Cerebral areas mediating visual redirection of gaze: Cooling deactivation of 15 loci in the cat

Lomber, Stephen G.; Payne, Bertram R.

doi:10.1002/cne.20123

Cited by 25 publications

(18 citation statements)

References 110 publications

(129 reference statements)

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“…Also, the findings from surgically rerouted visual connections to ferret auditory cortex (37) revealed crossmodal neuronal properties that resembled those of visual cortical neurons. Similarly, deafness induces the somatosensory reorganization of auditory cortices of adult ferrets where the neurons exhibited large receptive fields most often associated with higher-level cortices (30,31). The present data are consistent with these sensory features of crossmodally innervated neurons.…”

Section: Discussionsupporting

confidence: 88%

“…32). In the present experiment, deactivation of reorganized FAES blocked visual localization as effectively as cooling visual PMLS in hearing (31) as well as early-deafened animals (present results). These observations, at first, might appear puzzling, where an adaptive modification (crossmodal plasticity) is given the same priority as normal visuomotor circuitry that has evolved through millions of years of evolutionary pressure.…”

Section: Discussionsupporting

confidence: 74%

See 1 more Smart Citation

Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex

Meredith

Kryklywy²,

McMillan³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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126

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It is well known that early disruption of sensory input from one modality can induce crossmodal reorganization of a deprived cortical area, resulting in compensatory abilities in the remaining senses. Compensatory effects, however, occur in selected cortical regions and it is not known whether such compensatory phenomena have any relation to the original function of the reorganized area. In the cortex of hearing cats, the auditory field of the anterior ectosylvian sulcus (FAES) is largely responsive to acoustic stimulation and its unilateral deactivation results in profound contralateral acoustic orienting deficits. Given these functional and behavioral roles, the FAES was studied in early-deafened cats to examine its crossmodal sensory properties as well as to assess the behavioral role of that reorganization. Recordings in the FAES of early-deafened adults revealed robust responses to visual stimulation as well as receptive fields that collectively represented the contralateral visual field. A second group of early-deafened cats was trained to localize visual targets in a perimetry array. In these animals, cooling loops were surgically placed on the FAES to reversibly deactivate the region, which resulted in substantial contralateral visual orienting deficits. These results demonstrate that crossmodal plasticity can substitute one sensory modality for another while maintaining the functional repertoire of the reorganized region.vision | single-unit electrophysiology | orienting behavior | cooling deactivation A remarkable property of the brain is its capacity to respond to change. This neuroplastic process endows the nervous system with the ability to adjust itself to the loss of an entire set of sensory inputs or even two (1). Under these conditions, it is clearly adaptive for inputs from an intact modality to substitute for those that have been lost, such as auditory navigation in the blind. Crossmodal plasticity can also enhance perceptual performance within the remaining sensory modalities. Numerous reports document improvement over sighted subjects in auditory and somatosensory tasks in blind individuals (2-7), as well as enhanced performance in visual and tactile behaviors in the deaf (8-11). However, with the accumulation of studies examining such compensatory effects following early sensory loss, it is becoming evident that not all features of the replacement sensory modalities are equally represented. For example, early-deaf subjects exhibit supranormal abilities for visual localization (10) and visual motion detection (11, 12), but not visual brightness discrimination (13), contrast sensitivity (14), visual shape detection (15), grating acuity, vernier acuity, orientation discrimination, motion direction, or velocity discrimination (11). Thus, rather than a generalized overall improvement, it seems that only specific features of the replacement modality are affected by crossmodal plasticity.Crossmodal plasticity itself does not appear to be a uniformly distributed effect. Although it seems plausible ...

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Section: Discussionsupporting

confidence: 88%

Section: Discussionsupporting

confidence: 74%

Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex

Meredith

Kryklywy²,

McMillan³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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126

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“…Because it was not possible to conduct cytoarchitectonic assays on the archived tissue, the sulcal and gyral patterns defined by the stereotaxic atlas of the cat brain (Reinoso-Suárez, 1961), updated by more recent studies (Avendaño et al, 1988; Bowman and Olson, 1988; Clascá et al, 1997; Clemo and Meredith, 2004; Clemo et al, 2007; Lee and Winer, 2008; Lomber and Malhotra, 2008; Lomber and Payne, 2004; Mellott et al, 2010; Meredith, 2004; Meredith and Clemo, 1989; Mucke et al, 1982; Payne, 1993; Reinoso-Suárez,1961; Ribaupierre,1997; Rosenquist, 1985; Updyke, 1986; van der Gucht et al, 2001) were used to determine the borders of the cortical functional areas. The relative proportion of cortical projections from each area to the FAES was normalized as a percentage of the total projection from the cases in which the entire rostral-caudal series of cortical sections was available (BDA66, 71, 29 hearing; BDA65, 68, W87 early deaf).…”

Section: Methodsmentioning

confidence: 99%

Cortical and thalamic connectivity of the auditory anterior ectosylvian cortex of early-deaf cats: Implications for neural mechanisms of crossmodal plasticity

et al. 2016

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Early hearing loss leads to crossmodal plasticity in regions of the cerebrum that are dominated by acoustical processing in hearing subjects. Until recently, little has been known of the connectional basis of this phenomenon. One region whose crossmodal properties are well-established is the auditory field of the anterior ectosylvian sulcus (FAES) in the cat, where neurons are normally responsive to acoustic stimulation and its deactivation leads to the behavioral loss of accurate orienting toward auditory stimuli. However, in early-deaf cats, visual responsiveness predominates in the FAES and its deactivation blocks accurate orienting behavior toward visual stimuli. For such crossmodal reorganization to occur, it has been presumed that novel inputs or increased projections from non-auditory cortical areas must be generated, or that existing non-auditory connections were ‘unmasked.’ These possibilities were tested using tracer injections into the FAES of adult cats deafened early in life (and hearing controls), followed by light microscopy to localize retrogradely labeled neurons. Surprisingly, the distribution of cortical and thalamic afferents to the FAES was very similar among early-deaf and hearing animals. No new visual projection sources were identified and visual cortical connections to the FAES were comparable in projection proportions. These results support an alternate theory for the connectional basis for cross-modal plasticity that involves enhanced local branching of existing projection terminals that originate in non-auditory as well as auditory cortices.

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“…Such an integrated output demonstrates that these neurons are actively transforming this input information, likely in a way that facilitates the behavioral and/or perceptual role of the AES. Although this functional role has remained enigmatic, the selectivities of the neuronal populations within AES and its anatomical input/output organization point toward its playing a role in eye movements (Kimura and Tamai 1992;Tamai et al 1989), spatial localization (Lomber and Payne 2004;Malhotra et al 2004Malhotra et al , 2007, motion perception (Nagy et al 2003b;Scannell et al 1996), and coordinate transformations between the different sensory systems (Wallace et al 1992(Wallace et al , 2006.…”

Section: On the Functional Role Of The Aesmentioning

confidence: 99%

Spatial Heterogeneity of Cortical Receptive Fields and Its Impact on Multisensory Interactions

Carriere

Royal²,

Wallace³

2008

Journal of Neurophysiology

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Carriere BN, Royal DW, Wallace MT. Spatial heterogeneity of cortical receptive fields and its impact on multisensory interactions. J Neurophysiol 99: 2357-2368, 2008. First published February 20, 2008 doi:10.1152/jn.01386.2007. Investigations of multisensory processing at the level of the single neuron have illustrated the importance of the spatial and temporal relationship of the paired stimuli and their relative effectiveness in determining the product of the resultant interaction. Although these principles provide a good first-order description of the interactive process, they were derived by treating space, time, and effectiveness as independent factors. In the anterior ectosylvian sulcus (AES) of the cat, previous work hinted that the spatial receptive field (SRF) architecture of multisensory neurons might play an important role in multisensory processing due to differences in the vigor of responses to identical stimuli placed at different locations within the SRF. In this study the impact of SRF architecture on cortical multisensory processing was investigated using semichronic single-unit electrophysiological experiments targeting a multisensory domain of the cat AES. The visual and auditory SRFs of AES multisensory neurons exhibited striking response heterogeneity, with SRF architecture appearing to play a major role in the multisensory interactions. The deterministic role of SRF architecture was tightly coupled to the manner in which stimulus location modulated the responsiveness of the neuron. Thus multisensory stimulus combinations at weakly effective locations within the SRF resulted in large (often superadditive) response enhancements, whereas combinations at more effective spatial locations resulted in smaller (additive/subadditive) interactions. These results provide important insights into the spatial organization and processing capabilities of cortical multisensory neurons, features that may provide important clues as to the functional roles played by this area in spatially directed perceptual processes.

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Cerebral areas mediating visual redirection of gaze: Cooling deactivation of 15 loci in the cat

Cited by 25 publications

References 110 publications

Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex

Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex

Cortical and thalamic connectivity of the auditory anterior ectosylvian cortex of early-deaf cats: Implications for neural mechanisms of crossmodal plasticity

Spatial Heterogeneity of Cortical Receptive Fields and Its Impact on Multisensory Interactions

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