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

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

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

International audienc

Etude du code neuronal sous-tendant la perception de signaux de communication acoustique

Un des objectifs des neurosciences computationelles consiste à élucider le code neuronal utilisé dans le système nerveux central pour représenter l information et élaborer des réponses adaptées à ces stimuli. Tandis que le taux de décharge des neurones reste très utilisé dans les travaux explorant les relations entre activité neuronale et fonctions cognitives, de plus en plus de recherches montrent que les aspects temporels des décharges neuronales pourraient constituer un code rapide et efficace de l information. J ai étudié des enregistrements électrophysiologiques collectés dans une structure du cerveau de canaris impliquée dans la perception et la production des chants. Alors qu une minorité de ces neurones sont sélectifs pour le propre chant de l oiseau en terme de taux de décharge, les réponses d une majorité d entre eux portent l information nécessaire à la discrimination entre le propre chant et son inverse, cette information étant majoritairement portée par les aspects temporels des décharges. Nous avons ensuite analysé des enregistrements obtenus dans le système thalamocortical de cobayes lors de la présentation de vocalisations conspécifiques. Alors que ces stimuli déclenchent des réponses similaires du point de vue du nombre de PA, la quantité d information transmise par l organisation temporelle des PA est importante. Tant dans le système thalamocortical que dans un noyau sensorimoteur, les neurones semblent donc émettre des séquences de PA dont l organisation temporelle est bien mieux corrélée avec les stimuli que le nombre de PA. Cette propriété dynamique de l activité neuronale pourrait donc être impliquée dans la perception de stimuli naturels.A major goal in computational neuroscience is to understand the neural code used to represent perceptual information and elaborate appropriate motor responses. Whereas most of the researches about relationships between neural activity and cognitives functions still focus on the discharge rate, a growing number of studies show that spike timing could constitute a rapid and efficient neural code. We studied spike trains recorded in the HVC nucleus, brain s structure involved in the perception and the production of songs in songbirds. Whereas a minority of neurons were selective in terms of spike rate, it appeared that spike timing carried the information required to disriminate between the bird s own song and its reverse. We then studied auditory thalamocortical spike trains recorded during the presentation of conspecific vocalizations. In that case also, spike timing conveys information allowing the discrimination between vocalizations and their time-reversed versions whereas spike rate was similar for both stimuli. An analysis of the first 100ms of the spike trains revealed that first spike latency conveyed twice more information that spike count for a discrimination between vocalizations in their natural version. Therefore, in the thalamocortical auditory system as well as in a sensorimotor nucleus, neurons seem to emit temporal patterns of spikes that better correlate with sensory stimuli than spike count does. This dynamic property of neural activity may thus be involved in the perception of naturalistic stimuli.ORSAY-PARIS 11-BU Sciences (914712101) / SudocSudocFranceF

Can Extensive Training Transform a Mouse into a Guinea Pig? An Evaluation Based on the Discriminative Abilities of Inferior Colliculus Neurons

Humans and animals maintain accurate discrimination between communication sounds in the presence of loud sources of background noise. In previous studies performed in anesthetized guinea pigs, we showed that, in the auditory pathway, the highest discriminative abilities between conspecific vocalizations were found in the inferior colliculus. Here, we trained CBA/J mice in a Go/No-Go task to discriminate between two similar guinea pig whistles, first in quiet conditions, then in two types of noise, a stationary noise and a chorus noise at three SNRs. Control mice were passively exposed to the same number of whistles as trained mice. After three months of extensive training, inferior colliculus (IC) neurons were recorded under anesthesia and the responses were quantified as in our previous studies. In quiet, the mean values of the firing rate, the temporal reliability and mutual information obtained from trained mice were higher than from the exposed mice and the guinea pigs. In stationary and chorus noise, there were only a few differences between the trained mice and the guinea pigs; and the lowest mean values of the parameters were found in the exposed mice. These results suggest that behavioral training can trigger plasticity in IC that allows mice neurons to reach guinea pig-like discrimination abilities

Differences between Spectro-Temporal Receptive Fields Derived from Artificial and Natural Stimuli in the Auditory Cortex

<div><p>Spectro-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.</p> </div

What Is the Benefit of Ramped Pulse Shapes for Activating Auditory Cortex Neurons? An Electrophysiological Study in an Animal Model of Cochlear Implant

In all commercial cochlear implant (CI) devices, the activation of auditory nerve fibers is performed with rectangular pulses that have two phases of opposite polarity. Recently, several papers proposed that ramped pulse shapes could be an alternative shape for efficiently activating auditory nerve fibers. Here, we investigate whether ramped pulse shapes can activate auditory cortex (ACx) neurons in a more efficient way than the classical rectangular pulses. Guinea pigs were implanted with CI devices and responses of ACx neurons were tested with rectangular pulses and with four ramped pulse shapes, with a first-phase being either cathodic or anodic. The thresholds, i.e., the charge level necessary for obtaining significant cortical responses, were almost systematically lower with ramped pulses than with rectangular pulses. The maximal firing rate (FR) elicited by the ramped pulses was higher than with rectangular pulses. As the maximal FR occurred with lower charge levels, the dynamic range (between threshold and the maximal FR) was not modified. These effects were obtained with cathodic and anodic ramped pulses. By reducing the charge levels required to activate ACx neurons, the ramped pulse shapes should reduce charge consumption and should contribute to more battery-efficient CI devices in the future

Characteristics of the cells exhibiting significant STRF compared with those exhibiting no significant STRF using vocalizations and Dynamic Moving Ripples (DMRs).

<p>Unpaired t-tests were used to determine if the parameters differed between these 2 types of cells.</p