Predeliberation activity in prefrontal cortex and striatum and the prediction of subsequent value judgment

Abstract

Rational, value-based decision-making mandates selecting the option with highest subjective expected value after appropriate deliberation. We examined activity in the dorsolateral prefrontal cortex (DLPFC) and striatum of monkeys deciding between smaller, immediate rewards and larger, delayed ones. We previously found neurons that modulated their activity in this task according to the animal's choice, while it deliberated (choice neurons). Here we found neurons whose spiking activities were predictive of the spatial location of the selected target (spatial-bias neurons) or the size of the chosen reward (reward-bias neurons) before the onset of the cue presenting the decision-alternatives, and thus before rational deliberation could begin. Their predictive power increased as the values the animals associated with the two decision alternatives became more similar. The ventral striatum (VS) preferentially contained spatial-bias neurons; the caudate nucleus (CD) preferentially contained choice neurons. In contrast, the DLPFC contained significant numbers of all three neuron types, but choice neurons were not preferentially also bias neurons of either kind there, nor were spatial-bias neurons preferentially also choice neurons, and vice versa. We suggest a simple winner-take-all (WTA) circuit model to account for the dissociation of choice and bias neurons. The model reproduced our results and made additional predictions that were borne out empirically. Our data are compatible with the hypothesis that the DLPFC and striatum harbor dissociated neural populations that represent choices and predeliberation biases that are combined after cue onset; the bias neurons have a weaker effect on the ultimate decision than the choice neurons, so their influence is progressively apparent for trials where the values associated with the decision alternatives are increasingly similar.

On Reporting the Onset of the Intention to Move

“…In this vein, we showed that when monkeys were deciding between smaller, more immediate rewards and larger, delayed ones, their choices could be decoded from single-neuron activity in frontal cortex and the basal ganglia before they were even informed of the delays associated with the decision alternatives, and hence before rational deliberation could begin. As expected, and as the circuit model we devised suggested, the bias activity was more predictive as the values of the two alternatives became more similar (Maoz, Kim, Rutishauser, Lee, & Koch, 2010;Maoz et al, 2013). In all the Libet experiments and follow-ups discussed above, the values associated with the random left-or right-hand movements were generally similar, if not identical.…”

The role of the dorsal striatum in choice impulsivity

“…In addition, a later study by Maoz and colleagues demonstrated that the caudate preferentially contained “choice neurons,” a population of cells that tracks the actual choice by changing their activity accordingly (Fig. A) . Importantly, the choice‐related activity in the dorsal striatum exerted a more powerful influence on the behavioral result than the spatial bias–related activity in the ventral striatum.…”

“…(A) Modeling caudate activity for the reward valuation during intertemporal choice based on the biophysical association of neural activity with brain hemodynamic response . Caudate “choice neurons” encode the difference in temporally discounted values of intertemporal choice, which may manifest as the BOLD signal associated with reward valuation . In adults, the BOLD signal associated with immediate choice (immediate‐BOLD) is larger than the BOLD signal associated with delayed choice (delayed‐BOLD) as observed in Refs.…”

The point of no return in vetoing self-initiated movements

“…Similar preparatory signals have been observed using invasive electrophysiology (8, 9) and functional MRI (7, 10), and have been demonstrated also for choices between multiple-response options (6,7,10), for abstract decisions (10), for perceptual choices (11), and for value-based decisions (12). To date, the exact nature and causal role of such early signals in decision making is debated (12)(13)(14)(15)(16)(17)(18)(19)(20).…”