General information Frequency
parameters Population
identity
Individual identity Individual identity
L
HVC
Left Hemisphere Right Hemisphere
Species-specific signals
familiarNon Familiar
Own Species- specific whistles
Species- specific whistles
HVC
Pure tones Long
distance Short
distance
L
Pure tones White noise
Categorization Stimuli evoking a
motor response
Detail analysis Individual recognition
AWAKE AWAKE
Figure 4.7
Summary of the pattern of responses to behaviorally relevant classes of sounds in the fi eld L (L) and the main vocal area (HVC) of the left and right hemispheres of waked and anaesthetized male starlings (see explanations in the text). Dorsal is up and ventral is down.
a summary of the results). Under anesthesia, whatever the nucleus, it appeared that the number of responsive neurons was the same in both hemispheres. However, analysis of the responses to each class of stimuli showed a predominance of responses to artifi cial nonspecifi c sounds in the left hemisphere, and to class I songs, which are used in species-specifi c recognition, in the right hemisphere. These results suggest a specialization of the right hemisphere in processing species-specifi c signals, which, although the side of lateralization was not the same, is reminiscent of the functional specialization that has been observed in other animal species, such as, for example, rhesus monkeys ( Hauser & Andersson, 1994 ) and mice ( Ehret, 1987 ). When the birds were awake, we fi rst observed a signifi cantly higher number of responsive neurons in the right than in the left hemisphere. Given that responses to individual-specifi c songs prevailed when the birds were awake, this suggests an overall predominant role of the right hemisphere in individual recognition, which agrees with large evidence, in birds and mammals, of a dominant role of this hemisphere in conspecifi c recognition ( Vallortigara & Andrew, 1994 ). Moreover, we observed a relative left bias in responses to unfamiliar individual-specifi c (i.e., class II and III) songs in the fi eld L, and to all class II songs in the HVC. Class II songs are used in vocal interactions between social partners and are thought to evoke the listener ’ s approach ( Feare, 1984 ; Hausberger, 1991; Hausberger & Black, 1991; Hausberger et al., 1995 ). These results are therefore consistent with a prevailing role of the left hemisphere in categorization and in pro- cessing stimuli evoking a motor response, as has been proposed by several authors ( Goldberg & Costa, 1981; Rogers, 2000 ). In the right hemisphere, we observed a rela- tive predominance of responses to familiar and bird ’ s own songs in the fi eld L, and to warbling (i.e., class III songs) in the HVC. Warbling is a long and complex song that may be involved in female attraction ( Verheyen, 1980; Adret-Hausberger et al., 1990; Eens et al., 1991 ). Again, our results are therefore in total accordance with a putative role of the right hemisphere in detail analysis and individual recognition ( Vallortigara & Andrew, 1994 ; Andrew & Rogers, 2002; Vallortigara & Bisazza, 2002 ).
To sum up, our work on brain lateralization of song perception in starlings, in addi- tion to providing the fi rst clear evidence of hemispheric specialization in a songbird, supports the idea suggested by other authors that the left hemisphere would play a prevailing role in categorization, in processing stimuli evoking a motor response, and in producing responses that require inhibition until a decision is made, whereas the right hemisphere would play a major role in detail analysis, in individual recognition, and in producing rapid responses ( Goldberg & Costa, 1981; Andrew & Rogers, 2002;
Vallortigara & Bisazza, 2002 ).
New evidence of hemispheric specialization in song perception has been very recently provided in other songbird species. Thus, taking advantage of functional magnetic resonance imaging, which was recently adapted to starlings ( Van Meir et al., 2005 ) and zebra fi nches (e.g., Boumans et al., 2007 ; Voss et al., 2007 ), Poirier et al.
(2009) measured the blood-oxygen-level-dependent (BOLD) neural responses in anes- thetized male zebra fi nches that were exposed to their own song (BOS), a conspecifi c song (CON) and a heterospecifi c song (HET). They discovered, at the level of the midbrain in the ascending auditory pathway, that the differential activations elicited by BOS versus CON on the one hand and CON vs. HET on the other hand were both signifi cantly lateralized, to the right for BOS versus CON, and to the left for CON versus HET. According to them, the right lateralization they observed for BOS selectiv- ity could be due to a right lateralization of the auditory feedback control system that is crucial to song learning and maintenance, suggesting an anatomofunctional con- vergence between birds and humans. Indeed, in humans, speech learning and main- tenance are supposed to be supported by both a feed-forward and a feedback control, and recent studies suggest that the feed-forward control is lateralized to the left hemi- sphere while the auditory feedback control is, at least partially, lateralized to the right ( Toyomura et al., 2007 ; Tourville et al., 2008 ).
In conclusion, multiple and consistent lateralization effects for sensory processing in songbirds echo the lateralization fi ndings for perceptual processing in other taxa (e.g., Hauser & Andersson, 1994 ; Poremba et al., 2004 ; Taglialatela et al., 2008 ), includ- ing humans (reviewed in Zatorre, 2001 ), as well as robust lateralization fi ndings in the vocal and visual system of songbirds in male song behavior (see, e.g., George et al., 2006 , and this chapter for a review). Lateralization might therefore be a ubiquitous property of the vertebrate forebrain, especially in experience-dependent perceptual processing.
Sex Differences
In humans, a powerful neuromodulatory action of estradiol on the dynamics of functional brain organization seems to exist in the female brain, and there has been evidence of a role for ovarian hormones in shaping laterality of speech perception in women (e.g., Wadnerkar et al., 2008 ). Thus, Weis et al. (2008) have, for example, shown that the inhibitory infl uence of left-hemispheric language areas on homotopic areas of the right hemisphere is strongest during the menses, resulting in a pronounced lateralization. During the follicular phase, due to rising estradiol levels, inhibition and thus functional cerebral asymmetries are reduced.
In songbirds, males and females do not appear to differ markedly, and lateralization has been observed in both sexes. For example, in an attempt to determine whether the visual stimulus of a courting male modifi es song-induced expression of the IEG ZENK (zif268, egr1, NGFI-A, Krox 24) in the auditory forebrain of zebra fi nches, Avey et al. (2005) unexpectedly found a lateralization of Zenk response that was indepen- dent of sex, such that Zenk immunoreactivity was consistently higher in the left than in the right hemisphere and the majority of individual birds showed a left bias, sug-
gesting an overall specialization of the left auditory forebrain for song processing in females as well as in males.
More recently, Hauber et al. (2007) , studying anaesthetized, nonbreeding, adult female zebra fi nches, found signifi cantly greater normalized response strengths aver- aged for all the sounds they used (pure tones, white noise, and conspecifi c song) from right- than left-hemisphere units in two auditory forebrain regions (fi eld L and the caudolateral mesopallium; CLM). In fi eld L, the difference in responses between left and right hemispheres was only observed for the synthetic sounds while conspecifi c song responses were statistically identical in both sides, resulting in a differential response between song and other sounds that was actually greater in the left hemi- sphere. Further analysis indeed showed that only the left hemisphere displayed selec- tivity for conspecifi c song. In CLM, lateralization effect was only signifi cant when all sounds were considered, and it was largest for white noise. This study thus also sug- gests a potential specialization of the left hemisphere for processing song in female zebra fi nches.
Finally, left – right differences in nXIIts volume, motoneuron number, and syrinx muscle fi ber size (right > left) have been observed in both male and female zebra fi nches ( Wade et al., 2002 ). However, these results were obtained in birds that had been killed before the males ’ songs had reached their mature form. In a previous study ( Wade & Buhlman, 2000 ), in which birds were killed in adulthood, the same lateral biases were detected but those in the brains of adults (nXIIts volume and motoneuron number) were present only in males, who sing, and not in females, who do not.
According to Wade and colleagues, it is therefore possible that lateralization exists in the motor nucleus of both males and females prior to sexual maturity but that it is not maintained in adult females, who do not use the structure to the same degree as males. The neural lateralization may thus diminish in females in adulthood but in males may facilitate or be a consequence of increased song production.
The tight link that seems to exist between vocal behavior and lateralization has been better studied in female canaries who, unlike female zebra fi nches, do sing when they are given testosterone. Thus, a left syringeal dominance in song production has been observed in testosterone-treated female canaries ( Hartley et al., 1997 ). Moreover, in adult female canaries, the importance of the left hemisphere for controlling testos- terone-induced song increases with singing experience ( Greenspon & Stein, 1983 ), suggesting that the occurrence of left-lateralized control of vocal behavior may prove to be a characteristic typical of animals capable of vocal learning. Further studies, especially in species where both males and females sing, will be required to elucidate this point and to disentangle gender differences in lateralization from sexual dimor- phism in vocal behavior. In starlings, preliminary results suggest that females, who do sing, might be less lateralized than males (George et al., unpublished data), and no left – right difference has been observed in their telencephalon and cerebellum volume ( Van Meir et al., 2006 ).
Conclusion and Perspectives
Hemispheric asymmetries are a widespread phenomenon in all vertebrate species, whether at the individual or population level, and one can thus fi nd animal models for all types of asymmetries. Birdsong is the fi rst system in which nonhuman lateral- ization was demonstrated, and it is still among the best characterized. The early dis- covery of a left bias in the neural control of song production ( Nottebohm, 1971 , 1977 ; Nottebohm et al., 1976 ) has even greatly contributed to establishing a connection between studies on birdsong and studies on human speech. Yet, today, a query on song lateralization on PubMed retrieves less than a hundred papers, dating from 1976 to 2008, which has to be compared to the almost 9,000 papers, dating from 1951 to 2009, that can be retrieved with a query on language lateralization. This shows that songbirds are an emerging model in the fi eld of functional lateralization and that we undoubtedly still have a lot to learn from them.
Although the existence of motor asymmetries in song production of the Wasser- schlager canary has been one of the fi rst and most robust nonhuman examples of a lateralized neural control of behavior, we have seen that the degree and side of later- alization can vary greatly between species and that different species seem to have adopted different motor strategies that use the left and right sides of the syrinx in patterns of unilateral, bilateral, alternating, or sequential phonation to achieve the differing temporal and spectral characteristics of their songs ( Suthers, 1997 ). Lateraliza- tion may thus have evolved, as suggested by some authors ( Suthers, 1997 ; Suthers &
Goller, 1997 ), to make maximal use of the bipartite structure of the syrinx, and its mostly unilateral central control, for generation of spectrally and temporally complex acoustic signals. The evolutionary pressures that have led to hemispheric asymmetries in song production may therefore have been quite different from those leading to the lateralized central control of human speech ( Goller & Suthers, 1995 ).
In this respect, asymmetries in song perception, although much less investigated to date, may shed more light on the possible evolutionary origins of lateralization, especially in relation to language-like processes in the brain. Indeed, although evi- dence of hemispheric asymmetries in song perception is less steady than for song production, these asymmetries appear to show interesting parallels with asymmetries in speech processing. Thus, we have seen that starlings, which are highly social song- birds that have a sophisticated and plastic song, show a complex and state-dependent hemispheric specialization that is related to the social value of the acoustic signals (in terms of both familiarity and species-specifi c vs. individual recognition; see fi gure 4.7 ).
The left hemisphere appears to be specialized in processing unfamiliar songs and simple, short whistles that are used in long-distance individual recognition (especially through vocal interactions such as “ song matching ” ), while the right hemisphere appears to be specialized in processing familiar songs and complex, long vocalizations
that are used in individual recognition at short distance, especially between males and females. These results are in large accordance with other studies suggesting that the left hemisphere would be mainly involved in sustaining attention to stimuli for which a motor response is planned, and the right hemisphere in processing complex infor- mation ( Goldberg & Costa, 1981 ), in diffuse attention ( Andrew & Rogers, 2002 ), and in aggressive and sexual behaviors ( Vallortigara & Bisazza, 2002 ). Interestingly, studies performed in our laboratory (UMR6552 — Ethologie Animale et Humaine, Universit é Rennes 1 — CNRS, Rennes, France) have also demonstrated hemispheric specializations related to familiarity and social or emotional valence of stimuli in other species such as horses and monkeys ( Larose et al., 2006 ; De Boyer Des Roches et al., 2008 ; Baraud et al., 2009 ; de Latude et al., 2009 ). However, in starlings, we have also observed less pronounced hemispheric asymmetries for songs used in individual recognition (class II and III songs; see fi gure 4.6 ) than for nonspecifi c sounds and species-specifi c (class I) songs, which is particularly interesting. Indeed, one could imagine that the complex- ity of vocalizations bearing individual identity, which is especially clear in the case of warbling (or class III songs; see fi gure 4.6 ), could require a sophisticated processing involving both hemispheres, which could in turn explain why hemispheric differ- ences, thought about in terms of complementary functional specializations, might have evolved. In this respect, parallels with language are highly informative. Indeed, in humans, it has been shown that, whereas the left hemisphere plays a predominant role in the detection of verbal components in speech, the right hemisphere plays a major role in the detection of emotional prosody and in the processing of pitch infor- mation (e.g., Wernicke, 1874 ; Ross, 1981; Buchanan et al., 2000 ). Assuming that these different types of information differ in their acoustic structure and thus in their pro- cessing requirements, Zatorre (2001) has suggested an interesting unifying hypothesis to explain complementary functional specializations of the two hemispheres. This hypothesis states that:
Whereas the analysis of speech requires good temporal resolution to process rapidly changing energy peaks (formants) that are characteristic of many speech consonants (see, for example, the work of Tallal et al., 1993 ), it can be argued that tonal processes instead require good frequency resolution. In a truly linear system, temporal and spectral resolution are inversely related, so that improving temporal resolution can only come at the expense of degrading spectral resolution and vice versa. This tradeoff naturally arises from a fundamental physical constraint in acoustic processing: better resolution in the frequency domain can be obtained only at the expense of sampling within a longer time window, hence degrading temporal resolution; conversely, high resolution in the temporal domain entails a degraded spectral representation. The auditory nervous system is, of course, a highly nonlinear and distributed system; yet, it may also respect this fundamental computational constraint, such that in the left auditory cortex the high tem- poral resolution needed to process speech imposes an upper limit on the ability to resolve spec- tral information, and vice versa for the right auditory cortex. To put it more simply, the hypothesis is that there may be a tradeoff in processing in temporal and spectral domains, and
that auditory cortical systems in the two hemispheres have evolved a complementary specializa- tion, with the left having better temporal resolution, and the right better spectral resolution. (pp.
204 – 205)
This hypothesis has received experimental support from several human studies (see Zatorre, 2001 , for references) and would defi nitely deserve further investigation in songbirds, especially as spectral and temporal features of songs naturally vary between species and as these features can also be experimentally manipulated with great ease.
In general, processing complex information involves fi ne, simultaneous analysis of a variety of parameters that often requires mutually exclusive specializations, and hemispheric specializations can in this respect be compared as a special case of cerebral functional localizations. Now, it is well established that cerebral functional organiza- tion is greatly dependent upon early sensory experience (for some reviews, see Singer, 1986 ; Frey, 2007; Petersen, 2007 ). Our studies on starlings have demonstrated exp erience-dependent neuronal specialization and functional organization in the primary auditory area (fi eld L) of these birds, not only in relation to sensory experi- ence ( Cousillas et al., 2004 ) but also, and most importantly, in relation to social experience ( Cousillas et al., 2006 , 2008 ). One can thus wonder what role sensory and social experience may play in the development of hemispheric differences. Unfortu- nately, studies on songbirds are acutely lacking in this domain. Yet, songbirds consti- tute a particularly appropriate model that could certainly help us better address this issue, especially in relation to the communicative aspects of singing. Here again, par- allels with human studies could be very informative. In humans, the recent discovery of early leftward asymmetries in the arcuate fasciculus and in the corticospinal tract have led some authors to suggest that early macroscopic geometry, microscopic orga- nization, and maturation of the white matter bundles are related to the development of later functional lateralization ( Dubois et al., 2009 ). However, to our view, although early anatomical asymmetries unquestionably provide a basis for the development of functional hemispheric specialization, early experience is likely to play a more crucial role in this development. Thus, although anatomical asymmetries seem to appear very early in life, functional lateralization appears much later in development. For example, it has been observed that the functional lateralization of linguistic neural networks involved in automatic word recognition and in phonological processing is not yet developed in linguistically competent children age 10 years ( Spironelli & Angrilli, 2009 ). Moreover, there has been evidence of an infl uence of language on the func- tional organization of the brain. Thus, in adults, color categorical perception mainly takes place in the left hemisphere, whereas, in infants, it mainly takes place in the right hemisphere, and it appears that this hemispheric switch occurs when the words that distinguish the relevant category boundary are learned ( Franklin et al., 2008 ). In view of growing evidence for a potential implication of lateralization, and especially
atypical establishment of hemispheric specialization, in neurological and psychiatric disorders that sometimes involve severe impairment in social and/or language abilities, it appears of prime importance to better understand how lateralization develops, especially in relation to sensory or social experience and to the development of the ability to communicate with others. We believe that studies of the development of hemispheric asymmetries of songbirds are very promising in this respect because, as we have seen, songbirds are a unique model allowing experimental investigation of the interplay of neurobiological substrate and behavior. The power and uniqueness of songbirds as a model to study functional lateralization in relation to communicative aspects of vocal behavior lies in the fact that song is a learned behavior whose critical function is to communicate with other birds. As such, song behavior is inevitably strongly experience dependent. Moreover, this behavior is controlled by a highly evolved and well-characterized network of brain regions that are duplicated in two hemispheres that are not directly connected, and it is strongly hormone dependent.
Considering the fact that all these aspects of songs can be experimentally controlled and manipulated, which offers the possibility of compensating for the impossibility of experimentally controlling and manipulating language in human studies, there is no doubt that studies on hemispheric asymmetries of songbirds will long help us to better understand how the two halves of the brain process information, especially in relation to communicative behavior and its development, and also to the effects of not only experience but also gender and social factors.
Acknowledgments
I am grateful to Hugo Cousillas for his help in preparing this chapter and to Martine Hausberger for proofreading it.
References
Adret-Hausberger , M. , Guttinger , H. R. , & Merkel , F. W. ( 1990 ). Individual life history and song repertoire changes in a colony of starlings ( Sturnus vulgaris ) . Ethology , 84 , 265 – 280 .
Allan , S. E. , & Suthers , R. A. ( 1994 ). Lateralization and motor stereotypy of song production in the brown-headed cowbird . Journal of Neurobiology , 25 , 1154 – 1166 .
Andrew , R. J. ( 1991 ). The nature of behavioural lateralization in the chick . In R. J. Andrew (Ed.),
Neural and behavioural plasticity: The use of the domestic chick as a model (pp. 536 – 554 ). Oxford : Oxford University Press .
Andrew , R. J. ( 2002 ). Behavioral development and lateralization . In L. J. Rogers & R. J. Andrew (Eds.), Comparative vertebrate lateralization (pp. 157 – 205 ). Cambridge, England : Cambridge Uni- versity Press .