A large-capacity memory system that recognizes the calls and songs of individual birds.

Abstract

Auditory responses in the caudomedial neostriatum (NCM) of the zebra finch (Taeniopygia guttata) forebrain habituate to repeated presentations of a novel conspecific song. This habituation is long lasting and specific to individual stimuli. We here test the acoustic and ethological basis of this stimulus-specific habituation by recording extracellular multiunit activity in the NCM of awake male and female zebra finches presented with a variety of conspecific and heterospecific vocalizations, white noise, and tones. Initial responses to conspecific song and calls and to human speech were higher than responses to the other stimuli. Immediate habituation rates were high for all novel stimuli except tones, which habituated at a lower rate. Habituation to conspecific calls and songs outlasted habituation to other stimuli. The extent of immediate habituation induced by a particular novel song was not diminished when other conspeeific songs were presented in alternation. In addition, the persistence of habituation was not diminished by exposure to other songs before testing, nor was it influenced by gender or laterality. Our results suggest that the NCM is specialized for remembering the calls and songs of many individual conspecifics.Vocal communication using songs and calls is an important part of social and reproductive behavior in many songbird species (1). Songbirds learn their songs (and in some cases calls) from conspecific tutors, but include minor variations; as a result, these vocalizations have an acoustic form that is specific to each individual. We have previously shown that playbacks of novel conspecific songs elicit vigorous auditory responses in neurons in the caudomedial neostriatum (NCM) of the zebra finch (Taeniopygia guttata) brain. These responses habituate with repeated presentations of the same song, and the habituation persists for up to 48 h (2). We have now tested the specificity of these responses by using a larger variety of stimuli, presented in various temporal combinations to both male and female zebra finches. The results show that the initial activity elicited by noise, tones, and various conspecific or heterospecific vocalizations does not predict whether or not repeated exposure to any of these signals will produce longterm habituation. In addition, long-term habituation remains specific for individual songs and calls even when the bird is exposed to large numbers of similar stimuli that could potentially interfere with this form of memory.

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

“…It seems likely, therefore, that the NCM is (part of) the neural substrate for the representation of the learned tutor song, which is activated when the animal is reexposed to that song. This suggestion is consistent with previous electrophysiological recordings in the NCM of zebra finches, showing some degree of specificity in the response to conspecific songs (25). In the present study, increased IEG expression in the cHV did not correlate significantly with song copying, suggesting that the cHV may have a different role than the NCM.…”

Subcellular compartmentalization of aromatase is sexually dimorphic in the adult zebra finch brain

“…These areas are critical modulators of singing behavior (Nottebohm and Arnold, 1976) and song recognition (Mello et al, 1992;Chew et al, 1996;Bailey et al, 2002;Bailey and Wade, 2003). It is possible that synaptic aromatase may contribute to these processes in the zebra finch.…”

An Analysis of the Neural Representation of Birdsong Memory

“…2). Other (electrophysiological) studies of the NCM (Chew et al, 1996;Stripling et al, 1997) failed to find differences in neuronal responsiveness between BOS and novel song as well. To our knowledge, neuronal responsiveness to tutor song compared with BOS or novel song has not been investigated before, using either electrophysiology or IEG expression.…”

“…Nevertheless, female zebra finches can learn to recognize songs to which they have been exposed, and they develop a preference for these songs (Riebel, 2000;Riebel et al, 2002). Several studies have shown that both the NCM and the CMHV are involved in processing conspecific songs in female songbirds (Chew et al, 1996;MacDougall-Shackleton et al, 1998;Duffy et al, 1999;Gentner et al, 2001;Bailey et al, 2002;Sockman et al, 2002;Bailey and Wade, 2003;Gentner and Margoliash, 2003;Grace et al, 2003;Maney et al, 2003;Phillmore et al, 2003), as well as in female budgerigars . Preliminary results from our own laboratory indicate that, in female zebra finches, the CMHV may be part of the neural representation of learned tutor song (Terpstra et al, 2001).…”