Maintenance of spatial and motor codes during oculomotor delayed response tasks

Abstract

The most compelling neural evidence for working memory is persistent neuronal activity bridging past sensory cues and their contingent future motor acts. This observation, however, does not answer what is actually being remembered or coded for by this activity. To address this fundamental issue, we imaged the human brain during maintenance of spatial locations and varied whether the memory-guided saccade was selected before or after the delay. An oculomotor delayed matching-to-sample task (match) was used to measure maintained motor intention because the direction of the forthcoming saccade was known throughout the delay. We used a nonmatching-to-sample task (nonmatch) in which the saccade was unpredictable to measure maintained spatial attention. Oculomotor areas were more active during match delays, and posterior parietal cortex and inferior frontal cortex were more active during nonmatch delays. Additionally, the fidelity of the memory was predicted by the delay-period activity of the frontal eye fields; the magnitude of delay-period activity correlated with the accuracy of the memory-guided saccade. Experimentally controlling response selection allowed us to functionally separate nodes of a network of frontal and parietal areas that usually coactivate in studies of working memory. We propose that different nodes in this network maintain different representational codes, motor and spatial. Which code is being represented by sustained neural activity is biased by when in the transformation from perception to action the response can be selected.

Figure 1.

Schematic depiction of the oculomotor delayed-response tasks in which subjects used the location of the cue to make a memory-guided saccade. Both the matching-to-sample (top) and nonmatching-to-sample (bottom) tasks began with the brief presentation of a small green sample cue while the subject maintained central fixation. The cue appeared randomly at 1 of 16 possible locations at a 10° radius, none of which lie on the cardinal axes. A masking pattern was then briefly presented to disrupt iconic visual memory, followed by a long unfilled memory delay. During matching trials, the subject made a memory-guided saccade (depicted by the thin black line) after the disappearance of the fixation cue marking the end of the delay. Feedback was provided by the re-presentation of the cue. At this point, the subject corrected any errors by shifting gaze to the cue. The difference between the endpoint fixation after the memory-guided saccade and the fixation to acquire the feedback cue was used as an index of memory accuracy. During nonmatching trials, the subject made a saccade to the green square that did not match the location of the sample cue. ITI, Intertrial interval.

Figure 2.

Stimulus cue. Statistical parametric t maps contrasting stimulus cue activity between the oculomotor delayed matching-to-sample and nonmatching-to-sample tasks. Warm colors depict regions with greater cue period activity on matching than nonmatching trials. Cool colors depict regions with greater cue period activity on nonmatching than matching trials. MFG, Middle frontal gyrus.

Figure 3.

Statistical parametric t map of delay-period activity overlaid on a surface rendering of brain. The contrast was formed by collapsing across both oculomotor delayed matching-to-sample and nonmatching-to-sample delay periods. This delay-period contrast represents a linear combination of the delay-period regressors.

Figure 4.

Delay period. Statistical parametric t maps contrasting oculomotor delayed matching-to-sample versus nonmatching-to-sample delay-period-specific activity. Early (a) and late (b) delay contrasts are shown. Warm colors depict regions with greater delay-period activity on matching than nonmatching trials. Cool colors depict regions with greater delay-period activity on nonmatching than matching trials. MFG, Middle frontal gyrus; iPCS, inferior precentral sulcus.

Figure 5.

Scatterplot showing the correlation between memory-guided saccade (MGS) accuracy and the magnitude of the matching-to-sample delay-period parameter estimates in the right FEF. More accurate memory-guided saccades were associated with greater delay-period activity. Approximately one-quarter of the variance in the accuracy of the memory-guided saccade was predicted by the magnitude of delay-period activity. Similar correlations were found in the left FEF and right IPS.

Figure 6.

Memory-guided saccades. Statistical parametric t maps contrasting memory-guided saccades during the delayed matching-to-sample versus nonmatching-to-sample tasks. Warm colors depict regions with greater saccade period activity on matching than nonmatching trials. Cool colors depict regions with greater saccade period activity on nonmatching than matching trials. MFG, Middle frontal gyrus; SFS, superior frontal sulcus; iPCS, inferior precentral sulcus; POS, parietal-occipital sulcus; PCU, precuneus.

Figure 7.

Average ± SE BOLD time series data (15 subjects) for matching-to-sample (thick black line) and nonmatching-to-sample (thin gray line) oculomotor delayed-response tasks. The solid gray bar represents the delay interval. The gray gradient in the background depicts the probability that the BOLD signal is emanating from the delay period, and the darker indicates more probable. The right FEF and SEF show greater delay-period activity during the matching task, in which an oculomotor strategy is efficient. The right IPS shows greater delay-period activity during the nonmatching task when subjects are biased from using such a strategy. The middle frontal gyrus (BA 46) shows a trend toward greater activity early in the delay on matching trials and then switches and shows significantly greater activity on the nonmatching trials. Error bars indicate SEM.