Magazine
R649
Why some bird
brains are larger
than others
Fahad Sultan
How does brain size and design
influence the survival chances of a
species? A large brain may
contribute to an individual’s
success irrespective of its detailed
composition. I have studied the
size and shape of cerebella in
birds and looked for links between
the bird’s cerebellar design, brain
size and behavior. My results
indicate that the cerebellum in
large-brained birds does not scale
uniformly, but occurs in two
designs. Crows, parrots and
woodpeckers show an
enlargement of the cerebellar
trigeminal and visual parts, while
owls show an enlargement of
vestibular and tail somatosensory
cerebellar regions, likely related to
their specialization as nocturnal
raptors. The enlargement of
specific cerebellar regions in
crows, parrots and woodpeckers
may be related to their repertoire
of visually guided goal-directed
beak behavior. This specialization
may lead to an increased active
exploration and perception of the
physical world, much as primates
use of their hands to explore their
environment. The parallel
specialization seen in some birds
and primates may point to the
influence of a similar neuronal
machine in shaping selection
during phylogeny.
The cerebellum is a highly
conserved part of the brain
present in most vertebrates [1],
well suited for a comparative
study of size and design. The
cerebellum in birds, as in
mammals, consists of a strongly
folded, thin sheet of gray matter,
located dorsally to the brainstem.
In birds, it largely consists of a
single narrow strip that varies in
different species in the anteroposterior extension, which
corresponds to the cerebellar
length. The cerebellum of birds is
growth pattern and scored highly
on the second PC. Both PCs
together explained 66% of the
total variance (first PC, 44%;
second PC, 22%). The cerebellar
growth of the first group is based
on the enlargement of Larsell’s
lobuli IV and VI–IX, while in the owl
group lobuli I–II and X increase in
size (Figure 2A,B). The difference
in enlargement of these two
groups of lobuli in the two groups
of birds, i.e., crows, parrots and
woodpeckers versus owls was
statistically significant (Figure 2C).
The following groups of
cerebellar lobuli can be related to
functional subdivisions through
their afferents: somatosensory
(tail, III–IV; leg, IV–V; wing, IV–VIa;
head, V–VII and VIIIb–IXa) [3,4],
visual (VIc–IXc) [5,6], auditory
(VII–VIII) and vestibular (IXd–X) [7].
My analysis indicates that, in the
diurnal bird group (crows, parrots
and woodpeckers), the cerebellar
regions that receive visual and
trigeminal inputs show the
commonly subdivided into ten
groups of folds termed lobuli [2].
Both variability and regularity are
evident in the lobular pattern of
the bird cerebella. To quantify
these structural varieties and
relate them to functional or
phylogenetic differences, a
principal component analysis was
performed on the residuals of the
lobuli length, obtained from a
double-logarithmic regression of
lobuli length against body size
(see Supplemental Data on-line for
further details).
Generally, birds within a family
(Figure 1) tended to score similarly
on the two principal components
(PCs). The variability in the
principal plane is dominated by
variability between bird families
(one-way ANOVA with bird family
as factor: F(23, 24) = 4.59,
p < 0.001). The group of birds that
scored highly on the first PC
consisted of crows, parrots and
woodpeckers. In contrast, the
nocturnal owls had a different
Long-eared owl
2
51
Short-eared owl
50Barn owl
51
Cormorant Robin
8 Great horned owl
Lovebird
90 128
80
45
123
51 134
74
Flamingo
126
Partridge
123
128 Buzzard
Raven
60
Falcon
8
83 93
Eurasian jackdaw
60
85
8283
145 74
82
14
132
Macaw
Rock dove
Common gull
60
45
2
Herring gull 82 123
123
Carrion crow
Black-headed gull
14
14 1
82
17
Phalarope
14
74
Green 17
Great spotted
woodpecker
Hummingbird
woodpecker
48
Wild turkey
Common swift
Pheasant
Second principal component
Correspondence
1
0
–1
–2
46
8
–2
–1
0
1
First principal component
2
Current Biology
Figure 1. Multivariate analysis of cerebellar lobuli lengths in birds obtained from line
drawings in [2,10] (see Supplemental Data for further details).
The graph plots scores of the individual birds on the first two PCs. The two PCs explain
66% of the variance (PC1, 44%; PC2, 22%). The largest variation along the first PC is
between the woodpeckers, crows and parrots on the one hand, and the pheasants
(Partridge and Wild turkey) on the other. Owls loaded high on the second PC, while
swifts and hummingbirds loaded low. Generally, birds were clustered according to their
family grouping as seen in the owls (#51), ducks (#14), pigeons (#60), woodpeckers
(#17), crows (#123), parrots (#45), and gulls (#82). A one-way factorial ANOVA showed
a statistically significant effect of family grouping as a factor on the overall variance (Fratio 4.59, p < 0.001). Two species, the barn owl and mallard, were present in both
sources [2,10] and are plotted with interconnected dashed lines. Two individuals of the
rock dove were present in [10] and are also plotted separately and interconnected by a
dashed line. (Numbering of bird families taken from [11] and listed in Table S1 in Supplemental Data.)
Current Biology Vol 15 No 17
R650
Second principal component
A
1.0
II
I
X
0.8
0.6
III
0.4
V
0.2
IV IX
VIII
0
VIVII
0
0.2
0.4
0.6
0.8
1.0
First principal component
B
VI
VII
VIII
V
IX
IV
III
II
X
long-eared owl
VI
I
VII
VIII
V
IV
III
green woodpecker
IX
II
I X
Residuals lobuli length
to body weight
C
0.3
**
***
0.2
0.1
0
–0.1
lobuli I, II & X
lobuli IV, VI-IX
Owl families
Crow, Parrot and
Woodpecker families
Current Biology
Figure 2. Two groups of lobuli contributing
to different growth patterns in birds.
(A) Loadings of the individual lobuli on the
first two PCs. Evident are two groups:
lobuli IV, VI–IX load strongly on the first
PC, while lobuli I, II and X load on the
second PC. (B) Two birds with roughly
equal body size that correlate with the
two groups of lobuli are shown (longeared owl, 276 g; green woodpecker,
195 g). In (A,B) contributions of the lobuli
to the two first PCs are color coded: red
codes first PC, blue second PC. (C) Comparison of the residuals of the two lobuli
groups in the owl and in the crow, parrot
and woodpecker group. The summed
length of the lobuli that loaded highest on
either the first or second PC were taken
(PC1, IV, VI–IX; PC2, I, II and X) and the
residuals to body weight were calculated.
Residuals from birds (n = 12) from families
that loaded strongly on either the first
(crows, parrots and woodpeckers) or
second PC (owls) were taken. The difference between these bird groups were
statistically significant (t test for lobuli IV
and VI–IX: p < 0.001, df = 10; lobuli I, II
and X: p < 0.01, df = 10). Error bars: ±SD.
Bird drawings taken from [12].
greatest growth, while in the
nocturnal owl’s group the
vestibular and tail somatosensory
receiving regions show the
greatest enlargement. The lobuli
that are enlarged in crows, parrots
and woodpeckers (IV and VI–IX)
contribute to about 73% of the
overall cerebellar length in birds.
Not surprisingly, the birds that
have enlarged this part of the
cerebellum also have the longest
cerebella — normalized for their
body weight. The residuals of total
cerebellar length in the crow,
parrot and woodpecker families
were significantly larger than those
for the owl families (0.15 ± 0.04
compared to 0.04 ± 0.07, t test
p < 0.01, df = 10).
One unexpected observation
was that in excellent flyers only
the buzzard scores positively, and
that several birds with excellent
flying capabilities like the swift
and falcon score negatively in the
principal plane (Figure 1). This
implies that well-developed motor
skills per se do not require a large
cerebellum, contradicting the
common idea that cerebellar size
increase in birds is mainly linked
to their flying capabilities.
What could be the behavioral
denominator common to crows,
parrots and woodpeckers that is
not developed in owls? All of
these birds also have large brains;
however, their cerebellar designs
differ arguing against a simple coenlargement model [8]. The
enlargement of specific visual and
beak-related cerebellar parts in
crows, parrots and woodpeckers
fits well with their marked
adeptness in using their beaks
and/or tongues to manipulate and
explore external objects. Their
skills are even comparable to
those of primates in using their
hands [9]. The tight temporal
coupling between motor
command, expected sensory
consequences and resulting
afferents during visually guided
hand and beak usage may be the
reason why these animals need
large cerebella. The comparative
analysis of the birds cerebella
reveals that some brains may
have enlarged to solve similar
problems by similar means during
phylogeny. Furthermore it shows
that large brains have a specific
architecture with dedicated
building blocks.
Supplemental data
Supplemental data including
experimental procedures are available at
http://www.currentbiology.com/cgi/content/full/15/17/R649/
DC1/
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Department of Cognitive Neurology,
Hertie-Institute for Clinical Brain
Research, University of Tuebingen,
Otfried-Mueller-Strasse 27, 72076
Tuebingen, Germany.
E-mail: [email protected]