Cortical inter‐hemispheric circuits for multimodal vocal learning in songbirds

Abstract

Vocal learning in songbirds and humans is strongly influenced by social interactions based on sensory inputs from several modalities. Songbird vocal learning is mediated by cortico-basal ganglia circuits that include the SHELL region of lateral magnocellular nucleus of the anterior nidopallium (LMAN), but little is known concerning neural pathways that could integrate multimodal sensory information with SHELL circuitry. In addition, cortical pathways that mediate the precise coordination between hemispheres required for song production have been little studied. In order to identify candidate mechanisms for multimodal sensory integration and bilateral coordination for vocal learning in zebra finches, we investigated the anatomical organization of two regions that receive input from SHELL: the dorsal caudolateral nidopallium (dNCL ) and a region within the ventral arcopallium (Av). Anterograde and retrograde tracing experiments revealed a topographically organized inter-hemispheric circuit: SHELL and dNCL , as well as adjacent nidopallial areas, send axonal projections to ipsilateral Av; Av in turn projects to contralateral SHELL, dNCL , and regions of nidopallium adjacent to each. Av on each side also projects directly to contralateral Av. dNCL and Av each integrate inputs from ipsilateral SHELL with inputs from sensory regions in surrounding nidopallium, suggesting that they function to integrate multimodal sensory information with song-related responses within LMAN-SHELL during vocal learning. Av projections share this integrated information from the ipsilateral hemisphere with contralateral sensory and song-learning regions. Our results suggest that the inter-hemispheric pathway through Av may function to integrate multimodal sensory feedback with vocal-learning circuitry and coordinate bilateral vocal behavior.

Multi-dimensional tuning in motor cortical neurons during active behavior

“…AId receives topographic input from parallel circuits that process auditory, visual, and somatosensory information, so a similar mechanism to link different neuronal subpopulations within AId would be advantageous for facilitating sensorimotor integration across modalities (Zeier and Karten, 1971;Bottjer et al, 2000;Paterson and Bottjer, 2017).…”

“…In songbirds, the cortical region AId lies within an area that has been considered to be analogous to motor cortex in mammals: akin to infragranular layers of mammalian motor cortex, AId receives inputs that process multi-modal sensory information via dNCL (dorsal caudolateral nidopallium) as well as information from corticobasal ganglia circuitry that is dedicated to vocal learning, and in turn makes a variety of projections that give rise to feedforward and feedback pathways through subcortical and brainstem regions ( Fig. 1A) (Zeier and Karten, 1971;Bottjer et al, 2000;Karten, 2013;Paterson and Bottjer, 2017). Lesions of AId in juvenile zebra finches impair the bird's ability to achieve an accurate imitation of its memorized tutor song but do not induce vocal motor deficits (Bottjer and Altenau, 2010), suggesting an important role for this region in guiding motor refinement during sensorimotor learning.…”

A pan-mammalian map of interhemispheric brain connections predates the evolution of the corpus callosum

“…Mammals, however, evolved a highly topographic six-layered neocortex that recapitulates the peripheral sensory maps via point-to-point connections with subcortical regions (5)(6)(7). Moreover, the left and right cortical hemispheres of mammals are heavily interconnected compared with fewer such connections in birds, in which sensory-motor and associative regions of the telencephalic pallium receive limited input from the contralateral hemisphere (8,9) (Fig. 1).…”

Interhemispheric Integration for Complex Behaviors, Absent the Corpus Callosum in Normal Ontogeny

“…Consistent with this notion, it has recently been shown that precise homotopic wiring of the CC in the postnatal rodent brain requires preexisting functional homotopy (29). It is therefore plausible that ancestral pathways such as the anterior commissure (30) or symmetrical ascending bilateral inputs (13) are sufficient to provide the balance of interhemispheric integration and specialization required for complex multimodal cognition. The ability to conduct longitudinal investigations during a short sensitive period for vocal development makes the zebra finch an ideal model organism for investigating the behavioral relevance of this balance, allowing experimental manipulations not possible in humans.…”