Active encoding of decisions about stimulus absence in primate prefrontal cortex neurons

Abstract

Judging the presence or absence of a stimulus is likely the most basic perceptual decision. A fundamental difference of detection tasks in contrast to discrimination tasks is that only the stimulus presence decision can be inferred from sensory evidence, whereas the alternative decision about stimulus absence lacks sensory evidence by definition. Detection decisions have been studied in an intentional, action-based framework, in which decisions were regarded as intentions to pursue particular actions. These studies have found that only stimulus-present decisions are actively encoded by neurons, whereas the decision about the absence of a stimulus does not affect default neuronal responses. We tested whether this processing mechanism also holds for abstract detection decisions that are dissociated from motor preparation. We recorded single-neuron activity from the prefrontal cortex (PFC) of monkeys performing a visual detection task that forced a report-independent decision. We not only found neurons that actively encoded the subjective decision of monkeys about the presence of a stimulus, but also cells responding actively for the decision about the absence of stimuli. These results suggest that abstract detection decisions are processed in a different way compared with the previously reported action-based decisions. In a report-independent framework, neuronal networks seem to generate a second set of neurons actively encoding the absence of sensory stimulation, thus translating decisions into abstract categories. This mechanism may allow the brain to "buffer" a decision in a nonmovement-related framework.

Fig. 1.

Visual detection protocol and behavioral performance. (A) The monkeys initiated each experimental trial by grasping a lever and fixating a central fixation target. After 500 ms, a stimulus was displayed for 100 ms in 50% of the trials (intensity varied in nine levels, centered around the perceptual threshold). In the other 50% of the trials, no stimulus was shown. Both types of trials appeared randomly. After the delay period (2,700 ms), a color cue appeared to indicate the rule of how to respond to a particular decision. If a stimulus was presented, a red square cue required the monkey to release the lever within 1,000 ms to receive a fluid reward, whereas a blue cue demanded the monkey to keep holding the lever for another 1,200 ms. The rule applied in the inverse way if no stimulus was presented. Thus, movement preparation was excluded during the delay period. (B) Signal detection theory classifies an observer's behavioral options (hit, miss, correct rejection, and false alarms) at detection threshold, given two stimulus conditions (stimulus present or absent) and two possible decisions (“yes, stimulus present” and “no, stimulus absent”). (C and D) Psychometric detection curve for monkey H (C) and monkey M (D). Stimulus intensity is represented as % visual contrast; visual contrast of 0 indicates absence of stimulus. [Error bars (SEM) are so small that they are hidden behind the markers].

Fig. 2.

Recording sites and proportion of selective cells. (A) Right shows a top view of a monkey brain. The gray area marks the chamber location. The circular panels on Left show the precise recording sites inside each recording chamber in the lateral PFC for both monkeys. The proportion of decision neurons at individual recording sites is color-coded. iar, inferior arcuate sulcus; ps, principal sulcus; sar, superior arcuate sulcus. (B) Proportions of neurons coding stimulus intensity and decision in both phases.

Fig. 3.

Decision coding by “yes” neurons during the stimulus phase. (A and C) Responses of two example neurons coding the “yes” decision by increasing (A) or decreasing (C) their firing rates during the stimulus phase (analysis window highlighted by the gray shaded area). Top depict dot raster plots; Middle represent the corresponding spike density histograms averaged and smoothed with a Gaussian kernel for illustration. The vertical black lines indicate the presentation of the stimulus (at 500 ms) and the rule cue (at 3,300 ms). Stimulus duration is marked by a small horizontal bar underneath the x axis of each plot. Bottom show the choice probability indices as a function of time. Dotted lines mark significance levels. (B and D) Averaged and normalized responses (SI Materials and Methods) and choice probability indices of decision neurons grouped by response type. Shaded regions indicate SEM; n, number of neurons.

Fig. 4.

Decision coding by “yes” and “no” neurons during the delay phase. (A and C) Raster plots, spike density functions, and choice probability indices for neurons increasing their activity for “yes” decisions (A) or for “no” decisions (C) during the delay phase. (B and D) Normalized averaged responses (SI Materials and Methods) of the corresponding groups. Active “no” decision neurons newly emerged during the delay phase. Same layout as in Fig. 3.

Fig. 5.

Selectivity of decision cells during rule cue presentation. (A and B) Averaged neuronal activity of “yes” (A) and “no” delay phase decision neurons (B) is shown throughout the trial during “yes” and “no” decisions separated according to the rule cue (requiring a particular motor action). The figure has the same layout as in Fig. 3. (C) Proportion of all “yes” and “no” delay phase decision neurons significantly selective for the factors decision, stimulus intensity, motor action, and rule cue during the cue phase. The vertical black line at 3,300 ms depicts the onset of the rule cue. On average, the monkeys performed a motor action 300 ms after the rule cue onset in release trials. The gray area highlights the analysis window of the delay phase. No selectivity for the rule cue or the motor action is present during the delay phase analysis window.