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Models of vocal learning in the songbird: Historical frameworks and the stabilizing critic

Birdsong is a form of sensorimotor learning that involves a mirror‐like system that activates with both song hearing and production. Early models of song learning, based on behavioral measures, identified key features of vocal plasticity, such as the requirements for memorization of a tutor song and auditory feedback during song practice. The concept of a comparator, which compares the memory of the tutor song to auditory feedback, featured prominently. Later models focused on linking anatomically‐defined neural modules to behavioral concepts, such as the comparator. Exploiting the anatomical modularity of the songbird brain, localized lesions illuminated mechanisms of the neural song system. More recent models have integrated neuronal mechanisms identified in other systems with observations in songbirds. While these models explain multiple aspects of song learning, they must incorporate computational elements based on unknown biological mechanisms to bridge the motor‐to‐sensory delay and/or transform motor signals into the sensory domain. Here, I introduce the stabilizing critic hypothesis, which enables sensorimotor learning by (1) placing a purely sensory comparator afferent of the song system and (2) endowing song system disinhibitory interneuron networks with the capacity both to bridge the motor‐sensory delay through prolonged bursting and to stabilize song segments selectively based on the comparator signal. These proposed networks stabilize an otherwise variable signal generated by both putative mirror neurons and a cortical‐basal ganglia‐thalamic loop. This stabilized signal then temporally converges with a matched premotor signal in the efferent song motor cortex, promoting spike‐timing‐dependent plasticity in the premotor circuitry and behavioral song learning. © 2014 Wiley Periodicals, Inc. Develop Neurobiol 75: 1091–1113, 2015