The HVC Microcircuit: The Synaptic Basis for Interactions between Song Motor and Vocal Plasticity Pathways

Abstract

Synaptic interactions between telencephalic neurons innervating descending motor or basal ganglia pathways are essential in the learning, planning, and execution of complex movements. Synaptic interactions within the songbird telencephalic nucleus HVC are implicated in motor and auditory activity associated with learned vocalizations. HVC contains projection neurons (PNs) (HVC RA ) that innervate song premotor areas, other PNs (HVC X ) that innervate a basal ganglia pathway necessary for vocal plasticity, and interneurons (HVC INT ). During singing, HVC RA fire in temporally sparse bursts, possibly because of HVC INT -HVC RA interactions, and a corollary discharge can be detected in the basal ganglia pathway, likely because of synaptic transmission from HVC RA to HVC X cells. During song playback, local interactions, including inhibition onto HVC X cells, shape highly selective responses that distinguish HVC from its auditory afferents. To better understand the synaptic substrate for the motor and auditory properties of HVC, we made intracellular recordings from pairs of HVC neurons in adult male zebra finch brain slices and used spike-triggered averages to assess synaptic connectivity. A major synaptic interaction between the PNs was a disynaptic inhibition from HVC RA to HVC X , which could link song motor signals in the two outputs of HVC and account for some of the song playback-evoked inhibition in HVC X cells. Furthermore, single interneurons made divergent connections onto PNs of both types, and either PN type could form reciprocal connections with interneurons. In these two regards, the synaptic architecture of HVC resembles that described in some pattern-generating networks, underscoring features likely to be important to singing and song learning.

Stable propagation of a burst through a one-dimensional homogeneous excitatory chain model of songbird nucleus HVC

“…The slow and fast time constants τ 1 and τ 2 had respectively the values 1.1 ms and 0.2 ms to match roughly the 4.0 ms onset-to-peak time constants observed in paired intracellular recordings of HVC RA neurons [20]. The value I 0 = 0.3 nA was chosen to give a 1.0 mV peak excitatory post-synaptic potential (EPSP) which is consistent with experiment [20].…”

“…Of special importance for this paper is the experimental observation that HVC RA neurons synapse with other HVC RA neurons [20]. Thus it is possible for a feedforward network of excitatory neurons to exist in HVC, although we emphasize that there is no evidence presently for such a network.…”

Auditory P3a and P3b neural generators in schizophrenia: An adaptive sLORETA P300 localization approach

“…Then, a subject-adaptive WOI threshold was established using the 75% rise time from N200 amplitude to P300 amplitude (i.e. the time to reach 75% of the P300 peak amplitude (Mooney and Prather, 2005)). …”

Neural Coding of Syntactic Structure in Learned Vocalizations in the Songbird

“…Intracellular electrophysiological studies have so far demonstrated that the burst spikes in HVC X neurons arise through different subthreshold processes from those in HVC RA neurons (Lewicki, 1996;Mooney, 2000;Mooney and Prather, 2005;Long et al, 2010): the temporal precision of HVC RA bursts is mainly determined by selective excitatory synaptic inputs, whereas inhibitory synaptic inputs play primary roles in the establishment of HVC X bursts. Because inhibitory synaptic inputs to HVC X neurons presumably originate from interneurons within HVC, syntactic attributes in HVC X activity may be formed through the development of inhibitory interneurons after the establishment of the excitatory network.…”