Synaptic Transformations Underlying Highly Selective Auditory Representations of Learned Birdsong

Abstract

Stimulus-specific neuronal responses are a striking characteristic of several sensory systems, although the synaptic mechanisms underlying their generation are not well understood. The songbird nucleus HVC (used here as a proper name) contains projection neurons (PNs) that fire temporally sparse bursts of action potentials to playback of the bird's own song (BOS) but are essentially silent when presented with other acoustical stimuli. To understand how such remarkable stimulus specificity emerges, it is necessary to compare the auditory-evoked responsiveness of the afferents of HVC with synaptic responses in identified HVC neurons. We found that inactivating the interfacial nucleus of the nidopallium (NIf) could eliminate all auditory-evoked subthreshold activity in both HVC PN types, consistent with NIf serving as the major auditory afferent of HVC. Simultaneous multiunit extracellular recordings in NIf and intracellular recordings in HVC revealed that NIf population activity and HVC subthreshold responses were similar in their selectivity for BOS and that NIf spikes preceded depolarizations in all HVC cell types. These results indicate that information about the BOS as well as other auditory stimuli is transmitted synaptically from NIf to HVC. Unlike HVC PNs, however, HVC-projecting NIf neurons fire throughout playback of BOS as well as non-BOS stimuli. Therefore, temporally sparse BOS-evoked firing and enhanced BOS selectivity, manifested as an absence of suprathreshold responsiveness to non-BOS stimuli, emerge in HVC. The transformation to a sparse auditory representation parallels differences in NIf and HVC activity patterns seen during singing, which may point to a common mechanism for encoding sensory and motor representations of song.

Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird

“…Surgery and extracellular recording procedures were as described previously (42)(43)(44), with some modifications (SI Methods) with a new set of subjects. All electrophysiologic recordings were analyzed offline with Spike2 software.…”

“…All electrophysiologic recordings were analyzed offline with Spike2 software. The threshold for detecting multiunit activity was determined by the user at a level crossed by only high-amplitude events and excluded smallamplitude events (e.g., [42][43][44]. Multiunit activity.…”

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

“…This possibility is suggested by the fact that other nuclei such as NIF and Uva are known to provide distributed input to HVC, and to all three classes of HVC neurons [44,45]. However, some experiments suggest that this is a less plausible explanation than intrinsic generation of bursts within HVC.…”

Connections of thalamic modulatory centers to the vocal control system of the zebra finch

“…Auditory information also is transmitted from the HVC to an anterior forebrain pathway that includes area X within the songbird medial striatum; the nucleus dorsolateralis anterior thalami, pars medialis; the lateral magnocellular nucleus of the anterior nidopallium; and the RA. The source of auditory input to the HVC is thought to be the interfacial nucleus of the nidopallium (NIf), in which selectivity for the BOS is not as exclusive as in the HVC (4). Both the degree and selectivity of BOS-evoked responses in the HVC vary with natural and induced behavioral states such as sleeping, wakefulness, and anesthesia.…”