Les différences
cérébrales apportées par
l'évolution entre deux espèces
proches et à la base de comportements
congénitaux divergents n'ont jamais,
jusqu'à présent, été
élucidées. Cette étude
porte sur une association comportementale:
chants, hochement de tête et
bâillements chez le poulet et la
caille. Ce travail rapporte les
expérimentations basées sur des
transferts d'une espèce à l'autre
de greffes cérébrales
localisées et les modifications
comportementales ainsi induites !
Congenital species differences in behavior are
those that persist when different species are
reared in similar environments. Despite recent
progress in understanding both the mechanisms of
vertebrate neural development and changes in
developmental processes that could yield major
morphological differences in brain size and the
organization of brain areas, evolutionary
changes in more subtle features underlying the
striking differences seen in congenital
behaviors among species with similar brain
architecture remain to be explained.
Species differences in complex behavioral
acts could result from several alternative
mechanisms. Most simply, they could be produced
by changing the features of cells within a
single, higher brain area that generates motor
patterns or coordinates the activity of various
behavioral components into a unified whole.
Alternatively, there could be independent
changes to different, lower brain areas more
involved with modulating the fine details of the
different components of a complex motor act.
This latter possibility seems more difficult to
achieve because it requires independent changes
at different brain locations. Finally,
behavioral differences could result from a
combination of evolutionary changes to both
types of brain areas. Recent techniques for
creating surgical brain chimeras between avian
species that can hatch and behave normally have
made it possible to study this question
empirically, using a vocal behavior called
crowing. Crowing is a complex but relatively
stereotyped hormone-dependent vocalization
delivered by adult male gallinaceous birds.
Crowing and other patterns of adult male sexual
behavior can be induced in juvenile males and
females within a few days of hatching by
administration of the steroid hormone
testosterone. The structure of juvenile crows is
stable within individuals, and although each
individual has a unique crow, there is a great
resemblance among the crows of different animals
within a species.
Single chicken and quail crows differ
reliably in two parameters: their sound pattern
and the pattern of head movement given during
their delivery. Chicken crows generally have a
single part (some individuals have an
interruption of airflow in this single part,
which disappears with age), and except for a
tendency to dip their head slightly at the
beginning of sound production, chickens do not
have any consistent movement of the head in the
vertical plane at frequencies .4 Hz during
crowing. Quail crows have two or three parts
with very distinctive temporal relationships
among them. They also have a distinctive pattern
of amplitude and frequency modulations in the
final part of the crow. Quail rapidly bob their
heads up and down at frequencies of 4Ð20 Hz
during crowing, in synchrony with these
amplitude and frequence modulations. Both quail
and chickens have a large amplitude deflection
of the head up and forward preparatory to
crowing that has varying kinetics within and
between individuals; the quail head bobs are
superimposed on this larger amplitude head
movement. Quail do not produce such head bobs
when giving other vocalizations in their vocal
repertoire. Species differences in acoustical
and gestural aspects of crowing do not appear to
be influenced by imitative learning.
In a previous study, it was found that the
acoustical temporal pattern characteristic of
quail crowing can be transplanted into chickens
when the quail donor portion includes the
primordium of the midbrain. The present study
began by examining videotaped records of two of
these animals to ascertain their pattern of head
movementAs a control for general behavioral
abnormalities in the head movement of chimeras,
yawning, part of the normal behavioral
repertoire of both chicks and Japanese quail,
was recorded. During yawning in both species,
the neck is stretched vertically and the upper
mandible is raised upward; the head follows the
same overall trajectory as the low frequency,
high amplitude head movement preparatory to
crowing in both chickens and quail. This is
followed by swallowing and closing the bill.
Yawning is not usually accompanied by any
sound in either species. As an additional
surgical control, chickenÐchicken
transplants were carried out to assess the
effects of surgical intervention on head
movement. None of the chickenÐchicken
chimeras showed any differences in crowing, head
movement, yawning, or any other obvious
behavior from unoperated chickens. Thus, the
behavioral effects described below are not
attributable to surgical procedures.
[•••]
DISCUSSION : The experiments reported
here are not primarily concerned with
elucidating the involvement of separate brain
areas in the different, coordinated components
of a single behavior. This is a well documented
phenomenon for many behaviors, including bird
song. The focus is rather on the localization of
functional differences in the brains of these
two species that affect the components of a
complex, congenital behavior.
Brain regions that function the same way in
these two species will not yield any behavioral
effect when transplanted between them,
regardless of whether their ''output'' affects
one component or many components of a behavior.
The chimera will still behave like a normal
member of the host species. Transplantation will
identify only those brain regions that function
differently with regard to behavioral
performance. Such functional differences could
theoretically occur at any level of brain
organization. The work reported here and
previously, using transplants covering all areas
of the brain, has found two regions that affect
the species difference in crowing performance.
The degree to which the functional
differences in these regions influence many
components or only a single component of this
complex behavior is of particular interest for
understanding how evolution changes brains to
change behavior.
Although previous work in the fruit fly
Drosophila melanogaster has separately
examined the number of genes involved in
interspecies reproductive isolation, including
behavioral attributes, and the anatomical
localization of sex differences in mating
behavior within a species using mosaic
individuals this is the first study to examine
the functional localization of cell groups that
confer species differences in the subcomponents
of a single homologous behavior.
There are three particularly striking aspects
of the results presented here.
- First, the fact that quail head
movements were so well integrated into the
chicken crowing performance is significant
because it implies that the quail cells in the
transplant had a well coordinated functional
relationship with the other chicken parts of the
brain that orchestrate crowing. The head
movement may have a quail phenotype because the
actual motor pattern is autonomously generated
in the caudal brainstem and the quail cells
there simply receive an activating signal from
the chicken cells that communicate with them or
because the motor pattern is generated by a more
distributed group of cells and quail cells in
the brainstem exert developmental effects on the
functional phenotype of chicken cells in other
parts of the brain.
- A second aspect of interest stems
from the fact that at least one of the brain
regions affected by the transplants was the
nucleus supraspinalis, a column of motor cells
that innervate the major extrinsic neck muscles
used in the generation of head movements. It is
noteworthy that the chimeric animals only gave
the quail head movement pattern when crowing,
despite the fact that, when the head is moved
during yawning and noncrowing vocalizations,
animals presumably use some of the same quail
motor cells to activate the neck musculature.
The transplanted cells seem to function
''normally'' in several different modes in
chickens just as they do in quail; whatever the
signals are that decide whether these cells do
or do not produce the quail head movement
pattern on a particular occasion, the chicken
host brain clearly has the capacity to generate
them. Sound production and head movement may be
independently produced, but they clearly
interact. If the pattern of sound production is
not well matched to the pattern of head
movement, as in the caudal brainstem chimeras
studied here, the interaction may be a
disruptive one. It will be instructive to see
what happens in ''double'' chimeras of the
midbrain and brainstem, in which sound
production and head movement patterns are well
matched, particularly with regard to whether the
head movements induce quail-like amplitude and
frequency modulations in the sound.
- The third aspect of interest is the
change in the portion of the quail head movement
pattern that one obtains in the chimeras with a
change in the rostrocaudal position of the
transplant. This implies that there is some
underlying structure in the anatomy of the cell
groups in the quail caudal brainstem that
reliably generates different portions of the
temporal head movement sequence at different
rostrocaudal positions. The results suggest that
species differences in this complex behavior are
produced by alterations in the phenotypes of
different, regionally separated groups of cells
in the brain that independently affect
particular behavioral subcomponents. A simple
model in which crowing differences are due to
evolutionary changes in a single higher brain
area is not tenable. Whether the quail cell
differences that produce the behavioral change
in the chimeras have effects that are autonomous
to these lower brain areas or have a
developmental impact on the phenotypes of
chicken cells in higher brain regions will be
addressed in future experiments.
