Intrinsic and synaptic properties of neurons in an avian thalamic nucleus during song learning.

Abstract

The anterior forebrain pathway (AFP) of the avian song system is a circuit essential for song learning but not for song production. This pathway consists of a loop serially connecting area X in the basal ganglia, the medial portion of the dorsolateral nucleus of thalamus (DLM), and the pallial lateral magnocellular nucleus of the anterior neostriatum (lMAN). The majority of DLM neurons in adult male zebra finches closely resemble mammalian thalamocortical neurons in both their intrinsic properties and the strong GABAergic inhibitory input they receive from the basal ganglia. These observations support the hypothesis that the AFP and the mammalian basal ganglia-thalamocortical pathway use similar information-processing mechanisms during sensorimotor learning. Our goal was to determine whether the cellular properties of DLM neurons are already established in juvenile birds in the sensorimotor phase of song learning when the AFP is essential. Current- and voltage-clamp recording in DLM of juvenile male zebra finches showed that juvenile DLM has two distinct cell types with intrinsic properties largely similar to those of their respective adult counterparts. Immunostaining for glutamic acid decarboxylase (GAD) in juvenile zebra finches revealed that, as in adults, most area X somata are large and strongly GAD+ and that their terminals in DLM form dense GAD+ baskets around somata. GAD immunoreactivity in DLM was depleted by lesions of area X, indicating that a strong GABAergic projection from area X to DLM is already established in juveniles. Some of the DLM neurons exhibited large, spontaneous GABAergic synaptic events. Stimulation of the afferent pathway evoked an inhibitory postsynaptic potential or current that was blocked by the GABA(A) receptor antagonist bicuculline methiodide. The decay of the GABA(A) receptor-mediated currents was slower in juvenile neurons than in adults. In addition, the reversal potential for these currents in juveniles was significantly more depolarized both than that in adults and than the Cl(-) equilibrium potential; yet the reversal potential was still well below the firing threshold and thus inhibitory in the slice preparation. Our findings suggest that the signal-processing role of DLM during sensorimotor learning is generally similar to that in adulthood but that quantitative changes in synaptic transmission accompany the development of stereotyped song.