Persistent neural activity during the maintenance of spatial position in working memory

Abstract

The mechanism for the short-term maintenance of information involves persistent neural activity during the retention interval, which forms a bridge between the cued memoranda and its later contingent response. Here, we used event-related functional magnetic resonance imaging to identify cortical areas with activity that persists throughout working memory delays with the goal of testing if such activity represents visuospatial attention or prospective saccade goals. We did so by comparing two spatial working memory tasks. During a memory-guided saccade (MGS) task, a location was maintained during a delay after which a saccade was generated to the remembered location. During a spatial item recognition (SIR) task identical to MGS until after the delay, a button press indicated whether a newly cued location matched the remembered location. Activity in frontal and parietal areas persisted above baseline and was greater in the hemisphere contralateral to the cued visual field. However, delay-period activity did not differ between the tasks. Notably, in the putative frontal eye field (FEF), delay period activity did not differ despite that the precise metrics of the memory-guided saccade were known during the MGS delay and saccades were never made in SIR. Persistent FEF activity may therefore represent a prioritized attentional map of space, rather than the metrics for saccades.

Figure 1

a. Schematic of the memory-guided saccade (MGS) and spatial item-recognition (SIR) tasks. In both tasks, subjects maintained the position of a sample cue over a long and variable delay period. After the delay, subjects made a memory-guided saccade to the cued location in the MGS task. They decided whether a test cue matched the location of the sample cue (dotted box; was not visible to subject) in the SIR task. See methods for details. b. Horizontal eye position traces from single blocks of the MGS and SIR tasks in an example subject. (black line – eye position; grey line – target position).

Figure 2

Key regions of interest (ROI) are denoted on the grey-white matter boundary of the right lateral and left medial hemisphere folded (a) and inflated (b). Dark grey overlay indicates sulci, while light grey indicates gyri. Abbreviations: dm-sPCS = dorsal medial superior precentral sulcus; dl-sPCS = dorsal lateral superior precentral sulcus; iPCS = inferior precentral sulcus; pIFS = posterior inferior frontal sulcus; IPS = intraparietal sulcus; tPS = transverse parietal sulcus.

Figure 3

Behavioral data. a. Eye trace of a memory guided saccade (MGS) to a cued location in the lower right visual field. The difference between the fixation following the MGS and the corrective saccade after feedback was given was used to calculate the error in degrees of visual angle. b, d. Performance on the MGS and SIR tasks as a function of the delay period interval. Notice that the delay length does not affect performance. c. Performance was statistically the same in each subject for MGS and SIR tasks. e. Psychometric function for performance on the SIR task as function of the distance of the non-match test cue from the sample cue location. Each dot represents the average SIR accuracy when the sample cue location and the test cue did not match by the various distances. Notice that performance was successfully modified by this manipulation. f. Scatter plot illustrating that the separation distance between the sample cue and the non-match test cue that resulted in 50% SIR accuracy predicts the subject’s average MGS error.

Figure 4

Sample cue, memory delay and memory-guided response related activity. a. Encoding the position of the sample cue evoked a similar pattern of BOLD activity during the MGS and SIR tasks. b. Similarly, maintaining the sample cue’s position evoked a remarkable similar pattern of BOLD activity during the MGS and SIR tasks. After the delay period, memory for the sample cue’s location was tested by having subjects make an eye movement in the MGS task or a manual button response with the right hand in the SIR task. Panel c. shows the direct MGS vs SIR contrast at the response epoch rendered on the left and right dorsal cortical hemispheres.

Figure 5

Trial-averaged BOLD time courses aligned on the presentation of the sample cue during the MGS task. Only data from the hemisphere contralateral to the visual field within which the sample cue was presented are included. Separate lines represent the different delay lengths, where the time of the memory-guided saccade is indicated by the colored triangle. The peaks of the responses are staggered according to the memory delay length. Importantly, several regions of interest show evidence of sustained activity regardless of the length of the delay, even at very long delays. See Figure 2 for a list of the abbreviated regions.

Figure 6

Trial-averaged BOLD time courses time-locked to the presentation of the sample cue and the generation of the memory-guided response for the MGS and SIR tasks. Data from the hemisphere contralateral and ipsilateral to the visual field within which the sample cue was presented are plotted separately. See Figure 2 for abbreviated regions.

Figure 7

Indices of laterality bias during the delay periods of the MGS (left column) and SIR (right column) tasks. Each dot represents a subject’s laterality index (see methods for computation), where dots above the line of equality denote subjects whose delay period activity was greater when maintaining spatial positions in the contralateral compared to ipsilateral visual field. Only the dl-sPCS and IPS showed a contra-lateral bias. The ratio in the upper left corner is the fraction of subjects who showed a contralateral bias. See Figure 2 for a list of the abbreviated regions.