Emergence of Non-Linear Mixed Selectivity in Prefrontal Cortex after Training

Abstract

Neurons in the PFC are typically activated by different cognitive tasks, and also by different stimuli and abstract variables within these tasks. A single neuron's selectivity for a given stimulus dimension often changes depending on its context, a phenomenon known as nonlinear mixed selectivity (NMS). It has previously been hypothesized that NMS emerges as a result of training to perform tasks in different contexts. We tested this hypothesis directly by examining the neuronal responses of different PFC areas before and after male monkeys were trained to perform different working memory tasks involving visual stimulus locations and/or shapes. We found that training induces a modest increase in the proportion of PFC neurons with NMS exclusively for spatial working memory, but not for shape working memory tasks, with area 9/46 undergoing the most significant increase in NMS cell proportion. We also found that increased working memory task complexity, in the form of simultaneously storing location and shape combinations, does not increase the degree of NMS for stimulus shape with other task variables. Lastly, in contrast to the previous studies, we did not find evidence that NMS is predictive of task performance. Our results thus provide critical insights on the representation of stimuli and task information in neuronal populations, in working memory.

More Prominent Nonlinear Mixed Selectivity in the Dorsolateral Prefrontal than Posterior Parietal Cortex

“…Our results are consistent with another recent study from our laboratory which documented emergence of NMS in the PFC after training to perform working memory tasks for the first time, in a different cohort of animals ( Dang et al, 2021 ). In both of these studies, the percentage of neurons that exhibited NMS was modest, and nearly absent in some task variants ( Dang et al, 2021 ). Furthermore, lower NMS was not predictive of error trials, as would be expected by the suggested role of NMS in regulating flexible behavior ( Rigotti et al, 2013 ).…”

“…However, even prefrontal NMS was present in only a small percentage of neurons, did not result in a substantial rotation of the population responses in PCA space, and lower magnitude on a trial-to-trial basis was not predictive of errors in task execution. These findings suggest that the role of NMS is somewhat limited and that this is not the only mechanism through which complex tasks are represented in neural activity, in agreement with other recent studies ( Dang et al, 2021 ).…”

“…To classify neurons of the MSNG task into different categories of selectivity, we performed ANOVA tests to investigate how neurons encode various combinations of different task variables. We first performed a two-way ANOVA to determine the influence of task epoch (first vs second stimulus presentation epoch) on the neuron’s spatial turning ( Dang et al, 2021 ). The two ANOVA factors were the visual stimulus location and the task epoch (cue or match period) in which the stimulus appeared.…”

“…Individual neurons in the PFC typically encode multiple stimulus dimensions and task rules during performance of a task ( Asaad et al, 2000 ; Mansouri et al, 2006 ; Machens et al, 2010 ; Warden and Miller, 2010 ; Qi et al, 2015 ). A proportion of prefrontal neurons indeed exhibit NMS for these variables ( Rigotti et al, 2013 ; Parthasarathy et al, 2017 ; Johnston et al, 2020 ; Dang et al, 2021 ). These findings however have not been universal.…”

“…These findings however have not been universal. Some studies have failed to detect appreciable numbers of neurons with NMS ( Cavanagh et al, 2018 ; Dang et al, 2021 ). It is an open question therefore whether NMS is essential to perform any complex task.…”