-
Cell Mar 2023Resilience enables mental elasticity in individuals when rebounding from adversity. In this study, we identified a microcircuit and relevant molecular adaptations that...
Resilience enables mental elasticity in individuals when rebounding from adversity. In this study, we identified a microcircuit and relevant molecular adaptations that play a role in natural resilience. We found that activation of parvalbumin (PV) interneurons in the primary auditory cortex (A1) by thalamic inputs from the ipsilateral medial geniculate body (MG) is essential for resilience in mice exposed to chronic social defeat stress. Early attacks during chronic social defeat stress induced short-term hyperpolarizations of MG neurons projecting to the A1 (MG neurons) in resilient mice. In addition, this temporal neural plasticity of MG neurons initiated synaptogenesis onto thalamic PV neurons via presynaptic BDNF-TrkB signaling in subsequent stress responses. Moreover, optogenetic mimicking of the short-term hyperpolarization of MG neurons, rather than merely activating MG neurons, elicited innate resilience mechanisms in response to stress and achieved sustained antidepressant-like effects in multiple animal models, representing a new strategy for targeted neuromodulation.
Topics: Mice; Animals; Auditory Cortex; Thalamus; Neurons; Geniculate Bodies; Interneurons; Parvalbumins
PubMed: 37001500
DOI: 10.1016/j.cell.2023.02.036 -
Neuron Aug 2023The brain can combine auditory and visual information to localize objects. However, the cortical substrates underlying audiovisual integration remain uncertain. Here, we...
The brain can combine auditory and visual information to localize objects. However, the cortical substrates underlying audiovisual integration remain uncertain. Here, we show that mouse frontal cortex combines auditory and visual evidence; that this combination is additive, mirroring behavior; and that it evolves with learning. We trained mice in an audiovisual localization task. Inactivating frontal cortex impaired responses to either sensory modality, while inactivating visual or parietal cortex affected only visual stimuli. Recordings from >14,000 neurons indicated that after task learning, activity in the anterior part of frontal area MOs (secondary motor cortex) additively encodes visual and auditory signals, consistent with the mice's behavioral strategy. An accumulator model applied to these sensory representations reproduced the observed choices and reaction times. These results suggest that frontal cortex adapts through learning to combine evidence across sensory cortices, providing a signal that is transformed into a binary decision by a downstream accumulator.
Topics: Animals; Mice; Visual Perception; Acoustic Stimulation; Auditory Perception; Photic Stimulation; Frontal Lobe; Auditory Cortex
PubMed: 37295419
DOI: 10.1016/j.neuron.2023.05.008 -
PLoS Biology Aug 2023Music is core to human experience, yet the precise neural dynamics underlying music perception remain unknown. We analyzed a unique intracranial electroencephalography...
Music is core to human experience, yet the precise neural dynamics underlying music perception remain unknown. We analyzed a unique intracranial electroencephalography (iEEG) dataset of 29 patients who listened to a Pink Floyd song and applied a stimulus reconstruction approach previously used in the speech domain. We successfully reconstructed a recognizable song from direct neural recordings and quantified the impact of different factors on decoding accuracy. Combining encoding and decoding analyses, we found a right-hemisphere dominance for music perception with a primary role of the superior temporal gyrus (STG), evidenced a new STG subregion tuned to musical rhythm, and defined an anterior-posterior STG organization exhibiting sustained and onset responses to musical elements. Our findings show the feasibility of applying predictive modeling on short datasets acquired in single patients, paving the way for adding musical elements to brain-computer interface (BCI) applications.
Topics: Humans; Auditory Cortex; Music; Brain Mapping; Auditory Perception; Temporal Lobe; Acoustic Stimulation
PubMed: 37582062
DOI: 10.1371/journal.pbio.3002176 -
Trends in Neurosciences May 2023Crossmodal plasticity is a textbook example of the ability of the brain to reorganize based on use. We review evidence from the auditory system showing that such... (Review)
Review
Crossmodal plasticity is a textbook example of the ability of the brain to reorganize based on use. We review evidence from the auditory system showing that such reorganization has significant limits, is dependent on pre-existing circuitry and top-down interactions, and that extensive reorganization is often absent. We argue that the evidence does not support the hypothesis that crossmodal reorganization is responsible for closing critical periods in deafness, and crossmodal plasticity instead represents a neuronal process that is dynamically adaptable. We evaluate the evidence for crossmodal changes in both developmental and adult-onset deafness, which start as early as mild-moderate hearing loss and show reversibility when hearing is restored. Finally, crossmodal plasticity does not appear to affect the neuronal preconditions for successful hearing restoration. Given its dynamic and versatile nature, we describe how this plasticity can be exploited for improving clinical outcomes after neurosensory restoration.
Topics: Adult; Humans; Auditory Cortex; Acoustic Stimulation; Photic Stimulation; Hearing Loss; Deafness; Neuronal Plasticity
PubMed: 36990952
DOI: 10.1016/j.tins.2023.02.004 -
Journal of the Association For Research... Jun 2021The ability to process and perceive sensory stimuli is an essential function for animals. Among the sensory modalities, audition is crucial for communication, pleasure,... (Review)
Review
The ability to process and perceive sensory stimuli is an essential function for animals. Among the sensory modalities, audition is crucial for communication, pleasure, care for the young, and perceiving threats. The auditory cortex (ACtx) is a key sound processing region that combines ascending signals from the auditory periphery and inputs from other sensory and non-sensory regions. The development of ACtx is a protracted process starting prenatally and requires the complex interplay of molecular programs, spontaneous activity, and sensory experience. Here, we review the development of thalamic and cortical auditory circuits during pre- and early post-natal periods.
Topics: Animals; Auditory Cortex; Auditory Perception; Sound; Thalamus
PubMed: 33909161
DOI: 10.1007/s10162-021-00794-3 -
Neuroscience and Biobehavioral Reviews Jan 2022The auditory system provides us with extremely rich and precise information about the outside world. Once a sound reaches our ears, the acoustic information it carries... (Review)
Review
The auditory system provides us with extremely rich and precise information about the outside world. Once a sound reaches our ears, the acoustic information it carries travels from the cochlea all the way to the auditory cortex, where its complexity and nuances are integrated. In the auditory cortex, functional circuits are formed by subpopulations of intermingled excitatory and inhibitory cells. In this review, we discuss recent evidence of the specific contributions of inhibitory neurons in sound processing and integration. We first examine intrinsic properties of three main classes of inhibitory interneurons in the auditory cortex. Then, we describe how inhibition shapes the responsiveness of the auditory cortex to sound. Finally, we discuss how inhibitory interneurons contribute to the sensation and perception of sounds. Altogether, this review points out the crucial role of cortical inhibitory interneurons in integrating information about the context, history, or meaning of a sound. It also highlights open questions to be addressed for increasing our understanding of the staggering complexity leading to the subtlest auditory perception.
Topics: Acoustic Stimulation; Auditory Cortex; Auditory Perception; Interneurons
PubMed: 34822879
DOI: 10.1016/j.neubiorev.2021.11.021 -
Physiological Reviews Apr 2023Adaptation is an essential feature of auditory neurons, which reduces their responses to unchanging and recurring sounds and allows their response properties to be... (Review)
Review
Adaptation is an essential feature of auditory neurons, which reduces their responses to unchanging and recurring sounds and allows their response properties to be matched to the constantly changing statistics of sounds that reach the ears. As a consequence, processing in the auditory system highlights novel or unpredictable sounds and produces an efficient representation of the vast range of sounds that animals can perceive by continually adjusting the sensitivity and, to a lesser extent, the tuning properties of neurons to the most commonly encountered stimulus values. Together with attentional modulation, adaptation to sound statistics also helps to generate neural representations of sound that are tolerant to background noise and therefore plays a vital role in auditory scene analysis. In this review, we consider the diverse forms of adaptation that are found in the auditory system in terms of the processing levels at which they arise, the underlying neural mechanisms, and their impact on neural coding and perception. We also ask what the dynamics of adaptation, which can occur over multiple timescales, reveal about the statistical properties of the environment. Finally, we examine how adaptation to sound statistics is influenced by learning and experience and changes as a result of aging and hearing loss.
Topics: Animals; Acoustic Stimulation; Auditory Cortex; Auditory Perception; Noise; Adaptation, Physiological
PubMed: 36049112
DOI: 10.1152/physrev.00011.2022 -
Nature Reviews. Neuroscience Oct 2019Humans and other animals use spatial hearing to rapidly localize events in the environment. However, neural encoding of sound location is a complex process involving... (Review)
Review
Humans and other animals use spatial hearing to rapidly localize events in the environment. However, neural encoding of sound location is a complex process involving the computation and integration of multiple spatial cues that are not represented directly in the sensory organ (the cochlea). Our understanding of these mechanisms has increased enormously in the past few years. Current research is focused on the contribution of animal models for understanding human spatial audition, the effects of behavioural demands on neural sound location encoding, the emergence of a cue-independent location representation in the auditory cortex, and the relationship between single-source and concurrent location encoding in complex auditory scenes. Furthermore, computational modelling seeks to unravel how neural representations of sound source locations are derived from the complex binaural waveforms of real-life sounds. In this article, we review and integrate the latest insights from neurophysiological, neuroimaging and computational modelling studies of mammalian spatial hearing. We propose that the cortical representation of sound location emerges from recurrent processing taking place in a dynamic, adaptive network of early (primary) and higher-order (posterior-dorsal and dorsolateral prefrontal) auditory regions. This cortical network accommodates changing behavioural requirements and is especially relevant for processing the location of real-life, complex sounds and complex auditory scenes.
Topics: Acoustic Stimulation; Animals; Auditory Cortex; Auditory Pathways; Hearing; Humans; Sound Localization
PubMed: 31467450
DOI: 10.1038/s41583-019-0206-5 -
Hearing Research Jun 2023The auditory system transforms auditory stimuli from the external environment into perceptual auditory objects. Recent studies have focused on the contribution of the... (Review)
Review
The auditory system transforms auditory stimuli from the external environment into perceptual auditory objects. Recent studies have focused on the contribution of the auditory cortex to this transformation. Other studies have yielded important insights into the contributions of neural activity in the auditory cortex to cognition and decision-making. However, despite this important work, the relationship between auditory-cortex activity and behavior/perception has not been fully elucidated. Two of the more important gaps in our understanding are (1) the specific and differential contributions of different fields of the auditory cortex to auditory perception and behavior and (2) the way networks of auditory neurons impact and facilitate auditory information processing. Here, we focus on recent work from non-human-primate models of hearing and review work related to these gaps and put forth challenges to further our understanding of how single-unit activity and network activity in different cortical fields contribution to behavior and perception.
Topics: Animals; Auditory Cortex; Auditory Perception; Primates; Hearing Tests; Neurons; Acoustic Stimulation
PubMed: 37075536
DOI: 10.1016/j.heares.2023.108768 -
Nature Jan 2023Cochlear implants (CIs) are neuroprosthetic devices that can provide hearing to deaf people. Despite the benefits offered by CIs, the time taken for hearing to be...
Cochlear implants (CIs) are neuroprosthetic devices that can provide hearing to deaf people. Despite the benefits offered by CIs, the time taken for hearing to be restored and perceptual accuracy after long-term CI use remain highly variable. CI use is believed to require neuroplasticity in the central auditory system, and differential engagement of neuroplastic mechanisms might contribute to the variability in outcomes. Despite extensive studies on how CIs activate the auditory system, the understanding of CI-related neuroplasticity remains limited. One potent factor enabling plasticity is the neuromodulator noradrenaline from the brainstem locus coeruleus (LC). Here we examine behavioural responses and neural activity in LC and auditory cortex of deafened rats fitted with multi-channel CIs. The rats were trained on a reward-based auditory task, and showed considerable individual differences of learning rates and maximum performance. LC photometry predicted when CI subjects began responding to sounds and longer-term perceptual accuracy. Optogenetic LC stimulation produced faster learning and higher long-term accuracy. Auditory cortical responses to CI stimulation reflected behavioural performance, with enhanced responses to rewarded stimuli and decreased distinction between unrewarded stimuli. Adequate engagement of central neuromodulatory systems is thus a potential clinically relevant target for optimizing neuroprosthetic device use.
Topics: Animals; Rats; Cochlear Implantation; Cochlear Implants; Deafness; Hearing; Learning; Locus Coeruleus; Neuronal Plasticity; Norepinephrine; Auditory Cortex; Neurons; Reward; Optogenetics; Photometry
PubMed: 36544024
DOI: 10.1038/s41586-022-05554-8