The primary visual cortex, and feedback to it, are not necessary for conscious vision

Abstract

A compelling single case report of visual awareness (visual qualia) without primary visual cortex would be sufficient to refute the hypothesis that the primary visual cortex and the back-projections to it are necessary for conscious visual experience. In a previous study, we emphasized the presence of crude visual awareness in Patient G.Y., with a lesion of the primary visual cortex, who is aware of, and able to discriminate, fast-moving visual stimuli presented to his blind field. The visual nature of Patient G.Y.'s blind field experience has since been questioned and it has been suggested that the special circumstances of repeated testing over decades may have altered Patient G.Y.'s visual pathways. We therefore sought new evidence of visual awareness without primary visual cortex in patients for whom such considerations do not apply. Three patients with hemianopic field defects (Patient G.N. and Patient F.B. with MRI confirmed primary visual cortex lesions, Patient C.G. with an inferred lesion) underwent detailed psychophysical testing in their blind fields. Visual stimuli were presented at different velocities and contrasts in two- and four-direction discrimination experiments and the direction of motion and awareness reported using a forced-choice paradigm. Detailed verbal reports were also obtained of the nature of the blind field experience with comparison of the drawings of the stimulus presented in the blind and intact fields, where possible. All three patients reported visual awareness in their blind fields. Visual awareness was significantly more likely when a moving stimulus was present compared to no stimulus catch trials (P < 0.01 for each subject). Psychophysical performance in Patient F.B. and Patient G.N. was consistent with the Riddoch syndrome, with higher levels of visual awareness for moving compared to static stimuli (P < 0.001) and intact direction discrimination (P < 0.0001 for two- and four-direction experiments). Although the blind field experience of all three subjects was degraded, it was clearly visual in nature. We conclude that the primary visual cortex or back-projections to it are not necessary for visual awareness.

Figure 1

Patient G.N. (A) The visual field in Patient G.N.’s left and right eye. The black region shows the hemianopic left visual field with involvement of the macular region. Scale = 30° horizontal and vertical eccentricity. (B) Coronal MRI slices showing the extent of the lesion in Patient G.N.’s right occipital lobe. The lesion involves the medial and polar surface of the right hemisphere, and includes the upper and lower banks of the calcarine fissure and lingual gyrus but spares the lateral occipital surface. (C) Axial MRI slices of the lesion showing its anterior extension to the parahippocampal gyrus.

Figure 2

Patient F.B. (A) The visual field in Patient F.B.’s left and right eye. The black region shows the hemianopic right visual field with sparing at the vertical meridian in the right superior quadrant. Scale = 30° horizontal and vertical eccentricity. (B) Axial MRI slices showing the extent of Patient F.B.’s lesion. It involves the medial and polar surface of the left occipital lobe but spares its lateral surface.

Figure 3

The visual fields in Patient C.G.’s left and right eye. Darker black bars indicate areas of field loss. Patient C.G. has a left hemianopia involving the macular region with some sparing of the left lower quadrant at the vertical meridian.

Figure 4

Phenomenology. Patient G.N. and Patient F.B.’s drawings of the experiences in their blind hemifields. Patient G.N. was also asked to draw his experience of the same stimulus when presented in his intact field for comparison. Both subjects are able to depict their experiences visually as well as provide a verbal report of their visual nature.

Figure 5

Discrimination and awareness for fast and slow motion. Percent correct responses are plotted against percent aware responses for up/down experiments in Patients G.N. (circles) and F.B. (squares) (shaded rows in Table 1). Slow-motion trials are shown in red, fast-motion trials in blue. The black line indicates the predicted performance of patients with the Riddoch syndrome with the upper and lower limits of chance at P < 0.05 given by the dotted lines (Zeki and ffytche, 1998). The red square labelled ‘high’ is the high contrast, slow-motion experiment for Patient F.B.