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      An imbalance of excitation and inhibition in the multisensory cortex impairs the temporal acuity of audiovisual processing and perception

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      Cerebral Cortex
      Oxford University Press (OUP)

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          Abstract

          The neural integration of closely timed auditory and visual stimuli can offer several behavioral advantages; however, an overly broad window of temporal integration—a phenomenon observed in various neurodevelopmental disorders—could have far-reaching perceptual consequences. Non-invasive studies in humans have suggested that the level of GABAergic inhibition in the multisensory cortex influences the temporal window over which auditory and visual stimuli are bound into a unified percept. Although this suggestion aligns with the theory that an imbalance of cortical excitation and inhibition alters multisensory processing, no prior studies have performed experimental manipulations to determine the causal effects of a reduction of GABAergic inhibition on audiovisual temporal perception. To that end, we used a combination of in vivo electrophysiology, neuropharmacology, and translational behavioral testing in rats to provide the first mechanistic evidence that a reduction of GABAergic inhibition in the audiovisual cortex is sufficient to disrupt unisensory and multisensory processing across the cortical layers, and ultimately impair the temporal acuity of audiovisual perception and its rapid adaptation to recent sensory experience. Looking forward, our findings provide support for using rat models to further investigate the neural mechanisms underlying the audiovisual perceptual alterations observed in neurodevelopmental disorders, such as autism, schizophrenia, and dyslexia.

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          Most cited references78

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          Model of autism: increased ratio of excitation/inhibition in key neural systems

          Autism is a severe neurobehavioral syndrome, arising largely as an inherited disorder, which can arise from several diseases. Despite recent advances in identifying some genes that can cause autism, its underlying neurological mechanisms are uncertain. Autism is best conceptualized by considering the neural systems that may be defective in autistic individuals. Recent advances in understanding neural systems that process sensory information, various types of memories and social and emotional behaviors are reviewed and compared with known abnormalities in autism. Then, specific genetic abnormalities that are linked with autism are examined. Synthesis of this information leads to a model that postulates that some forms of autism are caused by an increased ratio of excitation/inhibition in sensory, mnemonic, social and emotional systems. The model further postulates that the increased ratio of excitation/inhibition can be caused by combinatorial effects of genetic and environmental variables that impinge upon a given neural system. Furthermore, the model suggests potential therapeutic interventions.
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            Excitatory/Inhibitory Balance and Circuit Homeostasis in Autism Spectrum Disorders.

            Autism spectrum disorders (ASDs) and related neurological disorders are associated with mutations in many genes affecting the ratio between neuronal excitation and inhibition. However, understanding the impact of these mutations on network activity is complicated by the plasticity of these networks, making it difficult in many cases to separate initial deficits from homeostatic compensation. Here we explore the contrasting evidence for primary defects in inhibition or excitation in ASDs and attempt to integrate the findings in terms of the brain's ability to maintain functional homeostasis.
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              Neuronal oscillations and multisensory interaction in primary auditory cortex.

              Recent anatomical, physiological, and neuroimaging findings indicate multisensory convergence at early, putatively unisensory stages of cortical processing. The objective of this study was to confirm somatosensory-auditory interaction in A1 and to define both its physiological mechanisms and its consequences for auditory information processing. Laminar current source density and multiunit activity sampled during multielectrode penetrations of primary auditory area A1 in awake macaques revealed clear somatosensory-auditory interactions, with a novel mechanism: somatosensory inputs appear to reset the phase of ongoing neuronal oscillations, so that accompanying auditory inputs arrive during an ideal, high-excitability phase, and produce amplified neuronal responses. In contrast, responses to auditory inputs arriving during the opposing low-excitability phase tend to be suppressed. Our findings underscore the instrumental role of neuronal oscillations in cortical operations. The timing and laminar profile of the multisensory interactions in A1 indicate that nonspecific thalamic systems may play a key role in the effect.
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                Author and article information

                Contributors
                (View ORCID Profile)
                (View ORCID Profile)
                Journal
                Cerebral Cortex
                Oxford University Press (OUP)
                1047-3211
                1460-2199
                September 15 2023
                September 09 2023
                July 18 2023
                September 15 2023
                September 09 2023
                July 18 2023
                : 33
                : 18
                : 9937-9953
                Article
                10.1093/cercor/bhad256
                37464944
                efb26ce5-fedd-469c-aa49-26172d08078c
                © 2023

                https://academic.oup.com/pages/standard-publication-reuse-rights

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