Neural correlates of a postponed decision report

Abstract

Depending on environmental demands, a decision based on a sensory evaluation may be either immediately reported or postponed for later report. If postponed, the decision must be held in memory. But what exactly is stored by the underlying memory circuits, the final decision itself or the sensory information that led to it? Here, we report that, during a postponed decision report period, the activity of medial premotor cortex neurons encodes both the result of the sensory evaluation that corresponds to the monkey's possible choices and past sensory information on which the decision is based. These responses could switch back and forth with remarkable flexibility across the postponed decision report period. Moreover, these responses covaried with the animal's decision report. We propose that maintaining in working memory the original stimulus information on which the decision is based could serve to continuously update the postponed decision report in this task.

Fig. 1.

Discrimination task. (A) Sequence of events during discrimination trials. The mechanical probe is lowered, indenting the glabrous skin of one digit of the restrained hand (PD); the monkey places its free hand on an immovable key (KD); the probe oscillates vertically, at the base stimulus frequency (f1); after a delay, a second mechanical vibration is delivered at the comparison frequency (f2); after another delay between the end of f2 and probe up (PU), the monkey releases the key (KU) and presses either a lateral or a medial push button (PB) to indicate whether the comparison frequency was higher or lower than the base, respectively. (B) Stimulus set used during recordings. Each box indicates a base/comparison frequency stimulus pair. The number inside the box indicates overall percentage of correct trials for that (f1, f2) pair. (C) Top view of the MPc. MPc was subdivided by a line passing from the midline to the posterior edge of the arcuate sulcus (AS); rostral to this line is the presupplementary motor cortex (pre-SMA), and posterior to this line is the SMA proper. (D) Symbols in the insets indicate microelectrode penetrations and the types of the neuronal responses: vibration frequency f1 (green), f2 (red), and sign of the difference f2 − f1 (d, partial differential response; blue), or strictly f2 − f1 (c, full differential response; black). The filled circles indicate 1–8 neurons, the open triangles indicate 9–16 neurons, and the plus signs indicate 17–24 neurons recorded at the shown locations.

Fig. 2.

Responses of four MPc neurons during the postponed decision report. (A) Raster plot of a neuron that responded immediately after f2 for trials f2 > f1. Each row of ticks is a trial, and each tick is an action potential. Trials were delivered in random order (10 trials per stimulus pair). Labels at the left indicate f1:f2 stimulus pairs. (B) Raster plot of a neuron that responded at the end of f2 and continued responding during the entire delay period between f2 and PU for pairs of trials f2 > f1. (C and D) Resulting coefficient values for f1 (a1, green) and f2 (a2, red) for neurons in A and B, as functions of time. During the postponed decision report period, these coefficients had significantly different magnitudes in A (blue trace in C) and statistically equal magnitudes and opposite signs in B (black trace in D). (E) Raster plot of a neuron that encoded f1 during the postponed decision report period. Its firing increased for low f1 frequencies for both f2 > f1 and f2 < f1 pairs. (F) Raster plot of a neuron that encoded f2 during the postponed decision report. Its firing increased for high f2 frequencies for both f2 > f1 and f2 < f1 pairs. (G and H) Values of a1 (green) and a2 (red) coefficients for the neurons in E and F. The filled circles indicate significant values.

Fig. 3.

Dynamics of MPc population responses during the vibrotactile discrimination task. (A) Values of a1 and a2 coefficients for all neurons selected times (200 ms) in B. For each point, at least one coefficient is significantly different from zero. Different plots are for various times in B; n = number of neurons. (B) Number of neurons with significant coefficients as a function of time. The green and red traces correspond to a1 and a2, respectively. The blue trace corresponds to neurons with both significant a1 and a2 coefficients of opposite signs, but significantly different magnitudes; these are partially differential (d) responses. The black trace corresponds to neurons with both significant a1 and a2 coefficients of opposite signs and statistically equal magnitude; these are fully differential (c) or categorical responses encoding f2 − f1. (C) Bar graphs of 50 randomly selected neurons from the 907 neurons that contributed to B. These bars indicate periods of responses encoding f1 (green bars), f2 (red bars), partially differential f2 − f1 (blue bars), and fully differential or categorical responses encoding f2 − f1 (black bars). Each line of bars represents the dynamics of the responses of one single neuron during the discrimination task. The dynamics of these coefficients was analyzed by using a sliding window of 200 ms duration moving in steps of 100 ms. Dynamics of coefficients for the four neurons of Fig. 2 A, B, E, and F are shown at the bottom of C (*). PU, probe up; KU, key up; PB, push button.

Fig. 4.

Correlation between neuronal and behavioral responses. Choice probability indices as a function of time. Green trace, Neurons that encoded information about f1; red trace, neurons that carried information about f2; blue trace, partially differential neurons that carried information about f1 and f2 (d); black trace, fully differential neurons that carried information about f2 − f1 only (c). The orange trace corresponds to neurons that had large choice probability indices and were tested in a control task in which animals received the same stimulus pairs but had to follow a visual cue to produce the motor choice response.