Contact Call-Driven Zenk Protein Induction and Habituation in Telencephalic Auditory Pathways in the Budgerigar (Melopsittacus Undulatus): Implications For Understanding Vocal Learning Processes

Abstract

Expression of the immediate early gene protein Zenk (zif 268, egr-1, NGF1A, Krox24) was induced in forebrain auditory nuclei in a vocal learning parrot species, the budgerigar (Melopsittacus undulatus), when the subjects either listened to playbacks of an unfamiliar contact call or to a contact call with which they had been familiarized previously. Auditory nuclei included the Field L complex (L1, L2a, and L3), the neostriatum intermedium pars ventrolateralis (NIVL), the neostriatum adjacent to caudal nucleus basalis (peri-basalis or pBas), an area in the frontal lateral neostriatum (NFl), the supracentral nucleus of the lateral neostriatum (NLs), and the ventromedial hyperstriatum ventrale (HVvm). The latter three nuclei are main sources of auditory input to the vocal system. Two patterns of nuclear staining were induced by contact call stimulation-staining throughout cell nuclei, which was exhibited by at least some neurons in all areas examined except L2a and perinucleolar staining, which was the only kind of staining exhibited in field L2a. The different patterns of Zenk staining indicate that auditory stimulation may regulate the Zenk-dependent transcription of different subsets of genes in different auditory nuclei. The numbers of neurons expressing Zenk staining increased from seven-to 43-fold over control levels when the birds listened to a repeating unfamiliar call. Familiarization of the subjects with the call stimulus, through repeated playbacks, greatly reduced the induction of Zenk expression to the call when it was presented again after an intervening 24-h interval. To determine if neurons exhibiting contact call-driven Zenk expression project to the vocal control system, call stimulation was coupled with dextran amines pathway tracing. The results indicated that tracer injections in the vocal nucleus HVo (oval nucleus of the hyperstriatum ventrale), in fields lateral to HVo and in NLs labeled many Zenk-positive neurons in HVvm, NFl, and NLs. These results support the idea that, in these neurons, egr-1 couples auditory stimulation to the synthesis of proteins involved in either the storing of new perceptual engrams for vocal learning or the processing of novel and/or meaningful acoustic stimuli related to vocal learning or the context in which it occurs.It is generally believed that the long-term changes in synaptic strength necessary for the maintenance of memories require protein synthesis controlled by the expression of immediate early genes

Expression of the immediate-early gene–encoded protein Egr-1 (zif268) during in vitro classical conditioning

“…1, lane 3), indicating that the antibody raised in mammals maintained its specificity in turtles. Similar findings have been reported for Egr-1 protein in bird brain tissue using the same antibody (Brauth et al 2002). Furthermore, it was recently shown that Egr-1 from a teleost shares a high sequence homology to other vertebrates (Burmeister and Fernald 2005).…”

“…Behavioral training studies have demonstrated a rapid and transient increase in hippocampal Egr-1 mRNA after spatial learning tasks in rats (Guzowski et al 2001), and in songbirds, expression of the homologous gene zenk increased sharply in the auditory nuclei of birds that listened to unfamiliar calls and declined when calls became familiar (Mello et al 1995;Brauth et al 2002). Egr-1 expression has also been implicated in having a key role in memory consolidation and/or reconsolidation processes.…”

Contact-call driven and tone-driven zenk expression in the nucleus ovoidalis of the budgerigar (Melopsittacus undulatus)

“…All birds were tested in acoustic chambers to which they had been acclimatized by sleeping overnight for a period of 3-7 days [19]. Control birds were immediately anesthetized and perfused in the morning of the experiment and did not have access to seeds.…”

“…Previous studies have used zenk gene expression to explore the response properties of ovoidalis and field L neurons to warble song [18] and the responsiveness of field L neurons to contact call [19] and food stimulation [20]. These studies show that neurons in the primary ascending auditory pathway (nucleus ovoidalis to field L) respond strongly to species-typical warble and that field L neurons respond to contact calls but not to food stimulation.…”

Information, information transfer, and information processing

“…Does hearing human speech and seeing human actions initiate comparable patterns in parrot brains? If action planning is the ability to select (even unconsciously) appropriate neurons and combine them into patterns of appropriate temporal activation (Arbib & Rizzolatti 1996), M/R training could strengthen or help form connections in whatever system does exist (Brauth et al 2001).…”