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.

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.

Exposure to 1800 MHz LTE electromagnetic fields under proinflammatory conditions decreases the response strength and increases the acoustic threshold of auditory cortical neurons.

Increased needs for mobile phone communications have raised successive generations (G) of wireless technologies, which could differentially affect biological systems. To test this, we exposed rats to single head-only exposure of a 4G long-term evolution (LTE)-1800 MHz electromagnetic field (EMF) for 2 h. We then assessed the impact on microglial space coverage and electrophysiological neuronal activity in the primary auditory cortex (ACx), under acute neuroinflammation induced by lipopolysaccharide. The mean specific absorption rate in the ACx was 0.5 W/kg. Multiunit recording revealed that LTE-EMF triggered reduction in the response strength to pure tones and to natural vocalizations, together with an increase in acoustic threshold in the low and medium frequencies. Iba1 immunohistochemistry showed no change in the area covered by microglia cell bodies and processes. In healthy rats, the same LTE-exposure induced no change in response strength and acoustic threshold. Our data indicate that acute neuroinflammation sensitizes neuronal responses to LTE-EMF, which leads to an altered processing of acoustic stimuli in the ACx.

When and How Does the Auditory Cortex Influence Subcortical Auditory Structures? New Insights About the Roles of Descending Cortical Projections.

For decades, the corticofugal descending projections have been anatomically well described but their functional role remains a puzzling question. In this review, we will first describe the contributions of neuronal networks in representing communication sounds in various types of degraded acoustic conditions from the cochlear nucleus to the primary and secondary auditory cortex. In such situations, the discrimination abilities of collicular and thalamic neurons are clearly better than those of cortical neurons although the latter remain very little affected by degraded acoustic conditions. Second, we will report the functional effects resulting from activating or inactivating corticofugal projections on functional properties of subcortical neurons. In general, modest effects have been observed in anesthetized and in awake, passively listening, animals. In contrast, in behavioral tasks including challenging conditions, behavioral performance was severely reduced by removing or transiently silencing the corticofugal descending projections. This suggests that the discriminative abilities of subcortical neurons may be sufficient in many acoustic situations. It is only in particularly challenging situations, either due to the task difficulties and/or to the degraded acoustic conditions that the corticofugal descending connections bring additional abilities. Here, we propose that it is both the top-down influences from the prefrontal cortex, and those from the neuromodulatory systems, which allow the cortical descending projections to impact behavioral performance in reshaping the functional circuitry of subcortical structures. We aim at proposing potential scenarios to explain how, and under which circumstances, these projections impact on subcortical processing and on behavioral responses.

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.

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.