Development of Intrinsic and Synaptic Properties in a Forebrain Nucleus Essential to Avian Song Learning

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Abstract
In male zebra finches, the lateral magnocellular nucleus of the anterior neostriatum (LMAN) is necessary for the development of learned song but is not required for the production of acoustically stereotyped (crystallized) adult song. One hypothesis is that the physiological properties of LMAN neurons change over development and thus limit the ability of LMAN to affect song. To test this idea, we used in vitro intracellular recordings to characterize the intrinsic and synaptic properties of LMAN neurons in fledgling [posthatch days (PHD) 22–32] and juvenile zebra finches (PHD 40–51) when LMAN lesions disrupt normal song development, and in adults (>PHD 90) when LMAN lesions are without effect. In fledglings, depolarizing currents caused LMAN projection neurons to fire bursts of action potentials because of a putative low-threshold calcium spike (LTS). In contrast, juvenile and adult LMAN projection neurons fired accommodating trains of action potentials when depolarized but did not exhibit the burst mode of firing. Electrical stimulation of thalamic afferents elicited both monosynaptic EPSPs mediated by AMPA and NMDA receptors and polysynaptic IPSPs mediated by GABAA receptors from LMAN neurons at all ages studied here. In whole-cell voltage-clamp recordings, the EPSCs (NMDA-EPSCs) consisted of fast and slow components. Unlike juvenile and adult NMDA-EPSCs, those in fledglings were dominated by the slower component. Thus, both the intrinsic and synaptic properties of LMAN neurons change markedly during early song development (PHD 22–40) and achieve several adult-like properties during early sensorimotor learning and well before the time when LMAN lesions no longer disrupt song development.