ABSTRACT
Although the brain relies on auditory information to calibrate vocal behavior, the neural substrates of vocal learning remain unclear. Here we demonstrate that lesions of the dopaminergic inputs to a basal ganglia nucleus in a songbird species (Bengalese finches, Lonchura striata var. domestica) greatly reduced the magnitude of vocal learning driven by disruptive auditory feedback in a negative reinforcement task. These lesions produced no measureable effects on the quality of vocal performance or the amount of song produced. Our results suggest that dopaminergic inputs to the basal ganglia selectively mediate reinforcement-driven vocal plasticity. In contrast, dopaminergic lesions produced no measurable effects on the birds' ability to restore song acoustics to baseline following the cessation of reinforcement training, suggesting that different forms of vocal plasticity may use different neural mechanisms. SIGNIFICANCE STATEMENT: During skill learning, the brain relies on sensory feedback to improve motor performance. However, the neural basis of sensorimotor learning is poorly understood. Here, we investigate the role of the neurotransmitter dopamine in regulating vocal learning in the Bengalese finch, a songbird with an extremely precise singing behavior that can nevertheless be reshaped dramatically by auditory feedback. Our findings show that reduction of dopamine inputs to a region of the songbird basal ganglia greatly impairs vocal learning but has no detectable effect on vocal performance. These results suggest a specific role for dopamine in regulating vocal plasticity.
Subject(s)
Dopamine/physiology , Finches/physiology , Learning/physiology , Vocalization, Animal/physiology , Animals , Basal Ganglia/cytology , Basal Ganglia/physiology , Cell Count , Conditioning, Operant/physiology , Feedback, Physiological , Male , Nerve Fibers/physiology , Neurons/physiology , Reinforcement, PsychologyABSTRACT
The N-methyl-D-aspartate receptor (NMDAR) is thought to be essential for synaptic plasticity and learning. However, recent work indicates that the role of this receptor depends on the prior history of the research subject. For example, animals trained on a hippocampus-dependent learning task are subsequently able to acquire new information in the absence of NMDAR activation. The current experiments were designed to identify the types of experiences that lead to NMDAR-independent learning. Using contextual fear conditioning in mice, we find that NMDAR-independent learning is only observed when (1) animals are trained on the same behavioral task and (2) initial learning is successfully encoded into long-term memory.
