Silent Synapses in a Thalamo-Cortical Circuit Necessary for Song Learning in Zebra Finches

Abstract

Developmental changes in synaptic properties may act to limit neural and behavioral plasticity associated with sensitive periods. This study characterized synaptic maturation in a glutamatergic thalamo-cortical pathway that is necessary for vocal learning in songbirds. Lesions of the projection from medial dorsolateral nucleus of the thalamus (DLM) to the cortical nucleus lateral magnocellular nucleus of the anterior nidopallium (LMAN) greatly disrupt song behavior in juvenile birds during early stages of vocal learning. However, such lesions lose the ability to disrupt vocal behavior in normal birds at 60–70 days of age, around the time that selective auditory tuning for each bird’s own song (BOS) emerges in LMAN neurons. This pattern has suggested that LMAN is involved in processing song-related information and evaluating the degree to which vocal motor output matches the tutor song to be learned. Analysis of reversed excitatory postsynaptic currents at DLM→LMAN synapses in in vitro slice preparations revealed a pronounced N-methyl-d-aspartate receptor (NMDAR)-mediated component in both juvenile and adult cells with no developmental decrease in the relative contribution of NMDARs to synaptic transmission. However, the synaptic failure rate at DLM→LMAN synapses in juvenile males during the sensitive period for song learning was significantly lower at depolarized potentials than at hyperpolarized potentials. In contrast, the failure rate at DLM→LMAN synapses did not differ at hyper- versus depolarized holding potentials in adult males that had completed the acquisition of a stereotyped song. This pattern indicates that juvenile cells have a higher incidence of silent (NMDAR-only) synapses, which are postsynaptically silent at hyperpolarized potentials due to the voltage-dependent gating of NMDARs. Thus the decreased involvement of the LMAN pathway in vocal behavior is mirrored by a decline in the incidence of silent synapses but not by changes in the relative number of NMDA and AMPA receptors at DLM→LMAN synapses. These findings suggest that a developmental decrease in silent synapses within LMAN may represent a neural correlate of behavioral plasticity during song learning.