Free choice activates a decision circuit between frontal and parietal cortex

Abstract

We often face alternatives that we are free to choose between. Planning movements to select an alternative involves several areas in frontal and parietal cortex that are anatomically connected into long-range circuits. These areas must coordinate their activity to select a common movement goal, but how neural circuits make decisions remains poorly understood. Here we simultaneously record from the dorsal premotor area (PMd) in frontal cortex and the parietal reach region (PRR) in parietal cortex to investigate neural circuit mechanisms for decision making. We find that correlations in spike and local field potential (LFP) activity between these areas are greater when monkeys are freely making choices than when they are following instructions. We propose that a decision circuit featuring a sub-population of cells in frontal and parietal cortex may exchange information to coordinate activity between these areas. Cells participating in this decision circuit may influence movement choices by providing a common bias to the selection of movement goals.

Figure 1. Task and behaviour

a Free search task. Three circular targets presented at eight potential locations spaced 10° apart around the central hand position, H. b, Instructed search task. Targets in the instructed search task were a circle, square and triangle; the monkey had to reach to them in that order. Each target had an equal, one-third, probability of being the rewarded target. c, The most frequent movement sequences made in response to an example configuration during the free search task. The same configuration elicits three different sequences. d, Instructed search configurations elicit the same sequence. Probability is shown above each arrow.

Figure 2. PMd–PRR spike–field coherence

a, b, Example PMd spike–PRR field coherence: a, Time–frequency coherence every 50 ms during free and instructed search. Amplitude is colour coded. Activity is aligned to search array onset (first vertical white bar). Average time of the first reach (second vertical white bar). White horizontal bar shows analysis window for b. b, Coherence line plot for free (black) and instructed (red) search tasks. Coherence is z-transformed. Significant difference at 15 Hz (**P < 0.05; t-test). c, d, Example PRR spike–PMd field coherence. e, Population average 15 Hz PMd–PRR spike–field coherence every 10 ms. PMd spike–PRR field coherence (solid); PRR spike–PMd field coherence (dashed). Free search (black); instructed search (red). Coherence is z-transformed before averaging; 95% confidence intervals, Bonferroni-corrected (shaded).

Figure 3. Spike response latencies

a, Example PMd neuron response to free search (black) and instructed search (red). Activity is aligned to search array onset. Movement to the cell’s preferred direction. b, Example PRR neuron. c, Population average PMd spike response for cells. Activity is baseline subtracted; s.e.m. (shaded). d, Population average PRR spike response. e, Population average PRR and PMd spike responses during centre-out task to the preferred direction. f, Population response latencies for PMd and PRR during free search, instructed search and the centre-out task. Error bars, 95% confidence intervals.

Figure 4. Receiver-operating characteristic choice probability estimated from the firing rate for neurons with and without significant PMd–PRR spike–field coherence

a, Population average choice probability for correlated (solid) and uncorrelated (dashed) PMd neurons; 95% confidence intervals (shaded). b, Same for PRR neurons.