Abstract
Many learned motor behaviors are acquired by comparing ongoing behavior with an internal representation of correct performance, rather than using an explicit external reward. For example, juvenile songbirds learn to sing by comparing their song with the memory of a tutor song. At present, the brain regions subserving song evaluation are not known. In this study, we report several findings suggesting that song evaluation involves an avian 'cortical' area previously shown to project to the dopaminergic midbrain and other downstream targets. We find that this ventral portion of the intermediate arcopallium (AIV) receives inputs from auditory cortical areas, and that lesions of AIV result in significant deficits in vocal learning. Additionally, AIV neurons exhibit fast responses to disruptive auditory feedback presented during singing, but not during nonsinging periods. Our findings suggest that auditory cortical areas may guide learning by transmitting song evaluation signals to the dopaminergic midbrain and/or other subcortical targets.
Highlights
Most human behaviors, such as speech, music, or athletic performance, are learned through a gradual process of trial and error
Motivated by the hypothesized role of dopaminergic signaling in reinforcement learning (Houk et al, 1994; Schultz et al, 1997; Bayer and Glimcher, 2005; Tsai et al, 2009), we set out to examine the role in vocal learning of a recently discovered songbird cortical area (Gale et al, 2008) that projects to ventral tegmental area (VTA) and substantia nigra pars compacta (SNc)
We have characterized the spatial extent of neurons within the intermediate arcopallium that project to VTA and SNc, and refer to the region of arcopallium retrogradely labeled from these midbrain dopaminergic areas as AIV
Summary
Most human behaviors, such as speech, music, or athletic performance, are learned through a gradual process of trial and error In all of these behaviors, the motor actions are shaped during learning by an internal model of good performance (Wolpert et al, 1995). We use the songbird as a model system to understand how complex behaviors can be learned by self-evaluation of motor performance, rather than relying on explicit external rewards such as food or social reinforcement. Songbirds learn their vocalizations by storing a memory, or ‘template’, of their tutor's song (Doupe and Kuhl, 1999). A key component of this vocal learning circuit is Area X, a basal ganglia homologue containing both striatal and pallidal components (Person et al, 2008)
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