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      Using the Principles of Multisensory Integration to Reverse Hemianopia

      , 1 , 1 , 1
      Cerebral Cortex
      Oxford University Press (OUP)

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          Abstract

          Hemianopia can be rehabilitated by an auditory-visual “training” procedure, which restores visual responsiveness in midbrain neurons indirectly compromised by the cortical lesion and reinstates vision in contralesional space. Presumably, these rehabilitative changes are induced via mechanisms of multisensory integration/plasticity. If so, the paradigm should fail if the stimulus configurations violate the spatiotemporal principles that govern these midbrain processes. To test this possibility, hemianopic cats were provided spatially or temporally noncongruent auditory-visual training. Rehabilitation failed in all cases even after approximately twice the number of training trials normally required for recovery, and even after animals learned to approach the location of the undetected visual stimulus. When training was repeated with these stimuli in spatiotemporal concordance, hemianopia was resolved. The results identify the conditions needed to engage changes in remaining neural circuits required to support vision in the absence of visual cortex, and have implications for rehabilitative strategies in human patients.

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          Most cited references42

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          Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors.

          One of the most impressive features of the central nervous system is its ability to process information from a variety of stimuli to produce an integrated, comprehensive representation of the external world. In the present study, the temporal disparity among combinations of different sensory stimuli was shown to be a critical factor influencing the integration of multisensory stimuli by superior colliculus neurons. Several temporal principles that govern multisensory integration were revealed: (1) maximal levels of response enhancement were generated by overlapping the peak discharge periods evoked by each modality; (2) the magnitude of this enhancement decayed monotonically to zero as the peak discharge periods became progressively more temporally disparate; (3) with further increases in temporal disparity, the same stimulus combinations that previously produced enhancement could often produce depression; and (4) these kinds of interactions could frequently be predicted from the discharge trains initiated by each stimulus alone. Since multisensory superior colliculus neurons project to premotor areas of the brain stem and spinal cord that control the orientation of the receptor organs (eyes, pinnae, head), they are believed to influence attentive and orientation behaviors. Therefore, it is likely that the temporal relationships of different environmental stimuli that control the activity of these neurons are also a powerful determinant of superior colliculus-mediated attentive and orientation behaviors.
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            Subcortical loops through the basal ganglia.

            Parallel, largely segregated, closed-loop projections are an important component of cortical-basal ganglia-cortical connectional architecture. Here, we present the hypothesis that such loops involving the neocortex are neither novel nor the first evolutionary example of closed-loop architecture involving the basal ganglia. Specifically, we propose that a phylogenetically older, closed-loop series of subcortical connections exists between the basal ganglia and brainstem sensorimotor structures, a good example of which is the midbrain superior colliculus. Insofar as this organization represents a general feature of brain architecture, cortical and subcortical inputs to the basal ganglia might act independently, co-operatively or competitively to influence the mechanisms of action selection.
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              Spatial factors determine the activity of multisensory neurons in cat superior colliculus.

              The responses of a neuron to stimuli from one sensory modality can be profoundly influenced by inputs from other sensory modalities. The present experiments demonstrate that the nature and the magnitude of these multisensory interactions depend on the positions of the stimuli in relation to their respective receptive fields. The spatial rules governing these interactions underscore the significance of the alignment of sensory maps in the brain.
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                Author and article information

                Contributors
                (View ORCID Profile)
                Journal
                Cerebral Cortex
                Oxford University Press (OUP)
                1047-3211
                1460-2199
                April 2020
                April 14 2020
                December 04 2019
                April 2020
                April 14 2020
                December 04 2019
                : 30
                : 4
                : 2030-2041
                Affiliations
                [1 ]Department of Neurobiology & Anatomy, Wake Forest University School of Medicine, Winston-Salem, NC 27157-1010, USA
                Article
                10.1093/cercor/bhz220
                7175010
                31799618
                5372ad40-50a5-4159-af67-27c1e409968c
                © 2019

                https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model

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