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)