Robust Neuronal Discrimination in Primary Auditory Cortex Despite Degradations of Spectro-temporal Acoustic Details: Comparison Between Guinea Pigs with Normal Hearing and Mild Age-Related Hearing Loss

International audienceThis study investigated to which extent the primary auditory cortex of young normal-hearing and mild hearing-impaired aged animals is able to maintain invariant representation of critical temporal-modulation features when sounds are submitted to degradations of fine spectro-temporal acoustic details. This was achieved by recording ensemble of cortical responses to conspecific vocalizations in guinea pigs with either normal hearing or mild age-related sensorineural hearing loss. The vocalizations were degraded using a tone vocoder. The neuronal responses and their discrimination capacities (estimated by mutual information) were analyzed at single recording and population levels. For normal-hearing animals, the neuronal responses decreased as a function of the number of the vocoder frequency bands, so did their discriminative capacities at the single recording level. However, small neuronal populations were found to be robust to the degradations induced by the vocoder. Similar robustness was obtained when broadband noise was added to exacerbate further the spectro-temporal distortions produced by the vocoder. A comparable pattern of robustness to degradations in fine spectro-temporal details was found for hearing-impaired animals. However, the latter showed an overall decrease in neuronal discrimination capacities between vocalizations in noisy conditions. Consistent with previous studies, these results demonstrate that the primary auditory cortex maintains robust neural representation of temporal envelope features for communication sounds under a large range of spectro-temporal degradations

Acoustic sequences in non-human animals: a tutorial review and prospectus.

Animal acoustic communication often takes the form of complex sequences, made up of multiple distinct acoustic units. Apart from the well-known example of birdsong, other animals such as insects, amphibians, and mammals (including bats, rodents, primates, and cetaceans) also generate complex acoustic sequences. Occasionally, such as with birdsong, the adaptive role of these sequences seems clear (e.g. mate attraction and territorial defence). More often however, researchers have only begun to characterise - let alone understand - the significance and meaning of acoustic sequences. Hypotheses abound, but there is little agreement as to how sequences should be defined and analysed. Our review aims to outline suitable methods for testing these hypotheses, and to describe the major limitations to our current and near-future knowledge on questions of acoustic sequences. This review and prospectus is the result of a collaborative effort between 43 scientists from the fields of animal behaviour, ecology and evolution, signal processing, machine learning, quantitative linguistics, and information theory, who gathered for a 2013 workshop entitled, 'Analysing vocal sequences in animals'. Our goal is to present not just a review of the state of the art, but to propose a methodological framework that summarises what we suggest are the best practices for research in this field, across taxa and across disciplines. We also provide a tutorial-style introduction to some of the most promising algorithmic approaches for analysing sequences. We divide our review into three sections: identifying the distinct units of an acoustic sequence, describing the different ways that information can be contained within a sequence, and analysing the structure of that sequence. Each of these sections is further subdivided to address the key questions and approaches in that area. We propose a uniform, systematic, and comprehensive approach to studying sequences, with the goal of clarifying research terms used in different fields, and facilitating collaboration and comparative studies. Allowing greater interdisciplinary collaboration will facilitate the investigation of many important questions in the evolution of communication and sociality.This review was developed at an investigative workshop, “Analyzing Animal Vocal Communication Sequences” that took place on October 21–23 2013 in Knoxville, Tennessee, sponsored by the National Institute for Mathematical and Biological Synthesis (NIMBioS). NIMBioS is an Institute sponsored by the National Science Foundation, the U.S. Department of Homeland Security, and the U.S. Department of Agriculture through NSF Awards #EF-0832858 and #DBI-1300426, with additional support from The University of Tennessee, Knoxville. In addition to the authors, Vincent Janik participated in the workshop. D.T.B.’s research is currently supported by NSF DEB-1119660. M.A.B.’s research is currently supported by NSF IOS-0842759 and NIH R01DC009582. M.A.R.’s research is supported by ONR N0001411IP20086 and NOPP (ONR/BOEM) N00014-11-1-0697. S.L.DeR.’s research is supported by the U.S. Office of Naval Research. R.F.-i-C.’s research was supported by the grant BASMATI (TIN2011-27479-C04-03) from the Spanish Ministry of Science and Innovation. E.C.G.’s research is currently supported by a National Research Council postdoctoral fellowship. E.E.V.’s research is supported by CONACYT, Mexico, award number I010/214/2012.This is the accepted manuscript. The final version is available at http://dx.doi.org/10.1111/brv.1216

Bioacoustics approaches to locate and identify animals in terrestrial environments. In "Sensors for Ecology". (F. Gaill, Y. Lagadeuc and J-F. Le Galliard eds)

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From the receptive field dynamics to the rate of transmitted information : some facets of the thalamo-cortical auditory system.

In this article, we first evaluate the literature describing reorganizations of auditory cortex topography after behavioral training. We then review the studies showing that receptive fields of auditory thalamocortical neurons express large dynamics in unanesthetized animals. During the time course of different behavioral training protocols, the frequency tuning curves of thalamocortical neurons can be selectively modified to code for the learned importance of acoustic stimuli. In other circumstances, when the vigilance state shifts from waking to sleep, the functional properties of thalamic and cortical neurons exhibit drastic modifications. Finally, we point out new lines of research. First, investigations describing the responses of neurons to communication signals (e.g. species-specific vocalizations) are important because they reveal how the thalamocortical auditory system processes biologically relevant sounds. Second, we suggest that the spike timing precision can largely increase the amount of information transmitted in the thalamocortical auditory system. This urges for more systematic studies in which the temporal organization of spike trains will be considered at presentation of natural stimuli

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

International audienceOver the last 15 years, an increasing number of studies have described the responsiveness of thalamic and cortical neurons to communication sounds. Whereas initial studies have simply looked for neurons exhibiting higher firing rate to conspecific vocalizations over their modified, artificially synthesized versions, more recent studies determine the relative contribution of "rate coding" and "temporal coding" to the information transmitted by spike trains. In this article, we aim at reviewing the different strategies employed by thalamic and cortical neurons to encode information about acoustic stimuli, from artificial to natural sounds. Considering data obtained with simple stimuli, we first illustrate that different facets of temporal code, ranging from a strict correspondence between spike-timing and stimulus temporal features to more complex coding strategies, do already exist with artificial stimuli. We then review lines of evidence indicating that spike-timing provides an efficient code for discriminating communication sounds from thalamus, primary and non-primary auditory cortex up to frontal areas. As the neural code probably developed, and became specialized, over evolution to allow precise and reliable processing of sounds that are of survival value, we argue that spike-timing based coding strategies might set the foundations of our perceptive abilities

Differences between spectro-temporal receptive fields derived from artificial and natural stimuli in the auditory cortex.

International audienceSpectro-temporal properties of auditory cortex neurons have been extensively studied with artificial sounds but it is still unclear whether they help in understanding neuronal responses to communication sounds. Here, we directly compared spectro-temporal receptive fields (STRFs) obtained from the same neurons using both artificial stimuli (dynamic moving ripples, DMRs) and natural stimuli (conspecific vocalizations) that were matched in terms of spectral content, average power and modulation spectrum. On a population of auditory cortex neurons exhibiting reliable tuning curves when tested with pure tones, significant STRFs were obtained for 62% of the cells with vocalizations and 68% with DMR. However, for many cells with significant vocalization-derived STRFs (STRF(voc)) and DMR-derived STRFs (STRF(dmr)), the BF, latency, bandwidth and global STRFs shape differed more than what would be predicted by spiking responses simulated by a linear model based on a non-homogenous Poisson process. Moreover STRF(voc) predicted neural responses to vocalizations more accurately than STRF(dmr) predicted neural response to DMRs, despite similar spike-timing reliability for both sets of stimuli. Cortical bursts, which potentially introduce nonlinearities in evoked responses, did not explain the differences between STRF(voc) and STRF(dmr). Altogether, these results suggest that the nonlinearity of auditory cortical responses makes it difficult to predict responses to communication sounds from STRFs computed from artificial stimuli

Neural correlates of moderate hearing loss: time course of response changes in the primary auditory cortex of awake guinea-pigs

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Neural representations during sleep : from sensory processing to memory traces.

In the course of a day, the brain undergoes large-scale changes in functional modes, from attentive wakefulness to the deepest stage of sleep. The present paper evaluates how these state changes affect the neural bases of sensory and cognitive representations. Are organized neural representations still maintained during sleep? In other words, despite the absence of conscious awareness, do neuronal signals emitted during sleep contain information and have a functional relevance? Through a critical evaluation of the animal and human literature, neural representations at different levels of integration (from the most elementary sensory level to the most cognitive one) are reviewed. Recordings of neuronal activity in animals at presentation of neutral or significant stimuli show that some analysis of the external word remains possible during sleep, allowing recognition of behaviorally relevant stimuli. Event-related brain potentials in humans confirm the preservation of some sensory integration and discriminative capacity. Behavioral and neuroimaging studies in humans substantiate the notion that memory representations are reactivated and are reorganized during post-learning sleep; these reorganisations may account for the beneficial effects of sleep on behavioral performance. Electrophysiological results showing replay of neuronal sequences in animals are presented, and their relevance as neuronal correlates of memory reactivation is discussed. The reviewed literature provides converging evidence that structured neural representations can be activated during sleep. Which reorganizations unique to sleep benefit memory representations, and to what extent the operations still efficient in processing environmental information during sleep are similar to those underlying the non-conscious, automatic processing continually at work in wakefulness, are challenging questions open to investigation

A spike timing code for discriminating conspecific vocalizations in the thalamocortical system of anesthetized and awake guinea-pigs.

International audienceUnderstanding how communication sounds are processed and encoded in the central auditory system is critical to understanding the neural bases of acoustic communication. Here, we examined neuronal representations of species-specific vocalizations, which are communication sounds that many species rely on for survival and social interaction. In some species, the evoked responses of auditory cortex neurons are stronger in response to natural conspecific vocalizations than to their time-reversed, spectrally identical, counterparts. We applied information theory-based analyses to single-unit spike trains collected in the auditory cortex (n = 139) and auditory thalamus (n = 135) of anesthetized animals as well as in the auditory cortex (n = 119) of awake guinea pigs during presentation of four conspecific vocalizations. Few thalamic and cortical cells (75%) displayed a significant amount of information (i.e., >2SD above chance levels), especially in the awake condition. The computed correlation index between spike trains (R(corr), defined by Schreiber et al., 2003) indicated similar spike-timing reliability for both the natural and time-reversed versions of each vocalization, but higher reliability for awake animals compared with anesthetized animals. Based on temporal discharge patterns, even cells that were only weakly responsive to vocalizations displayed a significant level of information. These findings emphasize the importance of temporal discharge patterns as a coding mechanism for natural communication sounds, particularly in awake animals