Dynamic Properties of the Representation of the Visual Field Midline in the Visual Areas 17 and 18 of the Ferret (Mustela putorius)

Cerebral Cortex, Aug 2008

In mammals, the visual field is split along the midline, each hemisphere representing the contralateral hemifield. We determined that, in the ferret, an 8- to 10-deg-wide strip of visual field near the midline is represented in both hemispheres. Bright squares (1.5 deg) were flashed at different azimuths within the central 20 deg of the visual field. Stimuli were flashed either alone or sequentially, and the responses were analyzed with the voltage-sensitive dye (VSD) RH 795 and/or by recording local field potentials (LFPs). In both VSD and LFP experiments, each stimulus evoked a cortical response field that extended over visual areas 17 and 18 up to a surface of 1–1.5 mm2 and then shrank again. Amplitude of the responses decreased approaching the visual midline and the latency increased. These positional differences are likely to originate from the spatiotemporal structure of the peripheral response fields (PRFs) that form a mosaic in areas 17 and 18, interrupted near the visual midline. Unexpectedly, interhemispheric connections appear not to modify these PRFs’ effects and may not contribute to the responses to discrete, flashed stimuli.

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Dynamic Properties of the Representation of the Visual Field Midline in the Visual Areas 17 and 18 of the Ferret (Mustela putorius)

0 Laboratoire de Neurosciences Cognitives, Ho pital de la Salpetrie` re , Paris 75651 , France 1 Department of Morphological Neuroscience, Gifu University School of Medicine , Gifu 501- 1194 , Japan 2 Department of Neuroscience, Karolinska Institutet , S-17177 Stockholm , Sweden 3 The Author 2007. Published by Oxford University Press. All rights reserved. For permissions , please 4 Department of Biomodeling and Bioinformatics, Eindhoven University of Technology , Eindhoven 5600 MB , The Netherlands In mammals, the visual field is split along the midline, each hemisphere representing the contralateral hemifield. We determined that, in the ferret, an 8- to 10-deg-wide strip of visual field near the midline is represented in both hemispheres. Bright squares (1.5 deg) were flashed at different azimuths within the central 20 deg of the visual field. Stimuli were flashed either alone or sequentially, and the responses were analyzed with the voltagesensitive dye (VSD) RH 795 and/or by recording local field potentials (LFPs). In both VSD and LFP experiments, each stimulus evoked a cortical response field that extended over visual areas 17 and 18 up to a surface of 1--1.5 mm2 and then shrank again. Amplitude of the responses decreased approaching the visual midline and the latency increased. These positional differences are likely to originate from the spatiotemporal structure of the peripheral response fields (PRFs) that form a mosaic in areas 17 and 18, interrupted near the visual midline. Unexpectedly, interhemispheric connections appear not to modify these PRFs' effects and may not contribute to the responses to discrete, flashed stimuli. Introduction The cerebral cortex contains orderly, discrete representations of the sensory peripheries, that is, the stimulation of neighboring points, on the peripheries, activates neighboring neurons in the related cortical areas. Two mechanisms contribute to integrating responses across the cortical sensory maps. One is the divergence/convergence in the afferent projections such that neighboring points in the sensory periphery activate overlapping cortical territories. The second are the tangential connections within the cortical maps. The cortical representations of the sensory peripheries are dynamic constructs, continuously updated by incoming inputs. The number and spatial distribution of cortical neurons activated by a peripheral stimulus (here referred to as the cortical response field [CRF]; see Discussion) change with time after stimulus onset, expanding and contracting over a time scale of 100--200 ms (Grinvald et al. 1994; Petersen and Diamond 2000; Petersen et al. 2003). This aspect of CRF dynamics is believed to reflect the tangential spread of activity along horizontal corticocortical connections (Petersen et al. 2003). The splitting of the sensory representations between the 2 hemispheres raises special problems. The representation of the retina, in particular, is divided between the 2 hemispheres along a line corresponding to the nasotemporal decussation of ganglion cell axons at the chiasm. This line is unsharp, and therefore, a narrow strip of the visual field midline is represented in both hemispheres. Interestingly, the cortical representations of this strip are also preferentially interconnected by callosal axons (Innocenti 1986; Manger et al. 2002). Here and in the companion paper (Makarov et al. Forthcoming), we investigate the role of interhemispheric connections in integrating the 2 hemirepresentations of the visual field. The rationale for the present study was the following. Whereas within the hemifield representations, the dynamics of the CRF should reflect conduction along the short intra-areal axons, near the visual midline they should reflect conduction along the long callosal axons. The different lengths and hence conduction delays of the 2 axonal systems should cause significant differences in the dynamics of the responses to stimuli presented along the midline versus those presented in the periphery of the visual field. However, the notion that callosal connections may fail to perfectly integrate the 2 hemifield representations conflicts with the widely accepted belief that the intrahemispheric (including intra-areal) and callosal axons are functionally equivalent, albeit specialized for different portions of the visual field (reviewed in Innocenti 1986; Kennedy et al. 1991). Furthermore, the recent evidence pointing to precise timing as an essential requirement in cortical function (e.g., Engel et al. 1997; Ikegava et al. 2004; Izhikevich et al. 2004) would suggest that the temporal properties of the response to a visual stimulus should be similar across the visual field. To analyze how the visual field is integrated along the interhemispherically split visual midline, we first investigated the width of the bihemispheric visual field representation. We next flashed short-lasting square stimuli alone or in a sequence at different positi (...truncated)


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Hiroyuki Nakamura, Maximilien Chaumon, Floor Klijn, Giorgio M. Innocenti. Dynamic Properties of the Representation of the Visual Field Midline in the Visual Areas 17 and 18 of the Ferret (Mustela putorius), Cerebral Cortex, 2008, pp. 1941-1950, 18/8, DOI: 10.1093/cercor/bhm221