Neural substrate of spatial memory in the superior colliculus after damage to the primary visual cortex

Abstract

In the primate brain, the primary visual cortex (V1) is a major source of visual information processing in the cerebral cortex, although some patients and monkeys with damage to the V1 show visually guided behaviors in the visual field affected by the damage. Until now, behaviors of the surviving brain regions after damage to V1 and their contribution to the residual visual functions remain unclear. Here, we report that the monkeys with a unilateral lesion of V1 can make not only visually guided saccades but also memory-guided saccades (MGS) into the affected visual field. Furthermore, while the monkeys were performing the MGS task, sustained activity was observed in a large fraction of the neurons in the superior colliculus ipsilateral to the lesion, which has been supposed as a key node for recovery after damage to V1. These neurons maintained the spatial information throughout the delay period regardless of whether they exhibited saccadic bursts or not, which was not the case on the intact side. Error analysis revealed that the sustained activity was correlated with monkeys' behavioral outcome. These results suggest that the ipsilesional SC might function as a neural substrate for spatial memory in the affected visual field. Our findings provide new insight into the understanding of the compensatory mechanisms after damage to V1.

Figure 1.

V1 and the extent of the lesion (A) and the experimental conditions (B). A, Top, The figures are line images traced from axial slices of MR images acquired at 1 week before the lesion. V1 is denoted in red (monkey A). The estimated lesion site (depicted in dark gray) is overlaid on the line trace of the axial slices of the MR images acquired after the lesion in monkey A (middle) and in monkey T (bottom). B, Schema of the experimental conditions. In both monkeys, the left V1 was removed. Thus, the right hemifield was affected and the left visual field was normal.

Figure 2.

Behavioral results for the VGS and MGS tasks. A, B, Left, Task schema; middle, trajectories; right; the success rates for each visual field in the two monkeys. In the middle panel, the differences in color indicate differences in the position of the target or the cue. ST, Saccade target. C, Distributions of the saccadic reaction times in monkey T (left) and monkey A (right). The dashed lines represent the results in the VGS task, while the solid lines represent the results in the MGS task. The insets to the right and above show the distribution of the saccadic reaction times in the normal visual field.

Figure 3.

Recording from the ipsi and contra SCs. A, B, Recording configuration (top row), a distribution of the depth of recording sites (lower left), and a map of the recording location (lower right) on each side. The neuronal activity of the ipsi SC (A, top row) and the contra SC (B, top row) was recorded while the monkeys were performing the tasks in the affected visual filed (A, top) or in the normal visual field (B, top). The target or the cue was presented inside the RF, RF_in, or outside the RF, RF_out, separated by 90° in direction. In the lower left panels, the open histograms indicate the visuomotor neurons and the shaded histograms indicate the visual neurons.

Figure 4.

Neuronal activity during the VGS task. A, Schema of the task and the raster plots of representative neurons in the ipsi SC (top row) and the contra SC (bottom row). ST, Saccade target. B, C, Activity of visuomotor neuron and visual neuron populations. Top rows, Spike density functions; bottom rows, time course of the AUC (area under the curve of the receiver operating characteristics curve, see Material and Methods). The left column shows the activity aligned with the target onset, and the right column shows the activity aligned with the saccade onset.

Figure 5.

Comparison of the basic properties of visual response and saccadic burst between the ipsi and the contra SCs. A, Comparison of visual responses. Right column, Magnitudes; left column, latencies. Top, Visuomotor neurons; bottom, visual neurons. Error bars in the bar graphs indicate SD. B, Comparison of the magnitude of the saccadic bursts. C, Top, Comparison of the magnitudes of the prestimulus activity. Bottom, Distribution of the net magnitudes of visual responses calculated by subtraction of the prestimulus activity from the gross magnitudes of visual response. A–C, The open histograms indicate the ipsi SC, and the shaded histograms indicate the contra SC. The arrowheads indicate the averaged firing rates; spks/s, Spikes per second.

Figure 6.

Neuronal activity during the MGS task. A, Schema of the task and the raster plots of representative neurons in the ipsi SC (top row) and contra SC (lower row). B, C, Activity of visuomotor neuron and visual neuron populations. Top rows, Spike density functions; lower rows, time course of the AUC. The left columns show activity aligned with the cue onset, the middle columns show activity aligned with the FP offset, and the right columns show activity aligned with the saccade onsets. Shaded areas indicate epochs 1-3.

Figure 7.

Distribution of the AUC in epochs 1-3 (Fig. 6B,C, indicated by shaded areas). A, B, The visuomotor and visual neurons were merged in the ipsi SC (A) and the contra SC (B), respectively.

Figure 8.

Error analysis. A, B, Activity of a representative neuron in the RF_in trials (A) and RF_out trials (B). In this session, we used a smaller sized cue to collect a sufficient number of error trials. C, Population analysis of the error trials. Activity during the 300 ms of the last part of the delay period was compared between the correct trials and error trials. The visuomotor and visual neurons were merged. Data represent mean ± SE; *p < 0.05 according to Mann–Whitney U test with Bonferroni's correction for multiple comparison; spks/s, Spikes per second.