Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system

Abstract

The ZENK gene encodes a zinc-finger-containing transcriptional regulator and can be rapidly activated in songbird brain by presentation of birdsong (Mello et al., 1992). Here we map the areas of the songbird forebrain that show this genomic response to birdsong, using in situ hybridization. After 30 min of song presentation ZENK mRNA levels reach a peak in the caudomedial telencephalon, in areas adjacent to or closely related with primary auditory structures. These areas include subfields of field L (L1 and L3), the caudomedial neostriatum (NCM), the caudomedial hyperstriatum ventrale (CMHV) anterior to field L, the caudal paleostriatum, and two field L targets, HVC shelf and RA cup. In contrast, ZENK induction is absent in some areas that show a response to song by other measures and where ZENK induction might have been expected. These include the direct thalamo- recipient field L subfield L2, and the nuclei of the circuit involved in the acquisition and production of learned song. These results demonstrate that ZENK induction following song presentation occurs only in a subset of areas physiologically activated by song, and draw attention to areas previously unsuspected as related to processing of complex auditory stimuli. Based on what is known about ZENK function in mammalian systems (Christy et al., 1989; Cole et al., 1989; Wisden et al., 1990), we speculate that areas revealed by ZENK induction might correspond to sites where critical neuronal modifications occur in response to birdsong presentation, possibly leading to the formation of song-related memories.

Revised nomenclature for avian telencephalon and some related brainstem nuclei

“…Several additional nuclei have been identified in songbirds that are important for auditory processing or are related to song learning and control, including the lateral magnocellular nucleus of the anterior neostriatum (lMAN or LMAN; Fig. 7D), the medial magnocellular nucleus of the anterior neostriatum (mMAN or MMAN), and the caudomedial neostriatum (NCM; Nottebohm et al, 1976;Bottjer et al, 1989;Mello et al, 1992;Mello and Clayton, 1994;Margoliash, 1997;Nordeen, 1997;. With the renaming of neostriatum, the name for each of these is altered by substituting nidopallium for neostriatum, and the established abbreviation remains the same (Table 4).…”

An Analysis of the Neural Representation of Birdsong Memory

“…However, analysis of the expression of immediate early genes (IEGs), a measure of neuronal activation (Sagar et al, 1988;Tischmeyer and Grimm, 1999;Davis et al, 2003), has revealed that other parts of the brain are involved in song perception. These brain regions include the caudomedial neostriatum (NCM) [also known as the caudomedial nidopallium (Reiner et al, 2004)] and the caudomedial hyperstriatum ventrale (CMHV) (or caudomedial mesopallium in the new nomenclature of Reiner et al, 2004) (Mello et al, 1992;Mello and Clayton, 1994;Jarvis and Nottebohm, 1997;Mello and Ribeiro, 1998;Bolhuis et al, 2000) (Fig. 1).…”

Localized neuronal activation in the zebra finch brain is related to the strength of song learning

“…Recent studies have investigated the expression of immediate early genes (IEGs) (12,13) in adult zebra finch males after exposure to unfamiliar conspecific song (14)(15)(16)(17). Expression of IEGs is a measure of neuronal activation (12,13).…”

“…Exposure of adult zebra finch males to conspecific song led to significantly increased expression of the IEG known as ZENK in the caudal part of the neostriatum (NCM) and of the hyperstriatum ventrale (cHV), but not in HVC, Area X, lMAN or RA, nor in Field L, a primary auditory projection area (14)(15)(16)(17)(18)(19)(20). The increase in ZENK expression did not occur after exposure to heterospecific song or to tone busts (14,15). Subsequent studies suggest a dissociation between the neural substrates of production and perception of song (20).…”

“…When an adult zebra finch male sings, there is neuronal activation in the song-control nuclei (20,21). However, when the bird hears a conspecific song without singing itself, there is no increased activation in these nuclei, but there is in other regions, including NCM and cHV (14)(15)(16)(17)(18)(19)(20). These findings suggest that NCM and cHV are important for song perception, but until now there is no evidence that indicates the role (if any) of either of these forebrain regions in the storage of auditory memories during song learning.…”