Short-term memory and perceptual decision for three-dimensional visual features in the caudal intraparietal sulcus (Area CIP)

Abstract

The purpose of the present study was to examine whether neurons in the caudolateral part of the intraparietal sulcus (area CIP), a part of the posterior parietal cortex, contribute to short-term memory and perceptual decision of three-dimensional (3D) surface orientation, in addition to its purely visual nature of responding selectively to 3D surface orientation. Activities of CIP neurons were recorded while monkeys performed a modified delayed matching-to-sample (DMTS) task using stereoscopic stimuli. Seventy-seven neurons were examined with a routine of the DMTS task, and 94% (72 of 77) of them showed selectivity to surface orientation. Furthermore, 82% (63 of 77) of the examined neurons showed sustained activity during delay, and 60% (38 of 63) of them showed selective delay activity depending on the sample stimulus, suggesting that they contribute to short-term memory of 3D visual features. On the other hand, 53% (41 of 77) of the examined neurons showed modulation of visual response depending on whether a stimulus appeared as a sample, match, or nonmatch stimulus (contextual modulation). The majority (73%, 30 of 41) of these neurons with contextual modulation showed activity change depending on whether the test stimuli did or did not match the sample stimuli (match-nonmatch modulation), suggesting their involvement in matching, or perceptual decision, concerning 3D visual features. These findings suggest that CIP neurons play important roles not only in the perception of 3D visual features but also in cognitive functions such as short-term memory and perceptual decision of 3D visual information.

Figure 1.

Outline of go–no-go DMTS or successive same–different discrimination. Monkeys had to make a go or no-go response depending on whether the 3D orientation of sample and test stimuli were the same or different. FS, Fixation spot; Stm, stimulus.

Figure 2.

Schematic illustration indicating the location of CIP in the top view of the left hemisphere.The intraparietal sulcus (ips), lunate sulcus (lu), and parietooccipital sulcus (po) are unfolded. AIP, Anterior intraparietal; VIP, ventral intraparietal; MIP, medial intraparietal; LIP, lateral intraparietal; PP, posterior parietal; PO, parietooccipital. CIP is located caudally and laterally in the intraparietal cortex between areas LIP and V3A and probably overlaps area LOP of the architectonic definition by Lewis and Van Essen (2000).

Figure 3.

Responses of a typical CIP neuron showing consistent selectivity to a 3D surface orientation regardless of the context of presentation (sample, match, or nonmatch). The bar beneath each histogram indicates when the stimulus was on. Two markers in each raster line indicate stimulus onset and offset. Responses to three different orientations (135 and 315° tilt plus frontoparallel orientation) are displayed, although unit activity was recorded with a set of nine different orientations. Insets indicate the stimuli presented; solid lines represent the orthographic projection of the simulated plate onto the frontoparallel plane; dashed lines schematically represent the orientation of the surface in depth caused by binocular disparity; and the arrow represents the surface normal.

Figure 4.

Plot of the preferred orientation for sample (x-axis) and match (y-axis) stimuli. Each dot represents one neuron.

Figure 5.

Activities of two typical sample-selective delay neurons showing decreasing (left column) and increasing (right column) trends. Note that all neuronal data during sample stimulus presentation and delay periods are sorted by a sample stimulus tilt angle. The broken-line graphs at the bottom indicate average discharge rates for different tilt angles during sample stimulus presentation (filled circles), former (F) half of delay (open triangles), and latter (L) half of delay (inverted open triangles). Dotted lines in the broken-line graphs indicate the spontaneous activity, and error bars indicate SE. FP, Frontoparallel orientation. Rasters and histograms above each broken-line graph display neuronal activities for three representative sample stimulus tilt angles. Bars at the top of the rasters indicate when the sample and test stimuli were on. Markers in each raster line indicate stimulus onset and offset. Other conventions of rasters and histograms are the same as in Figure 3.

Figure 6.

Plot of the preferred orientation during sample stimulus presentation (x-axis) and delay (y-axis) periods. Each dot represents one neuron. Note that all neuronal data during sample stimulus presentation and delay periods are sorted by sample stimulus tilt angle. A, Plot of the preferred orientation during the former half of the delay against that during the sample presentation period for 31 neurons that showed selective activity during both the sample presentation and the former delay. B, Plot of the preferred orientation during the latter half of delay against that during the sample presentation period for 19 neurons that showed selective activity during both the sample presentation and the latter delay.

Figure 7.

Distribution of delay trend indices showing the delay activity trend. A, Distribution of indices of 38 selective delay neurons. B, Distribution of 25 nonselective delay neurons. The index was calculated for each neuron by dividing the difference in activity between the former and latter delays by their sum, so an index >0 indicates an increasing trend, whereas one <0 indicates a decreasing trend.

Figure 8.

Broken-line graphs showing average response to stimuli of nine different orientations in different contexts: sample (closed circles), match (open triangles), and nonmatch (open inverted triangles). A, Responses of a typical neuron showing no contextual modulation of visual response, whose responses to three representative orientations are shown in the rasters and histograms in Figure 3. B, Responses of a typical neuron showing larger responses to match stimuli than to nonmatch stimuli. C, Responses of a typical neuron showing larger responses to test (match and nonmatch) stimuli than to sample stimuli. Dotted lines indicate the spontaneous activity, and error bars indicate SE. FP, Frontoparallel orientation.

Figure 9.

Population average histograms (top row) and their cumulative histograms (bottom row) of responses to preferred orientation in three different contexts (sample, match, and non-match). A, Averaged response of 24 match–nonmatch modulation neurons showing larger responses to match stimuli. B, Averaged response of six match–nonmatch modulation neurons showing larger responses to nonmatch stimuli. C, Averaged response of six sample–test modulation neurons showing larger responses to sample stimuli. D, Averaged response of eight sample–test modulation neurons showing larger responses to test stimuli. Differential latencies between the sample and match stimulus, sample and nonmatch stimulus, and match and nonmatch stimulus are indicated by closed triangles, open triangles, and arrows, respectively, in the cumulative histograms. The difference of activity between match and nonmatch trials did not reach statistical significance in neurons with sample–test modulation. For the calculation of differential latencies, see Materials and Methods.

Figure 10.

Distribution of the OCIs showing the relative power of the factors of orientation and context over neuronal responses. An index >0 indicates a larger effect of orientation, whereas one <0 indicates a larger effect of context. For details concerning how we calculated the OCI, see Materials and Methods.