Hemispheric differences in processing of vocalizations depend on early experience

Abstract

An intriguing phenomenon in the neurobiology of language is lateralization: the dominant role of one hemisphere in a particular function. Lateralization is not exclusive to language because lateral differences are observed in other sensory modalities, behaviors, and animal species. Despite much scientific attention, the function of lateralization, its possible dependence on experience, and the functional implications of such dependence have yet to be clearly determined. We have explored the role of early experience in the development of lateralized sensory processing in the brain, using the songbird model of vocal learning. By controlling exposure to natural vocalizations (through isolation, song tutoring, and muting), we manipulated the postnatal auditory environment of developing zebra finches, and then assessed effects on hemispheric specialization for communication sounds in adulthood. Using bilateral multielectrode recordings from a forebrain auditory area known to selectively process species-specific vocalizations, we found that auditory responses to species-typical songs and long calls, in both male and female birds, were stronger in the right hemisphere than in the left, and that right-side responses adapted more rapidly to stimulus repetition. We describe specific instances, particularly in males, where these lateral differences show an influence of auditory experience with song and/or the bird's own voice during development.

Fig. 1.

ARM and adaptation rate of NCM neuronal responses to song and LC stimuli in males. In intact male birds exposed to playback of a male song (Tutored) or just their own isolate song (Untutored), response magnitude to both song and call stimuli was significantly higher in the right hemisphere than in the left (Left, open squares; Right, filled squares). In devocalized male birds that heard neither self-vocalizations nor a tutor song (Devoc-Untutored), no lateral difference in NCM response magnitude to either songs (A) and LCs (B) was seen. Tutored birds (Intact-Tutored) showed significant lateral differences in adaptation rates for both songs (C) and LCs (D). The left side shows lower rates (slower adaptation) than the right. The adaptation rate is the slope of the decrease in response magnitude with successive presentations, normalized by the ARM; thus, the lower symbols (more negative points) represent faster adaptation. In response to songs (C), only Devoc-Tutored males showed no hemispheric differences in adaptation rates. In contrast, in response to LCs (D), Untutored, Devoc-Untutored, and Devoc-Tutored males showed no hemispheric differences. Error bars represent means ± SEM.

Fig. 2.

ARM and adaptation rate of NCM neuronal responses to song and LC stimuli in females. As in males, Intact-Tutored females have higher response magnitude in the right hemisphere in response to song (A) and LC (B). In contrast to the Intact-Untutored males, Intact-Untutored females (who heard only themselves) do not show a lateral difference in the magnitude of neuronal responses (Left, open circles; Right, filled circles). Untutored males hear their own isolate song and calls (which are abnormal but contain male-typical features), whereas females hear only their own acoustically simple calls. Similar contrasts were seen in measurements of adaptation rates. Unlike Tutored males who produce both song and calls, Tutored females who were able to produce calls (Intact-Tutored) did not show significant lateral differences in adaptation rates to song (C); however, this group did show significant lateral differences in adaptation rates to LCs (D). Error bars represent means ± SEM.

Fig. 3.

Representative vocalizations, multiunit responses, and sagittal section of NCM. (A) Sonogram of tutor song stimulus presented during development. Examples of song (B) and LC (C) produced by an Untutored male showing complex features of these abnormal “isolate” vocalizations and LC of a Tutored female (D). Representative normal LCs used as stimuli in the electrophysiology experiments (E, female call; F, male call). Representative multiunit neuronal responses from left and right NCM of a tutored male to a LC (G) and 2,750-Hz pure tone (H). (I) Representative sagittal section of NCM taken 0.75 mm from the midline. White asterisk indicates a typical lesion made at a recording site in dorsal NCM. (Scale bar: 1 mm.)