Abnormal retinotopic representations in human visual cortex revealed by fMRI

Abstract

The representation of the visual field in early visual areas is retinotopic. The point-to-point relationship on the retina is therefore maintained on the convoluted cortical surface. Functional magnetic resonance imaging (fMRI) has been able to demonstrate the retinotopic representation of the visual field in occipital cortex of normal subjects. Furthermore, visual areas that are retinotopic can be identified on computationally flattened cortical maps on the basis of positions of the vertical and horizontal meridians. Here, we investigate abnormal retinotopic representations in human visual cortex with fMRI. We present three case studies in which patients with visual disorders are investigated. We have tested a subject who only possesses operating rod photoreceptors. We find in this case that the cortex undergoes a remapping whereby regions that would normally represent central field locations now map more peripheral positions in the visual field. In a human albino we also find abnormal visual cortical activity. Monocular stimulation of each hemifield resulted in activations in the hemisphere contralateral to the stimulated eye. This is consistent with abnormal decussation at the optic chiasm in albinism. Finally, we report a case where a lesion to white matter has resulted in a lack of measurable activity in occipital cortex. The activity was absent for a small region of the visual field, which was found to correspond to the subject's field defect. The cases selected have been chosen to demonstrate the power of fMRI in identifying abnormalities in the cortical representations of the visual field in patients with visual dysfunction. Furthermore, the experiments are able to show how the cortex is capable of modifying the visual field representation in response to abnormal input.

Introduction

In primates, the cortical representation of the visual field in early visual areas is retinotopic. That is, neighbouring points on the retina project to neighbouring points on the cortical surface. In this article we focus on abnormal retinotopic cortical maps in human. We have studied patients with different visual dysfunction, which arise at different sites on the visual pathway. We endeavour to reveal the potential for the cortex to reorganise in the light of abnormal retinal input, and how visual cortical signals can reveal the underlying cause of visual field defects. For each of the studies described we concentrate on the cortical representation of the visual field that can be documented with functional magnetic resonance imaging (fMRI). We review briefly the evidence for retinotopic representations of the visual field in the human visual cortex. This is followed by a description of the general methods used to map retinotopic areas of the human occipital lobe with fMRI. Three case studies that demonstrate abnormal retinotopic representations in human visual cortex are then presented.

Holmes (1918) was able to determine the topographic mapping of the visual field onto calcarine cortex by documenting visual field defects of soldiers who suffered gunshot wounds to the occipital lobe. More detailed lesion studies along similar lines have allowed a fuller picture of the topographic cortical representation to be gained (Horton & Hoyt, 1991a; Sharpe & Wong, 1997). Studies of human patients with damage to extrastriate regions of the visual cortex revealed the nature and extent to which visual processing depended on areas beyond the calcarine sulcus (Clarke, Walsh, Schoppig, Assal, & Cowey, 1998; Damasio, Yamada, Damasio, Corbett, & McKee, 1980; Kennard, Lawden, Morland, & Ruddock, 1995; Zihl, von Cramon, & Mai, 1983). In addition, extrastriate lesions were shown to result in visual deficits that are restricted to one quadrant of the visual field (Horton & Hoyt, 1991b). This finding indicated that extrastriate visual areas in dorsal and ventral cortex represent the lower and upper quadrants of the visual field, respectively. Although a considerable amount is known about the visual representation in the human occipital lobe from lesion studies, electrophysiological primate studies have been able to reveal greater detail of the cortical representations of the visual field (Hubel & Wiesel, 1974; Tootell, Switkes, Silverman, & Hamilton, 1988).

Over the last decade functional imaging methods have emerged, which have allowed visual areas of the human brain to be identified and their properties measured (Engel, Glover, & Wandell, 1997; Sereno et al., 1995; Tootell, Dale, Sereno, & Malach, 1996; Zeki et al., 1991). These developments have profound implications on the study of patients with visual dysfunction. The patient can now undergo functional imaging so that information concerning the impact of the lesion on cortical activity elsewhere can be gained (Barbur, Watson, Frackowiak, & Zeki, 1993; Barton et al., 1996; Baseler, Morland, & Wandell, 1999; Sahraie, Weiskrantz, Simmons, Williams, & Barbur, 1996; Zeki & Ffytche, 1998). This represents a great advance, as human lesions are seldom loyal to any boundary that may divide different visual areas, so interpretation on the basis of anatomy alone is error prone. Lesions often involve white matter, and the consequences of such damage on intact cortical structures can only be assessed by measurement and localization of cortical activity. Furthermore, the effects on cortical visual representations of abnormalities that occur at earlier stages of the visual system can also be documented with functional imaging.

Perhaps the most successful implementation of functional imaging in assessing visual cortical function is the retinotopic mapping method based on fMRI. An early study revealed how visual field eccentricity was mapped along the calcarine sulcus (Engel et al., 1994). Studies by the same group (Engel et al., 1997) and others (DeYoe et al., 1996; Sereno et al., 1995) described methods by which visual areas could be identified on the basis of the cortical representations of vertical and horizontal meridians of the visual field. The same criterion for identifying different retinotopic maps had also been established in the studies that evaluated the cortical patterns of neural degeneration associated with sectioning the corpus colosum in monkey (Zeki, 1977) and human (Clarke & Miklossy, 1990).

In this article we will review three different studies that investigate the impact of visual dysfunction on cortical visual responses. The studies differ in the sense that the subjects have visual deficits that are expressed at different levels of the visual system. We first describe the effects on the cortical visual maps of abnormal retinal receptor distributions that are found in rod monochromacy. This study documents how the cortex is able to reorganize in response to abnormal input signals. On a similar theme, we examine how the cortical signals are arranged in human albinos. In human albinism the principal deficit occurs at the optic chiasm, where fibres undergo almost complete crossing unlike the normal pattern in which approximately half of the fibres project contralateral to the eye. We then describe how visual field defects can be documented with retinotopic mapping techniques in the case of cortical lesion. The theme is to demonstrate how the application of fMRI to cases of abnormal vision can reveal properties of the human visual system that are not highlighted by the study of normal vision.