Intrinsic and synaptic properties of neurons in the vocal-control nucleus IMAN from in vitro slice preparations of juvenile and adult zebra finches

Abstract

A common theme of diverse neural systems is that circuits that are important for initial acquisition of learning do not necessarily serve as a substrate for the long-term storage of that memory. The neural basis of vocal learning in songbirds provides an example of this phenomenon, since a circuit that is necessary for vocal production during initial stages of vocal development apparently plays no subsequent role in controlling learned vocalizations. This striking functional change suggests the possibility of marked physiological changes in synaptic transmission within this circuit. We therefore examined intrinsic and synaptic properties of neurons in the cortical nucleus IMAN (lateral magnocellular nucleus of the anterior neostriatum), which forms part of this developmentally regulated circuit, in an in vitro preparation of the zebra finch forebrain. Although both functional and morphological characteristics of these neurons change substantially during vocal development, we did not observe widespread, substantive changes in the electrophysiological characteristics of juvenile versus adult IMAN neurons examined in vitro. Overall, both the intrinsic properties and synaptic responses of IMAN neurons were similar in slices from juvenile birds (at ages when lesions of IMAN disrupt vocal production) and in slices from adult birds (when IMAN lesions have no effect on song production). However, one intrinsic property that did vary between juvenile and adult cells was spike duration, which was longer in juvenile cells, suggesting the potential for activation of second-messenger cascades and/or enhanced synaptic transmission onto target cells of IMAN neurons. The pattern of synaptic response observed in both juvenile and adult cells suggests that IMAN projection neurons receive direct excitatory afferent inputs, as well as disynaptic inhibitory inputs from interneurons within IMAN. Activation of inhibitory interneurons rapidly curtails the excitatory response seen in projection neurons. This inhibition was abolished by bicuculline, indicating that the inhibitory interneurons normally exert their postsynaptic response via GABA(A) receptors on projection neurons. The inhibitory response could also be blocked by CNQX (6-cyano-7-nitroquinoxaline-2,3-dione), suggesting that the activation of inhibitory interneurons within IMAN may be governed primarily by AMPA receptors.