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      Sound-Driven Synaptic Inhibition in Primary Visual Cortex

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          Summary

          Multimodal objects and events activate many sensory cortical areas simultaneously. This is possibly reflected in reciprocal modulations of neuronal activity, even at the level of primary cortical areas. However, the synaptic character of these interareal interactions, and their impact on synaptic and behavioral sensory responses are unclear. Here, we found that activation of auditory cortex by a noise burst drove local GABAergic inhibition on supragranular pyramids of the mouse primary visual cortex, via cortico-cortical connections. This inhibition was generated by sound-driven excitation of a limited number of cells in infragranular visual cortical neurons. Consequently, visually driven synaptic and spike responses were reduced upon bimodal stimulation. Also, acoustic stimulation suppressed conditioned behavioral responses to a dim flash, an effect that was prevented by acute blockade of GABAergic transmission in visual cortex. Thus, auditory cortex activation by salient stimuli degrades potentially distracting sensory processing in visual cortex by recruiting local, translaminar, inhibitory circuits.

          Highlights

          ► Activation of a sensory cortex causes hyperpolarizing responses in neighboring ones ► Sound activates GABAergic synapses onto layer 2/3 pyramids of the visual cortex ► Sound-driven inhibition is due to activation of few cells in layer 5 of visual cortex ► Sound-driven inhibition reduces neuronal and behavioral responses to visual stimuli

          Abstract

          Iurilli et al. examined the interplay between sensory modalities and discovered that auditory cortex activation can inhibit visual cortical neurons via cortico-cortical inputs that activate inhibitory subcircuits originating in the deep layers of the visual cortex.

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          Most cited references56

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          The normalization model of attention.

          Attention has been found to have a wide variety of effects on the responses of neurons in visual cortex. We describe a model of attention that exhibits each of these different forms of attentional modulation, depending on the stimulus conditions and the spread (or selectivity) of the attention field in the model. The model helps reconcile proposals that have been taken to represent alternative theories of attention. We argue that the variety and complexity of the results reported in the literature emerge from the variety of empirical protocols that were used, such that the results observed in any one experiment depended on the stimulus conditions and the subject's attentional strategy, a notion that we define precisely in terms of the attention field in the model, but that has not typically been completely under experimental control.
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            Turning on and off recurrent balanced cortical activity.

            The vast majority of synaptic connections onto neurons in the cerebral cortex arise from other cortical neurons, both excitatory and inhibitory, forming local and distant 'recurrent' networks. Although this is a basic theme of cortical organization, its study has been limited largely to theoretical investigations, which predict that local recurrent networks show a proportionality or balance between recurrent excitation and inhibition, allowing the generation of stable periods of activity. This recurrent activity might underlie such diverse operations as short-term memory, the modulation of neuronal excitability with attention, and the generation of spontaneous activity during sleep. Here we show that local cortical circuits do indeed operate through a proportional balance of excitation and inhibition generated through local recurrent connections, and that the operation of such circuits can generate self-sustaining activity that can be turned on and off by synaptic inputs. These results confirm the long-hypothesized role of recurrent activity as a basic operation of the cerebral cortex.
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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
                Journal
                Neuron
                Neuron
                Neuron
                Cell Press
                0896-6273
                1097-4199
                23 February 2012
                23 February 2012
                : 73
                : 4-2
                : 814-828
                Affiliations
                [1 ]Department of Neuroscience and Brain Technologies, Istituto Italiano di Tecnologia, Via Morego 30, 16163 Genova, Italy
                Author notes
                []Corresponding author paolo.medini@ 123456iit.it
                [2]

                These authors contributed equally to this work

                Article
                NEURON10983
                10.1016/j.neuron.2011.12.026
                3315003
                22365553
                732b7e9c-4c58-485f-8c6a-4eb5aea29f3c
                © 2012 ELL & Excerpta Medica.

                This document may be redistributed and reused, subject to certain conditions.

                History
                : 9 December 2011
                Categories
                Article

                Neurosciences
                Neurosciences

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