of a
transmission of negative
arousal.
Authors state that their
results are consistent
with the idea that
proximity and lower
rank creates anxiety due
to internal conflict
arising from possibility
of agonistic encounters
and constrained
behavioral options of
subordinates.
Note. Behavioral change/behavioral transition refers to scratching episodes occurring in a
social context with a subsequent change in behavior; for example, scratching occurring
between a change in behavior from grooming a conspecific to foraging.