Neural Intrinsic Timescales in the Macaque Dorsal Premotor Cortex Predict the Strength of Spatial Response Coding

Abstract

SummaryOur brain continuously receives information over multiple timescales that are differently processed across areas. In this study, we investigated the intrinsic timescale of neurons in the dorsal premotor cortex (PMd) of two rhesus macaques while performing a non-match-to-goal task. The task rule was to reject the previously chosen target and select the alternative one. We defined the intrinsic timescale as the decay constant of the autocorrelation structure computed during a baseline period of the task. We found that neurons with longer intrinsic timescale tended to maintain a stronger spatial response coding during a delay period. This result suggests that longer intrinsic timescales predict the functional role of PMd neurons in a cognitive task. Our estimate of the intrinsic timescale integrates an existing hierarchical model (Murray et al., 2014), by assigning to PMd a lower position than prefrontal cortex in the hierarchical ordering of the brain areas based on neurons' timescales.

A Diversity of Intrinsic Timescales Underlie Neural Computations

“…Importantly, this analysis highlighted a striking degree of within-region variability ( Figure 2 )—even within the anterior cingulate cortex (ACC), which sat at the apex of the hierarchy identified in Murray et al ( 2014 ); there was a spectrum of timescales including many neurons with short timescales. Further studies then applied the same single-neuron analysis to many different brain regions throughout the cortical hierarchy ( Figure 3 ), including posterior parietal cortex (Wasmuht et al, 2018 ), lateral prefrontal cortex (lPFC; Cavanagh et al, 2016 , 2018 ; Wasmuht et al, 2018 ; Fascianelli et al, 2019 ; Fontanier et al, 2020 ; Kim and Sejnowski, 2020 ), orbitofrontal cortex (OFC; Cavanagh et al, 2016 , 2018 ; Fascianelli et al, 2019 ), cingulate cortex (Cavanagh et al, 2016 , 2018 ; Fontanier et al, 2020 ), premotor cortex (Cirillo et al, 2018 ), and frontopolar cortex (Fascianelli et al, 2019 ). All of these regions contained single neurons with a diversity of timescales, suggesting that brain regions possessing a heterogonous distribution of timescales is a generalized feature of cortical organization.…”

“…(D) Histogram of single-neuron timescales for dorsal premotor cortex (PMd), recorded during a rule-based working memory task. Adapted from Cirillo et al ( 2018 ), where originally published with a CCBY4 licence.…”

“…Whereas decision-making requires the gradual integration of evidence across time (Gold and Shadlen, 2007 ), working memory involves the maintenance of task-relevant information in the absence of direct sensory input (Goldman-Rakic, 1995 ). A number of studies demonstrated that neuronal timescales predicted the strength of mnemonic encoding on a variety of different working-memory paradigms, with longer timescale neurons again playing a greater role in the maintenance of mnemonic information (Nishida et al, 2014 ; Cavanagh et al, 2018 ; Cirillo et al, 2018 ; Wasmuht et al, 2018 ; Fascianelli et al, 2019 ; Fontanier et al, 2020 ; Kim and Sejnowski, 2020 ; Figure 4B ). This effect was present in multiple brain regions [lPFC, cingulate cortex, frontal eye field (FEF), premotor cortex], and for multiple different modalities of mnemonic information (spatial location/response direction, expected reward size, stimulus color).…”

Multiple timescales of neural dynamics and integration of task-relevant signals across cortex

“…A few recent studies have shown that intrinsic timescales during the fixation period-presumably before strong task-relevant signals emerge in the cortical activity --can predict encoding of task-relevant signals later in the trial for some but not all cortical areas. This includes the encoding of chosen value during value-guided decision making (Cavanagh et al, 2016), persistent activity during working-memory tasks (Nishida et al, 2014;Cavanagh et al, 2018;Wasmuht et al, 2018), and activity related to upcoming behavioral responses during a visually-cued strategy task (Fascianelli et al, 2019;Cirillo et al, 2018). However, in all these studies, the decay rate of autocorrelation in the firing response of individual neurons during one epoch of the task (fixation period) is compared with encoding of task-relevant signals in other epochs of the task.…”

Brief localised monocular deprivation in adults alters binocular rivalry predominance retinotopically and reduces spatial inhibition

“…In either scenario, a brief deprivation duration would still tap on shared mechanisms, though it is noteworthy that the degree of similarity is dependent on other determinants such as the type of visual property examined, assessment task, and stimulus content. This is because experience-dependent plasticity in binocular vision involves a multitude of possible processes 61 and variations in these determinants may tap different neural correlates that perform differently at different time scales 62 , 63 .…”