Rank signals in four areas of macaque frontal cortex during selection of actions and objects in serial order

Abstract

Neurons in several areas of monkey frontal cortex exhibit ordinal position (rank) selectivity during the performance of serial order tasks. It has been unclear whether rank selectivity or the dependence of rank selectivity on task context varies across the areas of frontal cortex. To resolve this issue, we recorded from neurons in the supplementary motor area (SMA), presupplementary motor area (pre-SMA), supplementary eye field (SEF), and dorsolateral prefrontal cortex (dlPFC) as monkeys performed two oculomotor tasks, one requiring the selection of three actions in sequence and the other requiring the selection of three objects in sequence. We found that neurons representing all ranks were present in all areas. Only to a moderate degree did the prevalence and nature of rank selectivity vary from area to area. The two most prominent inter-area differences involved a lower prevalence of rank selectivity in the dlPFC than in the other areas and a higher proportion of neurons preferring late ranks in the SMA and SEF than in the other areas. Neurons in all four areas are rank generalists in the sense of favoring the same rank in both the serial action task and the serial object task.

Fig. 1.

Sequence of events in 2 serial order tasks. Arrows indicate saccades and broken circles indicate direction of gaze. A: a typical trial in the serial action task. The identity of an image presented at 3 locations in the visual field periphery served as a sequence cue (e.g., the picture of a butterfly instructed the monkey to make a saccade upward during the 1st trial phase, rightward during the 2nd phase, and leftward during the 3rd phase). Six different pictures signaled 6 different sequences. B: a typical trial in the serial object task. Monkeys had to make a saccade toward the red cross in the 1st trial phase, to the green hexagon during the 2nd phase, and to the blue triangle during the 3rd phase irrespective of the objects' locations. The object positions on the screen were changed in each trial phase.

Fig. 2.

Frequency of significant neuronal effects of rank, direction, and their interaction in each area during performance of the serial action task (A) and serial object task (B). Venn diagrams parcel out all possible combinations of effects. Bar histograms give total percentages of neurons exhibiting main effects of rank and direction regardless of what other effects were present. The presence of a main effect of rank indicated that firing varied significantly as a function of rank with the effect of direction factored out, regardless of what other effects were present. Likewise for a main effect of direction.

Fig. 3.

Examples of rank-selective neurons. Data in the “array” panels are aligned on array presentation. Data in the “go” panels are aligned on the go signal for the centrifugal saccade (offset of the central fixation spot). Presupplementary motor area (pre-SMA) neuron selective for 1st rank in the serial action task (A) and serial object task (B). Supplementary eye field (SEF) neuron selective for 2nd rank in the serial action task (C) and serial object task (D). SMA neuron selective for 3rd rank in the serial action task (E) and serial object task (F).

Fig. 4.

Distribution of rank-selective neurons by preferred rank in the serial action task (A) and serial object task (B). Polar plots represent the frequency distribution (radial axis) of neurons according to a continuous measure of preferred rank (theta axis) in which pure categorical rank 1, 2, or 3 selectivity corresponded to 0, 120, and 240° (- - -). Bar histograms represent the frequency distribution of neurons on the basis of which trial phase elicited strongest firing.

Fig. 5.

Mean firing rate as a function of time for SMA, pre-SMA, SEF, and dlPFC neurons classified as selective for the 1st, 2nd, or 3rd rank in the serial action task (A) and serial object task (B). Data in the array panels are aligned on array presentation. Data in the go panels are aligned on the signal for the centrifugal saccade (offset of the central fixation spot).

Fig. 6.

Correlation between indices of rank selectivity measured in the serial action task (horizontal axis) and serial object task (vertical axis) in each area. Each neuron contributed 3 indices for each task: (F2 − F1)/(F2 + F1), (F3 − F1)/(F + F1) and (F3 − F2)/(F3 + F2), where F1, F2 and F3 represent firing rates during trial phases 1- 3. Graphic presentation required breakdown into three indices. Statistical assessment of the correlation (text) did not.

Fig. 7.

A–D: population direction index (mean across neurons of the firing rate difference between the best and the worst direction normalized to the sum) in the serial action task (gray) and serial object task (black). Data are aligned on array presentation. The direction index becomes consistently positive earlier in the serial action task than in the serial object task because the monkey has advance knowledge of the direction of the next required saccade. E: mean ± SE of the direction index during the first 125 ms after each array presentation in the serial action task (white bars) and the serial object task (gray bars).

Fig. 8.

Data from an SEF neuron exhibiting a main effect of rank, a main effect of direction and a rank × direction interaction effect in both the serial action task (A) and the serial object task (B). The interaction between rank and direction reflects the neuron's responding to only two conjunctions of rank and direction (rank 1 + up and rank 2 + up). Main effects alone cannot give rise to such sharp tuning.

Fig. 9.

Frequency of significant neuronal effects of rank, direction and their interaction in each subdivision of PFC during performance of the serial action task (A) and serial object task (B).

Fig. 10.

Data from a dlPFC neuron selective for rank 1 in the serial action task but not in the serial object task.

Fig. 11.

Mean firing rate as a function of time of neurons tending to shift from rank 1 preference in the serial action task (gray line) to rank 3 preference in the serial object task (black line).