Intrinsic timescales across the basal ganglia

Abstract

Recent studies have shown that temporal stability of the neuronal activity over time can be estimated by the structure of the spike-count autocorrelation of neuronal populations. This estimation, called the intrinsic timescale, has been computed for several cortical areas and can be used to propose a cortical hierarchy reflecting a scale of temporal receptive windows between areas. In this study, we performed an autocorrelation analysis on neuronal populations of three basal ganglia (BG) nuclei, including the striatum and the subthalamic nucleus (STN), the input structures of the BG, and the external globus pallidus (GPe). The analysis was performed during the baseline period of a motivational visuomotor task in which monkeys had to apply different amounts of force to receive different amounts of reward. We found that the striatum and the STN have longer intrinsic timescales than the GPe. Moreover, our results allow for the placement of these subcortical structures within the already-defined scale of cortical temporal receptive windows. Estimates of intrinsic timescales are important in adding further constraints in the development of computational models of the complex dynamics among these nuclei and throughout cortico-BG-thalamo-cortical loops.

Intrinsic timescales as an organizational principle of neural processing across the whole rhesus macaque brain

“…Medial prefrontal hierarchy reported by Maisson et al, 2021 (E). Subcortical hierarchy reported by Nougaret et al, 2021 (F). The areas were defined bilaterally for each panel to match the recording sites of the data set—the Cortical Hierarchy Atlas of the Rhesus Macaque ( Jung et al, 2021 ) and Subcortical Atlas of the Rhesus Macaque ( Hartig et al, 2021 ) were used when possible (see Supplementary file 1 ).…”

“…Recently, INTs have been estimated in the medial wall of the PFC, including the ventromedial PFC (vmPFC), subgenual ACC (sgACC), pregenual ACC (pgACC), and dorsal ACC (dACC) ( Maisson et al, 2021 ; Figure 1E , left). Finally, a subcortical INT hierarchy has been described for regions of the basal ganglia: external segment of the globus pallidus (GPe), subthalamic nucleus (STN), and the striatum ( Nougaret et al, 2021 ; Figure 1F , left).…”

“…The stability score was estimated by averaging the correlation coefficients across steps. Abbreviations: Murray et al, 2014 ; Somatosensory hierarchy; Murray et al, 2014 ; Visual hierarchy; Fascianelli et al, 2019 ; Cirillo et al, 2018 ; Cavanagh et al, 2016 ; Maisson et al, 2021 ; Nougaret et al, 2021 . fMRI, functional magnetic resonance imaging.…”

“…Additional studies have replicated and extended the INT hierarchy, reinforcing the idea that brain regions exhibit unique timescales in their intrinsic activity, which reflect functional specialization in terms of temporal integration ( Cavanagh et al, 2016 ; Cirillo et al, 2018 ; Fascianelli et al, 2019 ; Murray et al, 2014 ; Ogawa and Komatsu, 2010 ; Rossi-Pool et al, 2021 ; Maisson et al, 2021 ). The concept of INT hierarchy has even been extended to subcortical regions—specifically the basal ganglia ( Nougaret et al, 2021 ). Moreover, a large-scale network model, based on anatomical connectivity (AC) and the strength of local recurrent connectivity, has been used to successfully reproduce the temporal hierarchy ( Chaudhuri et al, 2015 ).…”

“…Moreover, taking advantage of the whole-brain coverage of fMRI, we are investigating INT topography. This is important since more recent work has shown that there is significant heterogeneity within regions ( Cavanagh et al, 2020 ; Cirillo et al, 2018 ; Nougaret et al, 2021 ), even though initially INTs were assigned to cortical regions as a whole.…”