Neural correlates of a decision variable before learning to perform a match/non-match task

Abstract

The lateral prefrontal cortex plays an important role in working memory and decision-making, although little is known about how neural correlates of these functions are shaped by learning. To understand the effect of learning on the neuronal representation of decision-making, we recorded single neurons from the lateral prefrontal cortex of monkeys before and after they were trained to judge whether two stimuli appeared at matching spatial locations. After training, and in agreement with previous studies, a population of neurons exhibited activity that was modulated depending on whether the second stimulus constituted a match or not, which had predictive ability for the monkey's choice. However, even before training, prefrontal neurons displayed modulation depending on the match or non-match status of a stimulus, with approximately equal percentages of neurons preferring a match or a non-match. The difference in firing rate and discriminability for match and non-match stimuli before training was of comparable magnitude as that after training. Changes observed after training involved an increase in the percentage of neurons exhibiting this effect, a greater proportion of neurons preferring non-match stimuli, and a greater percentage of neurons representing information about the first stimulus during the presentation of the second stimulus. Our results suggest that the neuronal activity representing some match/non-match judgments is present in the lateral prefrontal cortex even when subjects are not required to perform a comparison and before any training.

Figure 1.

Schematic illustration of the task. A, Successive frames illustrate the sequence of stimulus presentations. Two stimuli were presented in sequence (S1 and S2), at either the same or diametric locations, followed by delay periods. After training, the second delay period was followed by two choice targets, and the monkeys were required to saccade to a green target if the two stimuli appeared at matching locations and to a blue target if they did not. In the pretraining stage, the animals were rewarded for maintaining fixation after the end of the second delay period. B, Stimulus set used for the analysis presented here.

Figure 2.

Example neurons with preference for a match or non-match stimulus. A, Rasters and PSTH representing responses of one lateral prefrontal neuron to a S2 stimulus (match) in the receptive field (yellow arc in the inset above the PSTH), preceded by a cue at the same location. Gray bars indicate times of stimulus presentations. B, Responses of the same neuron to the same S2 stimulus as a non-match. C, Firing rates of the same neuron for match and non-match responses appearing at each location fitted to a Gaussian curve. D–F, Responses of a second neuron with preference for non-match stimuli. G–I, Responses of a third neuron with different preference for spatial location depending on match/non-match status.

Figure 3.

Example neuron with preference for a match stimulus, A, over a non-match stimululs, B, recorded before training. C, Gaussian fit. Conventions are the same as in Figure 2.

Figure 4.

Magnitude of match/non-match preference before and after training. A, Population PSTH recorded before training, of neurons with significant preference for non-match over match stimuli. Blue line represents the match (non-preferred condition), and red the non-match (preferred), always presented at the best location in the receptive field. Gray bars represent times of stimulus presentation. B, Population PSTH of neurons with significant preference of non-match over match stimuli. Now the blue line representing the match is the preferred condition and red the non-preferred. C, D, Equivalent populations of neurons recorded after training in the task. Insets to the right of the figure are schematic; the location of the receptive field differed between neurons, and data were averaged from the best location of each neuron. C, Cue; M, match; NM, non-match.

Figure 5.

ROC analysis. A, Average ROC values comparing the distribution of responses to match and non-match stimuli presented for neurons with preference of non-match over match responses, recorded before (blue line) and after (red line) training. B, Average ROC values for neurons with preference of match over non-match stimuli.

Figure 6.

Correct and error trials. Average absolute difference in firing rate between match and non-match responses, for neurons with a significant difference between the two stimuli (shaded area in Fig. 3). A, Average from correct trials. B, Average from error trials. The same population of neurons with sufficient number of error trials (n = 20) is compared in both panels. C, Average ROC values are compared from correct and error trials.

Figure 7.

Regression analysis. A, Responses recorded during the cue period, before training. Each dot represents the s₁ and s₂ regression coefficients of a single neuron. Blue dots represent neurons with significant s₁ coefficients (i.e., significantly modulated by the location of the cue); green dots represent neurons with no significant s₁ coefficients. B, Responses recorded during the second stimulus presentation period. In addition to blue and green dots, purple dots represent neurons with significant s₂ coefficients (i.e., significantly modulated by the location of the second stimulus). Orange dots represent neurons with both significant s₁ and s₂ coefficients. C, D, Equivalent responses of neurons recorded after training. Up to three outliers appeared beyond the axis range in each panel. M, Match; NM, non-match.