Role of inter-hemispheric transfer in generating visual evoked potentials in V1-damaged brain hemispheres

Abstract

Partial cortical blindness is a visual deficit caused by unilateral damage to the primary visual cortex, a condition previously considered beyond hopes of rehabilitation. However, recent data demonstrate that patients may recover both simple and global motion discrimination following intensive training in their blind field. The present experiments characterized motion-induced neural activity of cortically blind (CB) subjects prior to the onset of visual rehabilitation. This was done to provide information about visual processing capabilities available to mediate training-induced visual improvements. Visual Evoked Potentials (VEPs) were recorded from two experimental groups consisting of 9 CB subjects and 9 age-matched, visually-intact controls. VEPs were collected following lateralized stimulus presentation to each of the 4 visual field quadrants. VEP waveforms were examined for both stimulus-onset (SO) and motion-onset (MO) related components in postero-lateral electrodes. While stimulus presentation to intact regions of the visual field elicited normal SO-P1, SO-N1, SO-P2 and MO-N2 amplitudes and latencies in contralateral brain regions of CB subjects, these components were not observed contralateral to stimulus presentation in blind quadrants of the visual field. In damaged brain hemispheres, SO-VEPs were only recorded following stimulus presentation to intact visual field quadrants, via inter-hemispheric transfer. MO-VEPs were only recorded from damaged left brain hemispheres, possibly reflecting a native left/right asymmetry in inter-hemispheric connections. The present findings suggest that damaged brain hemispheres contain areas capable of responding to visual stimulation. However, in the absence of training or rehabilitation, these areas only generate detectable VEPs in response to stimulation of the intact hemifield of vision.

Keywords: Callosal connections; Cortical blindness; Hemianopia; Inter-hemispheric transfer time; Visual cortex.

Copyright © 2015 Elsevier Ltd. All rights reserved.

Figures

Figure 1

Humphrey visual field perimetry (24-2 test) assessed monocularly and averaged across the two eyes. The grey scale indicates average luminance detection sensitivity in dB. Circles represent the visual field locations and sizes of random dot stimuli the subjects were asked to discriminate: red circles indicate stimuli that were presented in quadrants of intact vision, while blue circles represent stimuli that were not discriminable because they were presented inside blind regions of the visual field.

Figure 2

Schematic illustration of the global direction discrimination task performed during acquisition of Visual Evoked Potentials (VEPs). On each trial, after a random inter-trial interval of 1–2 s, a fixation cross appeared in the center of the computer screen for 1 s, followed by a cloud of stationary random dots presented inside a 5 deg diameter window in one of the 4 visual field quadrants. After an interval that varied randomly between 1–2 s, the dots began to move either to the right or the left for 500 ms. Subjects were asked to indicate direction of motion of the stimulus as soon as possible (Respond ASAP).

Figure 3

Recording of Visual Evoked Potentials (VEPs) during lateralized stimulus presentation. A: Schematic representation of 64 electrode locations used, with analyzed electrodes highlighted in black (contralateral to stimulus presentation, indicated in the cartoon on top) and red (ipsilateral to stimulus presentation). Ipsilateral responses are thought to arise because of inter-hemispheric transfer from the brain hemisphere contralateral to the presented stimulus. B: Grand average waveforms obtained from the contralateral and ipsilateral brain hemispheres in visually-intact control subjects for stimulus onset VEPs (SO-VEPs) during stimulus presentation in the lower left visual field quadrant (shown in A). Vertical line at time 0 ms indicates random dots onset. P1, N1, and P2 designate SO-VEP components analyzed. The black line shows SO-VEP responses from the brain hemisphere contralateral to the presented stimulus - i.e. from pooled P6, P8, PO8, and PO10 electrodes (outlined in black in A). Red line shows SO-VEP responses from the brain hemisphere ipsilateral to the presented stimulus - i.e., from pooled P5, P7, PO7, and PO9 electrodes (outlined in red in A). C: Grand average waveforms of control subjects for motion onset VEPs (MO-VEPs) illustrating the clear N2 component obtained for stimulus presentation in the lower left quadrant. Vertical line at time 0 indicates the onset of dot motion. As in B, the black waveform represents contralateral MO-VEP response, while the red waveform represents the ipsilateral MO-VEP response. In both B and C, the difference in latency between the red and back peaks/troughs denotes the inter-hemispheric transfer time.

Figure 4

Global direction discrimination performance in each quadrant of the visual field. A: Mean accuracies of control subjects for motion direction discrimination in the DR0 (open bars) and DR320 (grey shaded bars) conditions for all 4 visual field quadrants. B: Average response times of control subjects for motion direction discrimination with respect to DR0 (open bars) and DR320 (grey shaded bars) stimuli presented to each visual field quadrant. C: Plot of average accuracy exhibited by CB subjects when discriminating direction of motion of DR0 motion stimuli, indicated separately for stimulus presentation to intact (open bars) and blind (shaded bars) visual field quadrants. D: Average response times for CB subjects performing the global direction discrimination task using DR0 stimuli, plotted separately for stimulus presentation to intact (open bars) and blind (striped bars) visual field quadrants. E: Average accuracy of CB subjects while performing the direction discrimination task using DR320 stimuli, plotted separately for intact (solid grey bars) and blind (striped grey bars) visual field quadrants. F: Average response times of CB subjects performing the global direction discrimination task using DR320 motion stimuli, plotted separately for intact (solid grey bars) and blind (striped grey bars) visual field quadrants. See text for statistical results. UL = upper left quadrant, LL = lower left quadrant, UR = upper right quadrant, LR = lower right quadrant. Values plotted are means ± SEM. Numbers above bars in lower panels represent the number of participants in the mean for each particular quadrant.

Figure 5

Grand average waveforms in control subjects. A: Mean grand average SO-VEPs averaged across all 4 visual field quadrants. B: Mean grand average MO-VEPs for DR0 motion stimuli. C: Mean grand average MO-VEPs for DR320 motion stimuli. Black traces represent MO-VEP responses from the brain hemisphere contralateral to stimulus presentation. Red traces represent MO-VEP responses from the brain hemisphere ipsilateral to stimulus presentation.

Figure 6

Comparison of grand average waveforms following stimulus presentation to intact visual quadrants of CB subjects (black traces) and corresponding locations in visually-intact controls (grey traces). A: Grand average waveforms for SO-VEPs. B: Grand average waveforms for MO-VEPs.

Figure 7

Grand average waveforms obtained in response to stimulus onset (SO-VEPS) and motion onset (MO-VEPs) in CB subjects. A: Grand average SO-VEPs obtained contralateral (black trace) or ipsilateral (red trace) to intact visual field quadrants, and contralateral (gray trace) or ipsilateral (orange trace) to blind field quadrants. B: Grand average MO-VEP waveforms for DR0 motion stimuli obtained in CB subjects with left brain hemisphere damage only. Color conventions as in A. C: Grand average MO-VEP waveforms for DR0 motion stimuli for CB subjects with right brain hemisphere damage only. Color conventions as in A.

Figure 8

Latencies of visually-evoked components and inter-hemispheric transfer patterns in controls and CB subjects. A. Mean latencies for SO-P1, N1 and P2 components obtained from brain hemispheres contralateral (black bars) and ipsilateral (red bars) to visual stimuli presented to control subjects. A significant delay is observed between contra- versus ipsilaterally evoked responses for all components except for P2. B. Mean latencies for the MO-N2 component elicited from brain hemispheres contralateral and ipsilateral to visual stimuli (either DR0 – left bars, or DR320 – right bars) presented to control subjects. Note the significant delay for information reaching the ipsilateral brain hemisphere. C. Mean latencies for SO-P1, N1 and P2 components obtained from brain hemispheres contralateral and ipsilateral to visual stimuli presented to CB subjects. Data were averaged across all subjects. D. Mean latencies for the MO-N2 component elicited from brain hemispheres contralateral and ipsilateral to visual stimuli (either DR0 or DR320) presented to CB subjects with left brain hemisphere damage. Right-damaged subjects did not exhibit interhemispheric transfer for motion-evoked responses. Error bars = SEM. * = significant differences (see text for statistics). E. Schematic representation of interhemispheric transfer in visually intact controls (top diagram), as well as CB subjects with either left or right brain hemisphere V damage (bottom two diagrams). Mean ± SEM interhemispheric transfer times (IHTT) are provided for SO and MO-VEPs which exhibited them. LGN: lateral geniculate nucleus, SC: superior colliculus.