Dynamics of Cortical Neuronal Ensembles Transit from Decision Making to Storage for Later Report

Abstract

Decisions based on sensory evaluation during single trials may depend on the collective activity of neurons distributed across brain circuits. Previous studies have deepened our understanding of how the activity of individual neurons relates to the formation of a decision and its storage for later report. However, little is known about how decision-making and decision maintenance processes evolve in single trials. We addressed this problem by studying the activity of simultaneously recorded neurons from different somatosensory and frontal lobe cortices of monkeys performing a vibrotactile discrimination task. We used the hidden Markov model to describe the spatiotemporal pattern of activity in single trials as a sequence of firing rate states. We show that the animal's decision was reliably maintained in frontal lobe activity through a selective state sequence, initiated by an abrupt state transition, during which many neurons changed their activity in a concomitant way, and for which both latency and variability depended on task difficulty. Indeed, transitions were more delayed and more variable for difficult trials compared with easy trials. In contrast, state sequences in somatosensory cortices were weakly decision related, had less variable transitions, and were not affected by the difficulty of the task. In summary, our results suggest that the decision process and its subsequent maintenance are dynamically linked by a cascade of transient events in frontal lobe cortices.

Error-Robust Modes of the Retinal Population Code

“…Dimensionality reduction methods applicable to single-trial spiking data, the paradigm adopted in our work, include continuous state-space models in addition to HMMs. Hidden Markov models have been employed to capture population spiking in a variety of cortical structures, including frontal [90–92], premotor [93], gustatory [94], and somatosensory areas [91]. A similar latent-variable-based approach, restricted Boltzmann machines, were applied to visual cortex in [95].…”

Dimensionality reduction for large-scale neural recordings

“…By recording the response of a single neuron, it is usually difficult to identify the moment-by-moment fluctuations of these types of internal cognitive processes. However, if multiple neurons are recorded simultaneously, one can leverage statistical power across neurons to extract a succinct summary of the population activity on individual experimental trials 12,22–24 .…”

Itinerancy between attractor states in neural systems

“…Evidence for a delayed rapid transition from one discrete attractor state to another during decision making has been accrued during taste processing (where the decision is to expel or ingest a tastant) [28,30], in a somatosensory task [80], and in a detection of motion direction task [32]. However, an alternative analysis of the latter task revealed ramping as the typical dynamics during stimulus acquisition, with rapid transitions corresponding only to changes of mind [81].…”