Evidence for a causal inverse model in an avian cortico-basal ganglia circuit

Significance Auditory neural responses mirror motor activity in a songbird cortical area. The average temporal offset of mirrored responses is roughly equal to short sensorimotor loop delays. This correspondence between mirroring offsets and loop delays constitutes evidence for a causal inverse model. Causal inverse models can map a desired sensation into the required action. Learning by imitation is fundamental to both communication and social behavior and requires the conversion of complex, nonlinear sensory codes for perception into similarly complex motor codes for generating action. To understand the neural substrates underlying this conversion, we study sensorimotor transformations in songbird cortical output neurons of a basal-ganglia pathway involved in song learning. Despite the complexity of sensory and motor codes, we find a simple, temporally specific, causal correspondence between them. Sensory neural responses to song playback mirror motor-related activity recorded during singing, with a temporal offset of roughly 40 ms, in agreement with short feedback loop delays estimated using electrical and auditory stimulation. Such matching of mirroring offsets and loop delays is consistent with a recent Hebbian theory of motor learning and suggests that cortico-basal ganglia pathways could support motor control via causal inverse models that can invert the rich correspondence between motor exploration and sensory feedback.