Dataset Information

Inhibitory network interactions shape the auditory processing of natural communication signals in the songbird auditory forebrain.

ABSTRACT: 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.

SUBMITTER: Pinaud R

PROVIDER: S-EPMC2493480 | biostudies-literature | 2008 Jul

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Inhibitory network interactions shape the auditory processing of natural communication signals in the songbird auditory forebrain.

Pinaud Raphael R Terleph Thomas A TA Tremere Liisa A LA Phan Mimi L ML Dagostin André A AA Leão Ricardo M RM Mello Claudio V CV Vicario David S DS

Journal of neurophysiology 20080514 1

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 pronounce ...[more]

PMID: 18480371

Similar Datasets

Project description:Deviants are stimuli that violate one's prediction about the incoming stimuli. Studying deviance detection helps us understand how nervous system learns temporal patterns between stimuli and forms prediction about the future. Detecting deviant stimuli is also critical for animals' survival in the natural environment filled with complex sounds and patterns. Using natural songbird vocalizations as stimuli, we recorded multi-unit and single-unit activity from the zebra finch auditory forebrain while presenting rare repeated stimuli after regular alternating stimuli (alternating oddball experiment) or rare deviant among multiple different common stimuli (context oddball experiment). The alternating oddball experiment showed that neurons were sensitive to rare repetitions in regular alternations. In the absence of expectation, repetition suppresses neural responses to the 2nd stimulus in the repetition. When repetition violates expectation, neural responses to the 2nd stimulus in the repetition were stronger than expected. The context oddball experiment showed that a stimulus elicits stronger neural responses when it is presented infrequently as a deviant among multiple common stimuli. As the acoustic differences between deviant and common stimuli increase, the response enhancement also increases. These results together showed that neural encoding of a stimulus depends not only on the acoustic features of the stimulus but also on the preceding stimuli and the transition patterns between them. These results also imply that the classical oddball effect may result from a combination of repetition suppression and deviance enhancement. Classification analyses showed that the difficulties in decoding the stimulus responsible for the neural responses differed for deviants in different experimental conditions. These findings suggest that learning transition patterns and detecting deviants in natural sequences may depend on a hierarchy of neural mechanisms, which may be involved in more complex forms of auditory processing that depend on the transition patterns between stimuli, such as speech processing.

Project description:Sensory responses to courtship signals can be altered by reproductive hormones. In seasonally-breeding female songbirds, for example, sound-induced immediate early gene expression in the auditory pathway is selective for male song over behaviourally irrelevant sounds only when plasma estradiol reaches breeding-like levels. This selectivity has been hypothesized to be mediated by release of monoaminergic neuromodulators in the auditory pathway. We previously showed that in oestrogen-primed female white-throated sparrows, exposure to male song induced dopamine and serotonin release in auditory regions. In order to mediate hormone-dependent selectivity, this release must be (1) selective for song and (2) modulated by endocrine state. Therefore, in the current study we addressed both questions by conducting playbacks of song or a control sound to females in a breeding-like or non-breeding endocrine state. We then used high performance liquid chromatography to measure turnover of dopamine, norepinephrine, and serotonin in the auditory midbrain and forebrain. We found that sound-induced turnover of dopamine and serotonin did in fact depend on endocrine state; hearing sound increased turnover in the auditory forebrain only in the birds in a breeding-like endocrine state. Contrary to our expectations, these increases occurred in response to either song or artificial tones; in other words, they were not selective for song. The selectivity of sound-induced monoamine release was thus strikingly different from that of immediate early gene responses described in previous studies. We did, however, find that constitutive monoamine release was altered by endocrine state; whether the birds heard sound or not, turnover of serotonin in the auditory forebrain was higher in a breeding-like state than in a non-breeding endocrine state. Our results suggest that dopaminergic and serotonergic responses to song and other sounds, as well as serotonergic tone in auditory areas, could be seasonally modulated. This article is protected by copyright. All rights reserved.

Project description:It is increasingly recognized that brain-derived estrogens (neuroestrogens) can regulate brain physiology and behavior much faster than what was previously known from the transcriptional action of estrogens on nuclear receptors. One of the best examples of such neuromodulation by neuroestrogens concerns the acute regulation of sensory coding by the auditory cortex as demonstrated by electrophysiological studies of selected neurons in zebra finches. Yet, the spatial extent of such modulation by neuroestrogens is not known. Using functional magnetic resonance imaging, we demonstrate here that acute estrogen depletion alters within minutes auditory processing in male European starlings. These effects are confined to very specific but large areas of the auditory cortex. They are also specifically lateralized to the left hemisphere. Interestingly, the modulation of auditory responses by estrogens was much larger (both in amplitude and in topography) in March than in December or May/June. This effect was presumably independent from changes in circulating testosterone concentrations since levels of the steroid were controlled by subcutaneous implants, thus suggesting actions related to other aspects of the seasonal cycle or photoperiodic manipulations. Finally, we also show that estrogen production specifically modulates selectivity for behaviorally relevant vocalizations in a specific part of the caudomedial nidopallium. These findings confirm and extend previous conclusions that had been obtained by electrophysiological techniques. This approach provides a new very powerful tool to investigate auditory responsiveness in songbirds and its fast modulation by sex steroids.SIGNIFICANCE STATEMENT Neuroestrogens can acutely modulate sensory processing in a manner similar to neuromodulators. We report that acute estrogen depletion rapidly disrupts auditory processing in large areas of the male starling brain. Effects were larger in March than in December or May/June, lateralized to the left hemisphere and specific to behaviorally relevant stimuli. These findings confirm and extend previous data that identified an acute regulation of auditory neurons in zebra finches by (1) delineating the extent of the brain region affected, (2) confirming its lateralization, and (3) demonstrating that a large part of the auditory brain regions are acutely affected by estrogens. These findings provide a very powerful tool to investigate auditory responsiveness in songbirds and its fast modulation by sex steroids.

Dataset Information

Inhibitory network interactions shape the auditory processing of natural communication signals in the songbird auditory forebrain.

Publications

Inhibitory network interactions shape the auditory processing of natural communication signals in the songbird auditory forebrain.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets