Charlotte A. Boettiger and Allison J. Doupe

Developmentally restricted synaptic plasticity in a songbird nucleus required for song learning

University of California, San Francisco

Long-lasting changes in the strength of synaptic connections are widely thought to be a key physiological mechanism underlying learning. Investigating this hypothesis in studies of song learning in birds has a number of advantages. First, birdsong is a well-defined and temporally complex behavior whose learning has been well characterized. Song learning generally occurs in two conceptually distinct stages, which bear striking similarities to the acquisition of human speech: a sensory critical period during which a song model (or "tutor" song) must be heard and memorized, and a sensorimotor phase, during which vocal output is matched to the stored memory of the tutor song, using auditory feedback. Second, likely sites for the neural mechanisms underlying song learning lie in a discrete network of brain areas known as the song system, which is essential for vocal learning and production. One of these areas, the lateral portion of the magnocellular nucleus of the anterior neostriatum (LMAN), has a particularly important function during song learning, because lesions of LMAN during song acquisition perturb song development, while similar disruptions in adult birds do not affect normal song production.

The possibility that LMAN could contribute to tutor song memorization, and needs NMDA receptor (NMDAR)-dependent plasticity to do so, was suggested by the downregulation of NMDAR expression in LMAN during sensory learning, and by the requirement for normal NMDAR function in LMAN during tutoring for accurate copying. We therefore tested slice preparations of LMAN from zebra finches for the presence of such plasticity. In slices from birds early in song learning (20 d of age), pairing postsynaptic bursts in LMAN principal neurons with stimulation of recurrent collateral synapses had two effects. One was spike-timing- and NMDA receptor-dependent LTP of the recurrent synapses. In addition, thalamic afferent synapses that were stimulated out of phase with the postsynaptic bursting in LMAN neurons underwent LTD. Both types of plasticity could no longer be induced by the end of the sensory critical period for song memorization (60 d), consistent with a role for these mechanisms in sensory learning.

The properties of the observed plasticity are appropriate to establish recurrent circuitry within LMAN that reflects the spatiotemporal pattern of thalamic afferent activity evoked by tutor song. Such circuit organization could represent a memory of the tutor song, suitable for reinforcing particular vocal motor sequences during sensorimotor learning. Moreover, while this plasticity shares features with that described in other systems, the song system may be particularly amenable to testing whether experience dependent changes in synaptic strength are causally related to the learning of complex behaviors.
Monday, June 5, 2023
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