Hearing better with the right eye? The lateralization of multisensory processing affects auditory learning in Northern bobwhite quail (Colinus Virginianus) chicks

Abstract

Precocial avian species exhibit a high degree of lateralization of perceptual and motor abilities, including preferential eye use for tasks such as social recognition and predator detection. Such lateralization has been related, in part, to differential experience prior to hatch. That is, due to spatial and resulting postural constraints late in incubation, one eye and hemisphere—generally the right eye / left hemisphere—receive greater amounts of stimulation than the contralateral eye / hemisphere. This raises the possibility that the left hemisphere may specialize or show relative advantages in integrating information across visual and auditory modalities, given that it typically receives greater amounts of multimodal auditory and visual stimulation prior to hatch. The present study represents an initial investigation of this question in a precocial avian species, the Northern bobwhite quail (Colinus virginianus). Day-old bobwhite chicks received 5 min training sessions in which they vocalized to receive contingent playback of a bobwhite maternal call, presented with or without a light that flashed in synchrony with the notes of the call (i.e., bimodal versus unimodal exposure, respectively). Chicks were trained with or without eye patches that allowed them to experience the visual component of the bimodal stimulus with only the left eye (LE), right eye (RE), or both eyes (i.e., binocular; BIN). Finally, the light was placed in various positions relative to the speakers playing the maternal call across three experiments. 24 h later chicks were provided a simultaneous choice test between the familiarized and a novel bobwhite maternal call. Given that the right eye and ear typically face outward and are thus unoccluded by the body during late prenatal development, we hypothesized that RE chicks would show facilitated learning under bimodal conditions compared to all other training conditions. This hypothesis was partially confirmed in Experiment 1, when the light was positioned 40 cm above the source of the maternal call. However, we also observed evidence of suppressed learning in chicks provided BIN exposure to the bimodal audio-visual stimulus that was not present during auditory-only training. Experiments 2 and 3 demonstrated that this was likely related to activation of a left-hemisphere dependent fear response when the left eye was exposed to a visual stimulus that loomed above the auditory stimulus. These results indicate that multisensory processing is lateralized in a precocial bird and that these species may thus provide a unique model for studying experience-dependent plasticity of intersensory perception.