Neural codes in the thalamocortical auditory system: From artificial stimuli to communication sounds

Huetz, Chloé; Gourévitch, Boris; Edeline, Jean‐Marc

doi:10.1016/j.heares.2010.01.010

Cited by 36 publications

(29 citation statements)

References 129 publications

(124 reference statements)

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“…In terms of coding timescale, the information about individuals is found in spike patterns on a shorter integration window (∼10 ms), whereas the information about distance is in the firing rate estimated over longer windows (∼30 ms). The fact that the best discrimination for identity is found with short time windows corroborates numerous studies showing that neurons use a spike timing strategy to encode vocalizations (Wang et al, 2007; Huetz et al, 2011; Gaucher et al, 2013; Elie and Theunissen, 2015) and is consistent with what was found previously for neural discrimination of conspecific song in the Field L of zebra finches (Narayan et al, 2006). These spike patterns might originate from processing a particular sequence of acoustic features, but additional neuronal mechanisms must be in place to preserve this information despite the natural variations in these acoustic features.…”

Section: Discussionsupporting

confidence: 89%

Single Neurons in the Avian Auditory Cortex Encode Individual Identity and Propagation Distance in Naturally Degraded Communication Calls

et al. 2017

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One of the most complex tasks performed by sensory systems is “scene analysis”: the interpretation of complex signals as behaviorally relevant objects. The study of this problem, universal to species and sensory modalities, is particularly challenging in audition, where sounds from various sources and localizations, degraded by propagation through the environment, sum to form a single acoustical signal. Here we investigated in a songbird model, the zebra finch, the neural substrate for ranging and identifying a single source. We relied on ecologically and behaviorally relevant stimuli, contact calls, to investigate the neural discrimination of individual vocal signature as well as sound source distance when calls have been degraded through propagation in a natural environment. Performing electrophysiological recordings in anesthetized birds, we found neurons in the auditory forebrain that discriminate individual vocal signatures despite long-range degradation, as well as neurons discriminating propagation distance, with varying degrees of multiplexing between both information types. Moreover, the neural discrimination performance of individual identity was not affected by propagation-induced degradation beyond what was induced by the decreased intensity. For the first time, neurons with distance-invariant identity discrimination properties as well as distance-discriminant neurons are revealed in the avian auditory cortex. Because these neurons were recorded in animals that had prior experience neither with the vocalizers of the stimuli nor with long-range propagation of calls, we suggest that this neural population is part of a general-purpose system for vocalizer discrimination and ranging.SIGNIFICANCE STATEMENT Understanding how the brain makes sense of the multitude of stimuli that it continually receives in natural conditions is a challenge for scientists. Here we provide a new understanding of how the auditory system extracts behaviorally relevant information, the vocalizer identity and its distance to the listener, from acoustic signals that have been degraded by long-range propagation in natural conditions. We show, for the first time, that single neurons, in the auditory cortex of zebra finches, are capable of discriminating the individual identity and sound source distance in conspecific communication calls. The discrimination of identity in propagated calls relies on a neural coding that is robust to intensity changes, signals' quality, and decreases in the signal-to-noise ratio.

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Section: Discussionsupporting

confidence: 89%

Single Neurons in the Avian Auditory Cortex Encode Individual Identity and Propagation Distance in Naturally Degraded Communication Calls

et al. 2017

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“…These investigations in model systems led to the discovery of cricket-song selective neurons and their contribution to the females' phonotaxis behavior [77], of call selective neurons in frogs [78] and guinea pigs [79], of song selective neurons in songbirds [7,[80][81][82], of neurons selective to the echolocation signal in bats [5], and of brain regions selective for conspecific calls in primates [83]. Selectivity for conspecific communication calls can be reflected not only in the mean rate of single neurons but also (and sometimes only) in time-varying responses [84,85] or ensemble responses [86,87]. Thus, the auditory system is not only selective to natural sounds in a broad sense but appears to also exhibit specialized circuitry for the sole purpose of detecting and processing conspecific communication calls.…”

Section: Animal Vocalizationsmentioning

confidence: 99%

Neural processing of natural sounds

2014

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Natural sounds have unique statistical structure that makes them perceptually salient. The auditory system is finely tuned to this natural structure. Selective neurons found at the higher levels of the auditory system respond selectively to vocalizations used in communication. On-line Summary1. Natural sounds include animal vocalizations, environmental sounds such as wind, water and fire noises and non-vocal sounds made by animals and humans for communication. These natural sounds have characteristic statistical properties that make them perceptually salient and that drive auditory neurons in optimal regimes for information transmission. 2.Recent advances in statistics and computer sciences have allowed neuro-physiologists to extract the stimulus-response function of complex auditory neurons from responses to natural sounds. These studies have shown a hierarchical processing that leads to the neural detection of progressively more complex natural sound features and have demonstrated the importance of the acoustical and behavioral contexts for the neural responses.3. High-level auditory neurons have shown to be exquisitely selective for conspecific calls.This fine selectivity could play an important role for species recognition, for vocal learning in songbirds and, in the case of the bats, for the processing of the sounds used in echolocation. Research that investigates how communication sounds are categorized into behaviorally meaningful groups (e.g. call types in animals, words in human speech) remains in its infancy. Animals and humans also excel at separating communication sounds from each otherand from background noise. Neurons that detect communication calls in noise have been found but the neural computations involved in sound source separation and natural auditory scene analysis remain overall poorly understood. Thus, future auditory research will have to focus not only on how natural sounds are processed by the auditory system but also on the computations that allow for this processing to occur in natural listening situations. 5.The complexity of the computations needed in the natural hearing task might require a high-dimensional representation provided by ensemble of neurons and the use of natural sounds might be the best solution for understanding the ensemble neural code.The final publication is available at Nature via http://www.nature.com/nrn/journal/v15/n6/full/nrn3731.html PrefaceWe might be forced to listen to a high frequency tone at our audiologist's office or we might enjoy falling asleep with a white-noise machine but the sounds that really matter to us are the voices of our companions or music from our favorite radio station; the auditory system has evolved to process behaviorally relevant natural sounds. Research has shown not only that our brain is optimized for natural hearing tasks but also that using natural sounds to probe the auditory system is the best way to understand the neural computations that allow us to comprehend speech or appreciate music.

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“…Besides the somatosensory network, the auditory thalamocortical system is also extensively studied (Huetz et al 2011;Imaizumi and Lee 2014;Lee 2013;Winer et al 2005). However, it is challenging to record simultaneously the activity of the auditory thalamus (medial geniculate body, MGB) and the auditory cortex (AC) because of the lateral location of the AC and the relatively small size of the MGB.…”

Section: Tonotopic Mapping In the Auditory Thalamus Of Ratsmentioning

confidence: 99%

Large-scale recording of thalamocortical circuits: in vivo electrophysiology with the two-dimensional electronic depth control silicon probe

Fiáth

Beregszászi

Horváth

et al. 2016

Journal of Neurophysiology

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Fiáth R, Beregszászi P, Horváth D, Wittner L, Aarts AA, Ruther P, Neves HP, Bokor H, Acsády L, Ulbert I. Large-scale recording of thalamocortical circuits: in vivo electrophysiology with the two-dimensional electronic depth control silicon probe. J Neurophysiol 116: 2312-2330. First published August 17, 2016 doi:10.1152/jn.00318.2016.-Recording simultaneous activity of a large number of neurons in distributed neuronal networks is crucial to understand higher order brain functions. We demonstrate the in vivo performance of a recently developed electrophysiological recording system comprising a two-dimensional, multi-shank, high-density silicon probe with integrated complementary metal-oxide semiconductor electronics. The system implements the concept of electronic depth control (EDC), which enables the electronic selection of a limited number of recording sites on each of the probe shafts. This innovative feature of the system permits simultaneous recording of local field potentials (LFP) and single-and multiple-unit activity (SUA and MUA, respectively) from multiple brain sites with high quality and without the actual physical movement of the probe. To evaluate the in vivo recording capabilities of the EDC probe, we recorded LFP, MUA, and SUA in acute experiments from cortical and thalamic brain areas of anesthetized rats and mice. The advantages of large-scale recording with the EDC probe are illustrated by investigating the spatiotemporal dynamics of pharmacologically induced thalamocortical slow-wave activity in rats and by the two-dimensional tonotopic mapping of the auditory thalamus. In mice, spatial distribution of thalamic responses to optogenetic stimulation of the neocortex was examined. Utilizing the benefits of the EDC system may result in a higher yield of useful data from a single experiment compared with traditional passive multielectrode arrays, and thus in the reduction of animals needed for a research study. electronic depth control; silicon probe; high-density recording; thalamocortical oscillation; optogenetics DESPITE THE RAPID ADVANCEMENT of brain imaging techniques offering both high spatial and temporal resolution, electrophysiological tools are still widely used methods to investigate the complex spatiotemporal activity patterns of neuronal circuits. Over the past few decades, single-wire electrodes used for in vivo extracellular recording of action potentials evolved into multielectrode arrays covering the range of up to 1,000 recording sites NEW & NOTEWORTHY Recording the electrical activity of a large number of neurons located in the thalamocortical

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Neural codes in the thalamocortical auditory system: From artificial stimuli to communication sounds

Cited by 36 publications

References 129 publications

Single Neurons in the Avian Auditory Cortex Encode Individual Identity and Propagation Distance in Naturally Degraded Communication Calls

Single Neurons in the Avian Auditory Cortex Encode Individual Identity and Propagation Distance in Naturally Degraded Communication Calls

Neural processing of natural sounds

Large-scale recording of thalamocortical circuits: in vivo electrophysiology with the two-dimensional electronic depth control silicon probe

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