Abstract

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.

Highlights

  • The auditory cortex has been viewed as the ultimate step in processing the rich acoustic stream constantly reaching our ears and as a key structure in cognitive tasks involving auditory stimuli (Weinberger and Diamond, 1987; Edeline, 1999; Weinberger, 2004; Ohl and Scheich, 2005; Fritz et al, 2007)

  • This study suggested a progressive emergence of noise-invariant responses from the auditory nerve to the inferior colliculus (IC) and to A1, and proposed the adaptation to the noise statistics as a key mechanism to account for the noise-invariant representation in A1

  • From recordings obtained in anesthetized guinea pigs in the cochlear nucleus, inferior colliculus, auditory thalamus, A1 and a non-primary auditory cortex, Souffi et al (2020) reported that higher discrimination performance and more accurate representations in degraded acoustic conditions were found in IC and medial geniculate body (MGB); cortical representations, less accurate as the subcortical ones, were barely affected under these degraded conditions (Figure 1, modified from Souffi et al, 2020)

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Summary

INTRODUCTION

The auditory cortex has been viewed as the ultimate step in processing the rich acoustic stream constantly reaching our ears and as a key structure in cognitive tasks involving auditory stimuli (Weinberger and Diamond, 1987; Edeline, 1999; Weinberger, 2004; Ohl and Scheich, 2005; Fritz et al, 2007). In the avian auditory system, Schneider and Woolley (2013) described the emergence of noiseinvariant responses for a subset of cells (the broad spike cells) of a secondary auditory area (area NCM), whereas neurons in the field L and the mesencephalicus lateralis dorsalis (homologous of the primary auditory cortex and inferior colliculus, respectively) show background-corrupted responses They proposed that a sparse coding scheme (in the sense that neurons show less driven response to the same stimulus and respond only to a small subset of the stimuli) operating within the area NCM allows the emergence of this noise-invariant representation. From recordings obtained in anesthetized guinea pigs in the cochlear nucleus, inferior colliculus, auditory thalamus, A1 and a non-primary auditory cortex, Souffi et al (2020) reported that higher discrimination performance and more accurate representations in degraded acoustic conditions (presence of masking noise or vocoding) were found in IC and MGB; cortical representations, less accurate as the subcortical ones, were barely affected under these degraded conditions (Figure 1, modified from Souffi et al, 2020). All the results together suggest that noise-invariant representations emerge very early in the auditory system under conditions of anesthetized or awake passive listening, without necessarily the involvement of cortical activity (Lohse et al, 2020)

EFFECTS OF THE CORTICOFUGAL DESCENDING PROJECTIONS
Auditory Cortical Manipulations in Anesthetized Animals
Modulation of Cortical Projections by Optogenetic Techniques
DECIPHERING THE MECHANISMS UNDERLYING THE CORTICOFUGAL EFFECTS
Neuromodulation in the Auditory Cortex
POSSIBLE SCENARIOS
Findings
AUTHOR CONTRIBUTIONS
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