Lateralization of song perception in the European starling (Sturnus vulgaris)
Résumé
Lateralization is one of the most intriguing aspects of brain functions. Hemispheric specialization for perception, especially for perception of conspecific vocal signals, has been documented in humans (9), rhesus monkeys (3) and mice (2). Our interest in possible right-left asymmetries in brain pathways for avian song perception stems from the observation of laterality for the production of learned song (4-6, 8, 10). This laterality is reminiscent of the hemispheric dominance for speech skills observed in humans (1). It has often been concluded that communication signals were processed in the hemisphere that has a dominant role in song production. But there are only few data on the perceptual aspect of laterality. Therefore we wanted to see whether song perception was lateralized. Starlings offered a variety of discrimination levelsÿ: they discriminated between conspecific and nonspecific signals, but also between familiar and unfamiliar conspecific whistles. Those discrimination levels were used to see whether some signals were processed by one hemisphere rather than by the other one. Multiunit recordings were used to test the hemispheric dominance in song perception in 6 adult male starlings caught in the wild. Neuronal responses to complex sounds were recorded in the auditory telencephalon of each hemisphere. The conspecific stimuli were species-specific and individual whistles of the starling tested, of a familiar starling and of an unfamiliar starling. Nonspecific stimuli were a pure tone (3 kHz) and a white noise. Multiunit recordings were performed on animals that were awake. Neuronal activity was documented by post-stimulus time histograms (PSTHs). Response strength was defined as the ratio between discharge rate and spontaneous activity. The spatial distribution of activity in relation to time was plotted as a response map. We then used a backward correlation technique developed in our laboratory (7). This computation yielded the characteristics of the stimulus most likely to produce a neuronal response. The result of this backward correlation was expressed as a sonogram, one for each recording site. The sonograms were mapped, using the coordinates of each recording site. These maps allowed us to characterize the spatial distribution of neuronal selectivity. The correlation maps showed a slight difference of selectivity between the two hemispheres. In each starling a small region responded selectively to a part of one type of whistles (rhythmic whistles). In each bird this region was located in one hemisphere only. In addition, the activity maps showed that neuronal activity during presentation of species-specific stimuli was systematically stronger in one hemisphere than in the other. On the contrary this difference of activity did not exist during presentation of artificial stimuli (pure tone and white noise). In 4 of the 6 birds the selective region and the strongest activity were located in the right hemisphere. In the 2 other birds they were located in the left hemisphere. Hence in 4 of the 6 starlings, the right hemisphere seemed to process preferentially conspecific sounds, and in 2 birds the left hemisphere seemed to do so. Such individual variations are regularly found in studies of lateralization. Although we know neither which factors determine hemispheric dominance, nor the nature of this phenomenon, the observation of functional asymmetry is real. Our results suggest that the two hemispheres of starlings perceive and process conspecific signals differently. They add to the many parallels between the avian and human systems that have become paradigmatic of vocal learning.