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.

First Description of the Underwater Sounds in the Mediterranean Monk Seal Monachus monachus in Greece: Towards Establishing a Vocal Repertoire.

The Mediterranean monk seal Monachus monachus is one of the most endangered pinnipeds in the world, and is classified as "Endangered" by the International Union for the Conservation of Nature. Any additional knowledge about the species is invaluable to its effective conservation. In the present study, we deployed an autonomous underwater recorder in an important reproductive area of the Mediterranean monk seal in Greece to describe its underwater vocal repertoire. Over the 330 h of continuous recordings, 9231 vocalizations were labelled as potentially produced by Mediterranean monk seals, and 1694 good quality calls were analyzed. We defined 18 call types divided into three main call categories: harmonic, noisy, and pulsative calls. We also described the soundscape in which this endangered species lives and found that human activities around the two main pupping caves had a strong impact on the sonic environment of these seals: the noise level produced by boat traffic was high, and occurred on an hourly (25 to 50 min/hour) and daily basis (10.8 to 16.9 h/day). Such high levels of noise might not only impair the communication of the species, but also impact its survival, as chronic noise can induce physiological stress.

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.

Reduction in sound discrimination in noise is related to envelope similarity and not to a decrease in envelope tracking abilities.

Humans and animals constantly face challenging acoustic environments, such as various background noises, that impair the detection, discrimination and identification of behaviourally relevant sounds. Here, we disentangled the role of temporal envelope tracking in the reduction in neuronal and behavioural discrimination between communication sounds in situations of acoustic degradations. By collecting neuronal activity from six different levels of the auditory system, from the auditory nerve up to the secondary auditory cortex, in anaesthetized guinea-pigs, we found that tracking of slow changes of the temporal envelope is a general functional property of auditory neurons for encoding communication sounds in quiet conditions and in adverse, challenging conditions. Results from a go/no-go sound discrimination task in mice support the idea that the loss of distinct slow envelope cues in noisy conditions impacted the discrimination performance. Together, these results suggest that envelope tracking is potentially a universal mechanism operating in the central auditory system, which allows the detection of any between-stimulus difference in the slow envelope and thus copes with degraded conditions. KEY POINTS: In quiet conditions, envelope tracking in the low amplitude modulation range (<20 Hz) is correlated with the neuronal discrimination between communication sounds as quantified by mutual information from the cochlear nucleus up to the auditory cortex. At each level of the auditory system, auditory neurons retain their abilities to track the communication sound envelopes in situations of acoustic degradation, such as vocoding and the addition of masking noises up to a signal-to-noise ratio of -10 dB. In noisy conditions, the increase in between-stimulus envelope similarity explains the reduction in both behavioural and neuronal discrimination in the auditory system. Envelope tracking can be viewed as a universal mechanism that allows neural and behavioural discrimination as long as the temporal envelope of communication sounds displays some differences.

Social calls in humpback whale mother-calf groups off Sainte Marie breeding ground (Madagascar, Indian Ocean).

Humpback whales (Megaptera novaeangliae) use vocalizations during diverse social interactions or activities such as foraging or mating. Unlike songs produced only by males, social calls are produced by all types of individuals (adult males and females, juveniles and calves). Several studies have described social calls in the humpback whale's breeding and the feeding grounds and from different geographic areas. We aimed to investigate for the first time the vocal repertoire of humpback whale mother-calf groups during the breeding season off Sainte Marie island, Madagascar, South Western Indian Ocean using data collected in 2013, 2014, 2016, and 2017. We recorded social calls using Acousonde tags deployed on the mother or the calf in mother-calf groups. A total of 21 deployments were analyzed. We visually and aurally identified 30 social call types and classified them into five categories: low, medium, high-frequency sounds, amplitude-modulated sounds, and pulsed sounds. The aural-visual classifications have been validated using random forest (RF) analyses. Low-frequency sounds constituted 46% of all social calls, mid-frequency 35%, and high frequency 10%. Amplitude-modulated sounds constituted 8% of all vocalizations, and pulsed sounds constituted 1%. While some social call types seemed specific to our study area, others presented similarities with social calls described in other geographic areas, on breeding and foraging grounds, and during migrating routes. Among the call types described in this study, nine call types were also found in humpback whale songs recorded in the same region. The 30 call types highlight the diversity of the social calls recorded in mother-calf groups and thus the importance of acoustic interactions in the relationships between the mother and her calf and between the mother-calf pair and escorts.

Characterizing the suckling behavior by video and 3D-accelerometry in humpback whale calves on a breeding ground.

Getting maternal milk through nursing is vital for all newborn mammals. Despite its importance, nursing has been poorly documented in humpback whales (Megaptera novaeangliae). Nursing is difficult to observe underwater without disturbing the whales and is usually impossible to observe from a ship. We attempted to observe nursing from the calf's perspective by placing CATS cam tags on three humpback whale calves in the Sainte Marie channel, Madagascar, Indian Ocean, during the breeding seasons. CATS cam tags are animal-borne multi-sensor tags equipped with a video camera, a hydrophone, and several auxiliary sensors (including a 3-axis accelerometer, a 3-axis magnetometer, and a depth sensor). The use of multi-sensor tags minimized potential disturbance from human presence. A total of 10.52 h of video recordings were collected with the corresponding auxiliary data. Video recordings were manually analyzed and correlated with the auxiliary data, allowing us to extract different kinematic features including the depth rate, speed, Fluke Stroke Rate (FSR), Overall Body Dynamic Acceleration (ODBA), pitch, roll, and roll rate. We found that suckling events lasted 18.8 ± 8.8 s on average (N = 34) and were performed mostly during dives. Suckling events represented 1.7% of the total observation time. During suckling, the calves were visually estimated to be at a 30-45° pitch angle relative to the midline of their mother's body and were always observed rolling either to the right or to the left. In our auxiliary dataset, we confirmed that suckling behavior was primarily characterized by a high average absolute roll and additionally we also found that it was likely characterized by a high average FSR and a low average speed. Kinematic features were used for supervised machine learning in order to subsequently detect suckling behavior automatically. Our study is a proof of method on which future investigations can build upon. It opens new opportunities for further investigation of suckling behavior in humpback whales and the baleen whale species.

Acoustic behaviour of bottlenose dolphins under human care while performing synchronous aerial jumps.

Synchronous behaviours occur when two or more animals display the same behaviour at the same time. However, the mechanisms underlying this synchrony are not well understood. In this study, we carried out an experiment to determine whether or not Bottlenose dolphins use acoustic cues when performing a known synchronised exercise. For this, we recorded three dolphins while they performed requested aerial jumps both individually or synchronously in pairs, with a hydrophone array and a 360° underwater video camera allowing the identification of the subject emitting vocalisations. Results indicated that in pairs, dolphins synchronised their jumps 100% of the time. Whether they jumped alone or in pairs, they produced click trains before and after 92% of jumps. No whistles or burst-pulsed sounds were emitted by the animals during the exercise. The acoustic localisation process allowed the successful identification of the vocalising subject in 19.8% of all cases (N = 141). Our study showed that in all (n = 28) but one successful localisations, the click trains were produced by the same individual. It is worth noting that this individual was the oldest female of the group. This paper provides evidence suggesting that during synchronous behaviours, dolphins use acoustic cues, and more particularly click trains, to coordinate their movements; possibly by eavesdropping on the clicks or echoes produced by one individual leading the navigation.

Enhanced Discriminative Abilities of Auditory Cortex Neurons for Pup Calls Despite Reduced Evoked Responses in C57BL/6 Mother Mice.

A fundamental task for the auditory system is to process communication sounds according to their behavioral significance. In many mammalian species, pup calls became more significant for mothers than other conspecific and heterospecific communication sounds. To study the cortical consequences of motherhood on the processing of communication sounds, we recorded neuronal responses in the primary auditory cortex of virgin and mother C57BL/6 mice which had similar ABR thresholds. In mothers, the evoked firing rate in response to pure tones was decreased and the frequency receptive fields were narrower. The responses to pup and adult calls were also reduced but the amount of mutual information (MI) per spike about the pup call's identity was increased in mother mice. The response latency to pup and adult calls was significantly shorter in mothers. Despite similarly decreased responses to guinea pig whistles, the response latency, and the MI per spike did not differ between virgins and mothers for these heterospecific vocalizations. Noise correlations between cortical recordings were decreased in mothers, suggesting that the firing rate of distant neurons was more independent from each other. Together, these results indicate that in the most commonly used mouse strain for behavioral studies, the discrimination of pup calls by auditory cortex neurons is more efficient during motherhood.

Noise-Sensitive But More Precise Subcortical Representations Coexist with Robust Cortical Encoding of Natural Vocalizations.

Humans and animals maintain accurate sound discrimination in the presence of loud sources of background noise. It is commonly assumed that this ability relies on the robustness of auditory cortex responses. However, only a few attempts have been made to characterize neural discrimination of communication sounds masked by noise at each stage of the auditory system and to quantify the noise effects on the neuronal discrimination in terms of alterations in amplitude modulations. Here, we measured neural discrimination between communication sounds masked by a vocalization-shaped stationary noise from multiunit responses recorded in the cochlear nucleus, inferior colliculus, auditory thalamus, and primary and secondary auditory cortex at several signal-to-noise ratios (SNRs) in anesthetized male or female guinea pigs. Masking noise decreased sound discrimination of neuronal populations in each auditory structure, but collicular and thalamic populations showed better performance than cortical populations at each SNR. In contrast, in each auditory structure, discrimination by neuronal populations was slightly decreased when tone-vocoded vocalizations were tested. These results shed new light on the specific contributions of subcortical structures to robust sound encoding, and suggest that the distortion of slow amplitude modulation cues conveyed by communication sounds is one of the factors constraining the neuronal discrimination in subcortical and cortical levels.SIGNIFICANCE STATEMENT Dissecting how auditory neurons discriminate communication sounds in noise is a major goal in auditory neuroscience. Robust sound coding in noise is often viewed as a specific property of cortical networks, although this remains to be demonstrated. Here, we tested the discrimination performance of neuronal populations at five levels of the auditory system in response to conspecific vocalizations masked by noise. In each acoustic condition, subcortical neurons better discriminated target vocalizations than cortical ones and in each structure, the reduction in discrimination performance was related to the reduction in slow amplitude modulation cues.

Neural code: Another breach in the wall?

Brette presents arguments that query the existence of the neural code. However, he has neglected certain evidence that could be viewed as proof that a neural code operates in the brain. Albeit these proofs show a link between neural activity and cognition, we discuss why they fail to demonstrate the existence of an invariant neural code.

A Single Exposure to GSM-1800 MHz Signals in the Course of an Acute Neuroinflammatory Reaction can Alter Neuronal Responses and Microglial Morphology in the Rat Primary Auditory Cortex.

During mobile phone conversations, the temporal lobe neural networks involved in processing auditory information are exposed to electromagnetic fields (EMF) such as pulse-modulated GSM-1800 MHz radiofrequencies that convey wireless communications. The effects of these EMF on the brain affected by a pathological condition remain little investigated. In this study, rats injected with lipopolysaccharide (LPS) to induce neuroinflammation were exposed "head-only" to GSM-1800 MHz signals for two hours at a specific absorption rate (SAR) that reached an average value of 1.55 W/kg in the auditory cortex (ACx). Immunodetection of Iba1, a microglial marker, and electrophysiological recordings in the ACx three to six hours after global system for communication (GSM) exposure, or sham-exposure, showed that exposure to GSM-1800 MHz resulted in a growth of microglial processes and a reduction in spontaneous firing rate. More importantly, there was a significant reduction in evoked responses to artificial and natural stimuli and an increase in response duration. The response latency and the bandwidth of the frequency tuning were unchanged, but the GSM exposure led to a higher proportion of cortical sites exhibiting abnormally high acoustic thresholds. These modifications were not observed in rats exposed to GSM-1800 MHz without pretreatment with LPS. Together our data provide evidence that in neuroinflammatory conditions, acute exposure to GSM-1800 MHz can significantly affect microglia and neuronal activity underling auditory perception.

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.

This 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.

Dysfunctional Dopaminergic Neurones in Mouse Models of Huntington's Disease: A Role for SK3 Channels.

BACKGROUND: Huntington's disease (HD) is a late-onset fatal neurodegenerative disorder caused by a CAG trinucleotide repeat expansion in the gene coding for the protein huntingtin and is characterised by progressive motor, psychiatric and cognitive decline. We previously demonstrated that normal synaptic function in HD could be restored by application of dopamine receptor agonists, suggesting that changes in the release or bioavailability of dopamine may be a contributing factor to the disease process. OBJECTIVE: In the present study, we examined the properties of midbrain dopaminergic neurones and dopamine release in presymptomatic and symptomatic transgenic HD mice. METHODS AND RESULTS: Using intracellular sharp recordings and immunohistochemistry, we found that neuronal excitability was increased due to a loss of slow afterhyperpolarisation and that these changes were related to an apparent functional loss and abnormal distribution of SK3 channels (KCa2.3 encoded by the KCNN3 gene), a class of small-conductance calcium-activated potassium channels. Electrochemical detection of dopamine showed that this observation was associated with an enhanced dopamine release in presymptomatic transgenic mice and a drastic reduction in symptomatic animals. These changes occurred in the context of a progressive expansion in the CAG repeat number and nuclear localisation of mutant protein within the substantia nigra pars compacta. CONCLUSIONS: Dopaminergic neuronal dysfunction is a key early event in HD disease progression. The initial increase in dopamine release appears to be related to a loss of SK3 channel function, a protein containing a polyglutamine tract. Implications for polyglutamine-mediated sequestration of SK3 channels, dopamine-associated DNA damage and CAG expansion are discussed in the context of HD.

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

Over the last decade, the consequences of acoustic trauma on the functional properties of auditory cortex neurons have received growing attention. Changes in spontaneous and evoked activity, shifts of characteristic frequency (CF), and map reorganizations have extensively been described in anesthetized animals (e.g., Noreña and Eggermont, 2003, 2005). Here, we examined how the functional properties of cortical cells are modified after partial hearing loss in awake guinea pigs. Single unit activity was chronically recorded in awake, restrained, guinea pigs from 3 days before up to 15 days after an acoustic trauma induced by a 5 kHz 110 dB tone delivered for 1 h. Auditory brainstem responses (ABRs) audiograms indicated that these parameters produced a mean ABR threshold shift of 20 dB SPL at, and one octave above, the trauma frequency. When tested with pure tones, cortical cells showed on average a 25 dB increase in threshold at CF the day following the trauma. Over days, this increase progressively stabilized at only 10 dB above control value indicating a progressive recovery of cortical thresholds, probably reflecting a progressive shift from temporary threshold shift (TTS) to permanent threshold shift (PTS). There was an increase in response latency and in response variability the day following the trauma but these parameters returned to control values within 3 days. When tested with conspecific vocalizations, cortical neurons also displayed an increase in response latency and in response duration the day after the acoustic trauma, but there was no effect on the average firing rate elicited by the vocalization. These findings suggest that, in cases of moderate hearing loss, the temporal precision of neuronal responses to natural stimuli is impaired despite the fact the firing rate showed little or no changes.

Cortical inhibition reduces information redundancy at presentation of communication sounds in the primary auditory cortex.

In all sensory modalities, intracortical inhibition shapes the functional properties of cortical neurons but also influences the responses to natural stimuli. Studies performed in various species have revealed that auditory cortex neurons respond to conspecific vocalizations by temporal spike patterns displaying a high trial-to-trial reliability, which might result from precise timing between excitation and inhibition. Studying the guinea pig auditory cortex, we show that partial blockage of GABAA receptors by gabazine (GBZ) application (10 µm, a concentration that promotes expansion of cortical receptive fields) increased the evoked firing rate and the spike-timing reliability during presentation of communication sounds (conspecific and heterospecific vocalizations), whereas GABAB receptor antagonists [10 µm saclofen; 10-50 µm CGP55845 (p-3-aminopropyl-p-diethoxymethyl phosphoric acid)] had nonsignificant effects. Computing mutual information (MI) from the responses to vocalizations using either the evoked firing rate or the temporal spike patterns revealed that GBZ application increased the MI derived from the activity of single cortical site but did not change the MI derived from population activity. In addition, quantification of information redundancy showed that GBZ significantly increased redundancy at the population level. This result suggests that a potential role of intracortical inhibition is to reduce information redundancy during the processing of natural stimuli.

How do auditory cortex neurons represent communication sounds?

A major goal in auditory neuroscience is to characterize how communication sounds are represented at the cortical level. The present review aims at investigating the role of auditory cortex in the processing of speech, bird songs and other vocalizations, which all are spectrally and temporally highly structured sounds. Whereas earlier studies have simply looked for neurons exhibiting higher firing rates to particular conspecific vocalizations over their modified, artificially synthesized versions, more recent studies determined the coding capacity of temporal spike patterns, which are prominent in primary and non-primary areas (and also in non-auditory cortical areas). In several cases, this information seems to be correlated with the behavioral performance of human or animal subjects, suggesting that spike-timing based coding strategies might set the foundations of our perceptive abilities. Also, it is now clear that the responses of auditory cortex neurons are highly nonlinear and that their responses to natural stimuli cannot be predicted from their responses to artificial stimuli such as moving ripples and broadband noises. Since auditory cortex neurons cannot follow rapid fluctuations of the vocalizations envelope, they only respond at specific time points during communication sounds, which can serve as temporal markers for integrating the temporal and spectral processing taking place at subcortical relays. Thus, the temporal sparse code of auditory cortex neurons can be considered as a first step for generating high level representations of communication sounds independent of the acoustic characteristic of these sounds. This article is part of a Special Issue entitled "Communication Sounds and the Brain: New Directions and Perspectives".

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

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.

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

Over 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.

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

Understanding 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 (<10%) displayed a firing rate preference for the natural version of these vocalizations. In contrast, when the information transmitted by the spike trains was quantified with a temporal precision of 10-50 ms, many 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.