Posterior parietal cortex encodes autonomously selected motor plans

Abstract

The posterior parietal cortex (PPC) of rhesus monkeys has been found to encode the behavioral meaning of categories of sensory stimuli. When animals are instructed with sensory cues to make either eye or hand movements to a target, PPC cells also show specificity depending on which effector (eye or hand) is instructed for the movement. To determine whether this selectivity retrospectively reflects the behavioral meaning of the cue or prospectively encodes the movement plan, we trained monkeys to autonomously choose to acquire a target in the absence of direct instructions specifying which effector to use. Activity in PPC showed strong specificity for effector choice, with cells in the lateral intraparietal area selective for saccades and cells in the parietal reach region selective for reaches. Such differential activity associated with effector choice under identical stimulus conditions provides definitive evidence that the PPC is prospectively involved in action selection and movement preparation.

Figure 1. The behavioral tasks and monkeys' choice sequences

(A) Diagram of interleaved effector delay-instructed saccade (top) and reach (bottom), and effector choice trials (middle). (B) Behavioral choice data from one day's session for each monkey plotting the cumulative number of trials in which the monkeys chose saccades and reaches. Both curves are very close to the diagonal line, indicating monkey selected saccades and reaches with virtually equal probability.

Figure 2. Single-neuron activity during the effector choice task

Neural activity of example LIP (A) and PRR (B) cells during trials in which the monkey chose saccades (red) and reaches (green). Spike trains were aligned to the cue onset. The peri-stimulus time histograms (PSTH) were smoothed using a Gaussian kernel (s.d. = 50 ms) and its thickness represents the standard error (+/-s.e.m) calculated with the bootstrap method.

Figure 3. Comparison of activity between saccade chosen and reach chosen trials for the entire population

Left and right panels are corresponding to LIP and PRR cells, respectively. (A) to (D) represent four consecutive time intervals: cue duration (0-0.6 second after cue onset), early delay (0-0.3 second after cue off), late delay (0.3-0.6 second after cue off) and post-GO (0-0.1 second after GO signal - central fixation off). The p-value in each panel represents statistical significance of differential activity between saccade and reach chosen trials for entire LIP or PRR population, measured by two-tailed Wilcoxon signed rank test. Open circles indicate neurons showing significantly different (p < 0.05, Kruskal-Wallis test) firing rates in saccade and reach chosen trials. Data points on the edge of plots represent normalized firing rates of few cells with activity far beyond the range of the plots (60 sp/s).

Figure 4. Distribution and time course of choice probabilities (CPs)

(A) and (B) show the histograms of CPs calculated based on spiking activity within a 200 ms window centered on the GO signal for 100 LIP and 91 PRR neurons, respectively. The filled bars correspond to cells whose choice probability was significantly different from 0.5 measured by a permutation test. The triangle marker indicates the mean choice probability for each population. (C) The time course of the mean CP (line) and its 95% confidence interval (shadow) calculated by ROC analysis with a 200 ms time window sliding with 20 ms steps.

Figure 5. Time course of population activity

Population histograms averaged across all isolated LIP (A) and PRR (B) neurons during saccade (red) and reach (green) chosen trials. The vertical thin lines indicate cue on, cue off and central fixation off (GO signal), respectively. The horizontal thin line indicates baseline activity, which was defined by mean firing rate during the 300 ms interval beginning from 500 ms before cue onset for both saccade and reach chosen trials. Post-GO activity (0-100 ms interval after GO) of LIP population was significant higher than the baseline (p < 0.005) if the monkeys decided to saccade, but dropped to baseline (p > 0.5) if the monkeys decided to reach. On the other hand, post-GO activity of the PRR population was significantly higher than the baseline (p < 0.0001) in trials in which reaches were chosen, but dropped to baseline (p > 0.8) in trials in which saccades were chosen. Statistical significance was measured by a Kruskal-Wallis non-parametric ANOVA.