Decrements in auditory responses to a repeated conspecific song are long-lasting and require two periods of protein synthesis in the songbird forebrain.

Abstract

Earlier work showed that playbacks of con- Songbirds use their songs and calls to communicate with members of their own species. Male songbirds typically learn these vocalizations from adult conspecifics during a sensitive period in development. These learned songs and calls can differ markedly between individuals, though they also share species-typical features (1-3). Much is known about the brain pathways birds use for the production of learned vocalizations (4, 5), but our understanding of circuits that discriminate and store these signals is just beginning to develop (6, 7). One forebrain area that may play a role in perceptual aspects of vocal communication is the caudo-medial neostriatum (NCM), where playback of conspecific song is more effective than heterospecific song or non-song sounds in inducing the expression of the immediate early gene ZENK (also known as zif-268, egr-1, NGFI-A, or Krox-24) (8, 9). The ZENK response in NCM disappears when the same song is played back repeatedly, but a full ZENK response is elicited again if a novel song is presented (10). ZENK is one of a group of immediate early genes that encode transcriptional regulators thought to mediate the long-term effects of depolarization on neural activity and thus to play a role in memory formation (11)(12)(13)(14).These observations suggest that NCM is part of a system that processes and memorizes species-specific sounds.In the present study we recorded the electrophysiological responses of NCM neurons to conspecific and heterospecific song in the presence or absence of protein or RNA synthesis inhibitors. We describe a long-lasting decrease in responsive-The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.ness of NCM neurons to repetitions of the same song stimulus and suggest that this may be a good system in which to study the cellular and molecular basis of perceptual learning.* METHODS Experimental Animals and Surgical Procedures. Forty adult male zebra finches (Taeniopygia guttata) obtained from our breeding colony or from a local supplier were used. Under anesthesia, birds were surgically prepared for recording. Twenty-four to 48 h later, the awake-animals were restrained for recordings and microinjections. Recording sessions typically lasted 4-5 h, conforming to an approved animal use protocol. At the end of each experiment, small electrolytic lesions were made for use in locating the recording sites. The birds were then killed and the brains were processed for histology. For all procedural details, see ref. 15.Auditory Stimulation. The songs of 50 male zebra finches and 5 canaries from our archives were digitized at 20 kHz (Signal, Engineering Design, Belmont, MA) to provide a set of conspecific and heterospecific songs that the birds had never heard before. The zebra finch songs were 1.2-2.0 s long and contained introductory notes and one or two motifs. The canary...

Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography

“…Measurement of long-term response habituation in NCM, by both electrophysiology and the study of the song stimulation-induced up-regulation of ZENK, has suggested that this area might encode the long-lasting sensory memory of the TUT (31,40). Other experiments point to the fact that NCM and CM might be involved in short-term plasticity related to song discrimination (18,19,48). The greater representation of TUT and BOS revealed by fMRI in our experiments therefore might reflect an important aspect of the sensory memory for these developmentally salient familiar stimuli.…”

“…In parallel with song motor learning, auditory song selectivity gradually emerges during development (13)(14)(15)(16)(17). Robust sensory responses to auditory stimuli have been recorded in the primary auditory area in the caudal telencephalic region (field L), the caudomedial nidopallium (NCM), the caudal mesopallium (CM), and the caudomedial ventral hyperstriatum (18)(19)(20)(21), as well as in the song nuclei HVC, LMAN, X, and nucleus interface of the nidopallium (22)(23)(24)(25)(26)(27)(28). Sensory representation of birdsong in the song nuclei and the secondary auditory areas NCM and CM is characterized by response selectivity to song ownership, familiarity, and species-specific features.…”

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

“…Dorsocaudal NCM neurons are known to habituate to repeated presentation of song stimuli, but we did not observe substantial habituation in our recordings in ventral NCM (as in ref. 40; see also SI Results). Three recording/playback periods consisted of a baseline aCSF retrodialysis (30 min), followed by 30 min of either estradiol (30 μg/mL) or FAD (100 μM) retrodialysis, and then followed by 30 min of washout with aCSF.…”

Differential expression of glutamate receptors in avian neural pathways for learned vocalization

“…We chose auditory regions, because a few subunits/subtypes appeared to have some differential expression relative to the surrounding subdivision (mGluR1 in caudal N for example; Fig. 2), and these regions are involved in auditory processing of learned vocalizations (Chew et al, 1995; . Expression profiles of 21 glutamate receptor subunits/ subtypes from the four glutamate receptor subfamilies in adult zebra finch male brain.…”