An Associational Model of Birdsong Sensorimotor Learning I. Efference Copy and the Learning of Song Syllables

Abstract

Birdsong learning provides an ideal model system for studying temporally complex motor behavior. Guided by the well-characterized functional anatomy of the song system, we have constructed a computational model of the sensorimotor phase of song learning. Our model uses simple Hebbian and reinforcement learning rules and demonstrates the plausibility of a detailed set of hypotheses concerning sensory-motor interactions during song learning. The model focuses on the motor nuclei HVc and robust nucleus of the archistriatum (RA) of zebra finches and incorporates the long-standing hypothesis that a series of song nuclei, the Anterior Forebrain Pathway (AFP), plays an important role in comparing the bird's own vocalizations with a previously memorized song, or “template.” This “AFP comparison hypothesis” is challenged by the significant delay that would be experienced by presumptive auditory feedback signals processed in the AFP. We propose that the AFP does not directly evaluate auditory feedback, but instead, receives an internally generated prediction of the feedback signal corresponding to each vocal gesture, or song “syllable.” This prediction, or “efference copy,” is learned in HVc by associating premotor activity in RA-projecting HVc neurons with the resulting auditory feedback registered within AFP-projecting HVc neurons. We also demonstrate how negative feedback “adaptation” can be used to separate sensory and motor signals within HVc. The model predicts that motor signals recorded in the AFP during singing carry sensory information and that the primary role for auditory feedback during song learning is to maintain an accurate efference copy. The simplicity of the model suggests that associational efference copy learning may be a common strategy for overcoming feedback delay during sensorimotor learning.

Experience is required for the maintenance and refinement of FM sweep selectivity in the developing auditory cortex

“…It is likely that experience with echolocation is essential for the development of response selectivity in the pallid bat auditory cortex. Although we have focused on the role of sensory experience, motor feedback may play a role (22)(23)(24). Further studies will need to examine whether purely sensory experience with externally generated echolocation pulses is sufficient to support the development of response selectivity, or whether the combined sensorimotor experience of echolocating is required.…”

The Dorsomedial Striatum Reflects Response Bias during Learning

“…Such a role for the basal ganglia in generating spontaneous variations in behavior has been proposed during birdsong learning (Kao et al, 2005) and may also explain classic effects of striatal lesions of the striatum on spontaneous alternation behavior (Chorover and Gross, 1963;Divac et al, 1978). From a theoretical perspective, bias-related changes in striatal activity could enable plasticity in cortical systems that receive projections from thalamic areas innervated by the basal ganglia, as proposed in a leading theory of basal ganglia function by Houk and Wise (1995) and also in a computational model of birdsong learning (Troyer and Doupe, 2000). A recent study by Andalman and Fee (2009) has provided direct evidence for bias-like signals existing within the basal ganglia components of the songbird system and being under control of cortex-like areas (the anterior forebrain pathway).…”

Rhythmic Activity in a Forebrain Vocal Control NucleusIn Vitro

“…The sustained rhythmic activity described here may contribute to this integration. The rhythmic activity in HVC could also help create predictive signals hypothesized to follow premotor activation of HVC cells (Troyer and Doupe, 2000). In this scenario, the predictive signal (or "efference copy") is compared with a model song during song learning, and such a signal may need to preserve the phasic patterns characteristic of auditory activity.…”