Coherent neuronal ensembles are rapidly recruited when making a look-reach decision

Abstract

Summary Selecting and planning actions recruits neurons across many areas of the brain but how ensembles of neurons work together to make decisions is unknown. Temporally-coherent neural activity may provide a mechanism by which neurons coordinate their activity in order to make decisions. If so, neurons that are part of coherent ensembles may predict movement choices before other ensembles of neurons. We recorded neuronal activity in the lateral and medial banks of the intraparietal sulcus (IPS) of the posterior parietal cortex, while monkeys made choices about where to look and reach and decoded the activity to predict the choices. Ensembles of neurons that displayed coherent patterns of spiking activity extending across the IPS, “dual coherent” ensembles, predicted movement choices substantially earlier than other neuronal ensembles. We propose that dual-coherent spike timing reflects interactions between groups of neurons that play an important role in how we make decisions.

Temporal coding of reward-guided choice in the posterior parietal cortex

“…Although the gamma activity may be most informative when spiking is greatest, the integration period for the beta activity may extend past the time of greatest synchronous activity to include a later period of peak information. In this way, the computations in the PPC may be functionally linked to the distributed ensembles underlying the formation of decisions (9,13). In summary, we propose that the relative timing of local spiking and choice information reveals a temporal reference for computations across local and large-scale decision networks.…”

“…84 units for monkey C and 43 units for monkey R) showed significant SFC with the nearby LFP during the baseline epoch (the 500 ms preceding the target onset), and 119 units (79%; 78 units for monkey C and 41 units for monkey R) showed significant SFC during the choice epoch (200-700 ms after target onset). We found prominent SFC with a peak in the beta-frequency range (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) [permutation tests, familywise error probability (P FWER ) < 0.05] (Fig. 2 A and B).…”

“…We hypothesize that the encoding of decisions in the PPC should depend on the temporal structure present in neuronal activity. Previous studies have shown that coherently active ensembles of cells in the PPC predict reaction times (9) and movement choices (13,21) better than neurons without coherent dynamics. However, whether and how the coding of decisions depends on the temporally structured firing of PPC neurons remains unknown.…”

“…Decisions are made within a network that extends across many regions of the brain (20)(21)(22)(23)(24)(25), so efficient and flexible mechanisms are required to enable distributed computations. Dynamic and frequency-specific correlations in activity between brain areas are ubiquitous and offer potential physiological mechanisms supporting distributed computations in decision networks (13,21,(26)(27)(28)(29)(30)(31)(32)(33)(34). We hypothesize that the encoding of decisions in the PPC should depend on the temporal structure present in neuronal activity.…”

“…Firing rates of neurons in the PPC encode movement intention and the temporal evolution of movement choices (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13) as well as decision variables such as expected rewards, the subjective desirability during reward-guided decisions (14)(15)(16)(17)(18), and the certainty in perceptual decisions (19). Decisions are made within a network that extends across many regions of the brain (20)(21)(22)(23)(24)(25), so efficient and flexible mechanisms are required to enable distributed computations.…”