The role of GABA in the central processing of complex auditory signals is not fully understood. We have studied the involvement of GABA A-mediated inhibition in the processing of birdsong, a learned vocal communication signal requiring intact hearing for its development and maintenance. We focused on caudomedial nidopallium (NCM), an area analogous to parts of the mammalian auditory cortex with selective responses to birdsong. We present evidence that GABA A-mediated inhibition plays a pronounced role in NCM's auditory processing of birdsong. Using immunocytochemistry, we show that approximately half of NCM's neurons are GABAergic. Whole cell patch-clamp recordings in a slice preparation demonstrate that, at rest, spontaneously active GABAergic synapses inhibit excitatory inputs onto NCM neurons via GABA A receptors. Multi-electrode electrophysiological recordings in awake birds show that local blockade of GABA A-mediated inhibition in NCM markedly affects the temporal pattern of song-evoked responses in NCM without modifications in frequency tuning. Surprisingly, this blockade increases the phasic and largely suppresses the tonic response component, reflecting dynamic relationships of inhibitory networks that could include disinhibition. Thus processing of learned natural communication sounds in songbirds, and possibly other vocal learners, may depend on complex interactions of inhibitory networks.
To map the encoding of auditory cues in songbirds, multiunit electrophysiological responses to pure tone stimuli (250-5000 Hz) were recorded at 373 sites throughout the avian analogue of the mammalian auditory cortex in the caudal telencephalon of awake, restrained canaries. We found that a dorso-ventral tonotopic gradient from low to high frequency stimuli extends from the rostral field L2 to caudal-most caudo-medial nidopallium (NCM), similar to the frequency-dependent patterns of ZENK gene expression in canary NCM and to electrophysiological responses in other songbird species. However, response characteristics differ across the region. In field L2, responses are vigorous, phasic, and do not habituate to repeated presentations of the same stimulus. In an important subset of field L2 sites, tuning width narrows over the course of the response, which then terminates rapidly at stimulus offset. These properties are associated with inhibition at many nonpreferred frequencies and poststimulus inhibition at responsive frequencies. In contrast, NCM sites habituate to repeated sine waves, have wider tuning and lower amplitude responses, and rarely show inhibitory effects. Tuning curves in NCM are also flatter than those of field L2, and are often multipeaked. In addition, tuning width increases as the response unfolds and poststimulus excitation is often sustained in NCM. In sum, specific parts of the canary caudo-medial telencephalon differ in their response properties, suggesting differential roles in auditory processing. NCM properties, in particular, may allow for response integration across multiple spectrally varying stimulus elements, such as those that occur during birdsong.
Songbirds rely on auditory processing of natural communication signals for a number of social behaviors,including mate selection,individual recognition and the rare behavior of vocal learning - the ability to learn vocalizations through imitation of an adult model,rather than by instinct. Like mammals,songbirds possess a set of interconnected ascending and descending auditory brain pathways that process acoustic information and that are presumably involved in the perceptual processing of vocal communication signals. Most auditory areas studied to date are located in the caudomedial forebrain of the songbird and include the thalamo-recipient field L (sub fields L1,L2 and L3),the caudomedial and caudolateral mesopallium (CMM and CLM,respectively) and the caudomedial nidopallium (NCM). This review focuses on NCM,an auditory area previously proposed to be analogous to parts of the primary auditory cortex in mammals. Stimulation of songbirds with auditory stimuli drives vigorous electrophysiological responses and the expression of several activity-regulated genes in NCM.Interestingly,NCM neurons are tuned to species-specific songs and undergo some forms of experience-dependent plasticity in-vivo . These activity-dependent changes may underlie long-term modifications in the functional performance of NCM and constitute a potential neural substrate for auditory discrimination. We end this review by discussing evidence that suggests that NCM may be a site of auditory memory formation and/or storage.
BackgroundWhite-handed gibbons (Hylobates lar) are small Asian apes known for living in stable territories and producing loud, elaborate vocalizations (songs), often in well-coordinated male/female duets. The female great call, the most conspicuous phrase of the repertoire, has been hypothesized to function in intra-sexual territorial defense. We therefore predicted that characteristics of the great call would correlate with a caller’s physical condition, and thus might honestly reflect resource holding potential (RHP). Because measurement of RHP is virtually impossible for wild animals, we used age as a proxy, hypothesizing that great call climaxes are difficult to produce and maintain over time, and that older adults will therefore perform lower quality great calls than young adults. To test this we analyzed the great call climaxes of 15 wild lar gibbon females at Khao Yai National Park, Thailand and 2 captive females at Leo Conservation Center, Greenwich, CT.ResultsFindings show that call climaxes correlate with female age, as young animals (n = 8, mean age: 12.9 years) produced climaxes with a higher frequency range (delta F0), maximum F0 frequency and duty cycle than old animals (n = 9, mean age: 29.6 years). A permuted discriminant function analysis also correctly classified calls by age group. During long song bouts the maximum F0 frequency of great call climaxes’ also decreased. Additional data support the hypothesis that short high notes, associated with rapid inhalation as an individual catches its breath, reflect increased caller effort. Older females produced more high notes than younger females, but the difference only approached statistical significance, suggesting that calling effort may be similar across different ages. Finally, for the first time in this species, we measured peak intensity of calls in captive females. They were capable of producing climaxes in excess of 100 dB at close range (2.7 m).ConclusionsAge and within-bout differences in the lar gibbon great call climax suggest that call features correlate with physical condition and thus the call may have evolved as an honest signal in the context of intra-sexual territorial defense and possibly also in male mate choice via sexual selection, although further testing of these hypotheses is necessary.
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