The cost of multiplexing: PFC integrates multiple sources of information in non-orthogonal components accounting for behavioral variability

Abstract

The frontal eye field (FEF) is a prefrontal cortical area classically associated with spatial attention, perception, and oculomotor functions. FEF exhibits complex response properties through mixed selectivity neurons, allowing a high dimensional representation of the information. However, recent studies have shown that FEF encodes information in a low-dimensional regime hence limiting the coding capacity of the neural population. How the FEF encodes multiple sources of information with such limited encoding capacity remains elusive. To address this question, we trained two macaques to perform a visual attention task while we recorded FEF neuronal activity using multi-contact electrodes. FEF neurons encoded task- (spatial location of cue, POS; time in trial, CTOA) and behaviour- (reaction time, RT; focus of attention, TA) related parameters prior to target onset. We found a clear modulation of the RT and TA as a function of the CTOA. Using dPCA, we characterized the functional relationship between neural populations associated with each parameter and investigated how this functional relationship predicts behavior. We found that CTOA variability was associated to two different components the activation of which was correlated with the TA and the RT, respectively. These CTOA related components were non-orthogonal with the RT and TA related components. These results suggest that when different sources of information are implemented during task performance, they show a very precise geometrical configuration in non-orthogonal components. This allows high simultaneous information encoding capacity at the cost of an impaired capacity to use attention information and an enhanced responsiveness toward external stimuli.