Prefrontal spatial working memory network predicts animal's decision making in a free choice saccade task

Abstract

While neurons in the lateral prefrontal cortex (PFC) encode spatial information during the performance of working memory tasks, they are also known to participate in subjective behavior such as spatial attention and action selection. In the present study, we analyzed the activity of primate PFC neurons during the performance of a free choice memory-guided saccade task in which the monkeys needed to choose a saccade direction by themselves. In trials when the receptive field location was subsequently chosen by the animal, PFC neurons with spatially selective visual response started to show greater activation before cue onset. This result suggests that the fluctuation of firing before cue presentation prematurely biased the representation of a certain spatial location and eventually encouraged the subsequent choice of that location. In addition, modulation of the activity by the animal's choice was observed only in neurons with high sustainability of activation and was also dependent on the spatial configuration of the visual cues. These findings were consistent with known characteristics of PFC neurons in information maintenance in spatial working memory function. These results suggest that precue fluctuation of spatial representation was shared and enhanced through the working memory network in the PFC and could finally influence the animal's free choice of saccade direction. The present study revealed that the PFC plays an important role in decision making in a free choice condition and that the dynamics of decision making are constrained by the network architecture embedded in this cortical area.

Determining Monkey Free Choice Long before the Choice Is Made: The Principal Role of Prefrontal Neurons Involved in Both Decision and Motor Processes

“…Importantly the decision neurons’ activity could not depend on differences in visual responses because all three targets were always presented. Thus, our results indicate that neurons that exhibit a bias in the prestimulus period are not necessarily dissociated from those that are involved in decision formation, as proposed (Maoz et al, 2013 ), and that a neural response bias can emerge, even in the absence of a value-based decision in line with the results of Mochizuki and Funahashi ( 2016 ). In our free-choice condition, decision and motor neurons anticipated the choice long before the stimulus was presented and held it until the onset of movement.…”

“…One possible explanation for the absence of a neural bias in the PF in these experiments (Kim and Shadlen, 1999 ; Roy et al, 2014 ) is that they required a perceptual choice rather than a goal choice as in our task. In a recent study (Mochizuki and Funahashi, 2016 ), it was reported that the prestimulus activity of some neurons in PF was predictive of the future choice of monkeys. However, whether the neurons that exhibited the predictive power were those involved in decision or motor processes was not distinguished.…”

Decoding the neural dynamics of free choice in humans

“…Planning an instructed saccade involves the same effector specific circuits that execute eye movements, namely, the frontal eye fields (FEFs) [2,3] and the lateral intraparietal area (LIP), [4][5][6][7][8], as well as a characteristic sustained neuronal activity in frontal areas, representing information about stimuli maintained in working memory during the delay period [9][10][11]. On the other hand, although monkey studies have demonstrated that free-choice decision processes (e.g., choosing between 2 equal reward options) appear to be represented in an effector specific frontoparietal network [12][13][14][15][16][17][18][19][20][21], the temporal dynamics of the neural correlates of free-choice decisions compared with those underlying instructed planning are poorly understood.…”

Neuromodulation of Prefrontal Cortex in Non-Human Primates by Dopaminergic Receptors during Rule-Guided Flexible Behavior and Cognitive Control

“…It is also necessary to perform D1R manipulations in FEF and DLPFC while testing both for spatial WM performance and attentional selection of response goals. An interesting possibility would be to study dopamine modulation in a task that incorporates both WM and response selection between competing alternatives, like the free-choice saccade task recently explored by Mochizuki and Funahashi ( 2016 ), where PFC activity was found to predict the eventual free choice of a saccadic goal.…”