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mise à jour du 22 août 2002
 Proc. Natl. Acad. Sci. USA
1997; 94, 2001-2006
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Changes in multiple brain regions underlie species differences in a complex, congenital behavior
Evan Balaban
Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138; and The Neurosciences Institute,
10640 John Jay Hopkins Drive, San Diego, CA 92121  


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.