Distinct neural states encode task identity in frontal eye field and interact with its core spatial properties

Abstract

The prefrontal cortex (PFC) plays a key role in selecting, maintaining and representing sensory information, and in its integration with our current internal goals and expectations, implementing such cognitive processes as executive functions, attention, decision making and working memory. Performing computation over all of these functional cognitive processes and dynamically shifting from one to the other based on task demands requires a complex functional organization and a high degree of coding flexibility. The PFC cells show a non-linear mixed selectivity characterized by specific tuning for multiple task- and behaviour related parameters. This non-linear mixed selectivity thought to allow for a high-dimensional representation of information. Here, we asked if the PFC is mainly involved in specific task-parameters representation, or if it additionally holds a higher order representation for task-identity. We thus trained two macaques to perform three different tasks: a memory guided saccade task and two detection tasks involving different attention mechanisms. Multi-unit activity was recorded in the frontal eye field, bilaterally, while monkeys performed these three tasks in a same session. Using demixed Principal Component Analysis, we found a two-dimensional neural state that characterized each of these tasks. The lower dimensional representation of the activity recorded during the performance of the two attentional tasks were more similar to each other than to the memory-guided saccade task. Furthermore, we report that task and spatial information are non-linearly mixed, a signature of a high-dimensional neural representation. Overall, this indicates that PFC encodes task identity information and flexibly adjusts its sensory processes as a function of the specific ongoing task. Significance StatementOne long lasting question in cognitive neuroscience is whether PFC mainly represents the different parameters that are needed to perform any given task, or if it additionally holds a higher order representation for task-identity. We recorded from the macaque frontal eye fields while monkeys performed a memory guided saccade task and two detection tasks involving different attention mechanisms. We found a task-identity neural state in which the two attentional tasks were represented similarly to each other but differently from the memory-guided saccade task. We also report that task and spatial information are non-linearly mixed, a signature of a high-dimensional neuronal representation. Overall, this indicates that PFC encodes task identity information and flexibly adjusts its sensory processes as a function of the specific ongoing task.