Maintained avalanche dynamics during task-induced changes of neuronal activity in nonhuman primates

Abstract

Sensory events, cognitive processing and motor actions correlate with transient changes in neuronal activity. In cortex, these transients form widespread spatiotemporal patterns with largely unknown statistical regularities. Here, we show that activity associated with behavioral events carry the signature of scale-invariant spatiotemporal clusters, neuronal avalanches. Using high-density microelectrode arrays in nonhuman primates, we recorded extracellular unit activity and the local field potential (LFP) in premotor and prefrontal cortex during motor and cognitive tasks. Unit activity and negative LFP deflections (nLFP) consistently changed in rate at single electrodes during tasks. Accordingly, nLFP clusters on the array deviated from scale-invariance compared to ongoing activity. Scale-invariance was recovered using 'adaptive binning', that is identifying clusters at temporal resolution given by task-induced changes in nLFP rate. Measures of LFP synchronization confirmed and computer simulations detailed our findings. We suggest optimization principles identified for avalanches during ongoing activity to apply to cortical information processing during behavior.

Neuronal avalanches in input and associative layers of auditory cortex

“…Our findings of robust power laws even under nonstationary conditions, i.e. evoked responses, are in line with previous reports in nonhuman primates based on the local field potential (Yu et al, 2017). We conclude that 2photon imaging of cortical layers at cellular resolution in combination with robust spike density estimates allows for the clear identification of scale-invariant activity in ongoing and evoked population activity in primary auditory cortex.…”

The scale-invariant, temporal profile of neuronal avalanches in relation to cortical γ–oscillations

“…The scale-invariant nature of neuronal avalanches describes the firing of nerve cells 8,9 and, at larger scales, captures neuronal population dynamics in zebrafish 10 , nonhuman primates 7,11,12 , and humans [13][14][15][16][17][18] . This supports the idea that the brain might operate close to a critical state [19][20][21][22] where numerous aspects of information processing are optimized [23][24][25][26][27][28][29][30] .…”

Temporal signatures of criticality in human cortical excitability as probed by early somatosensory responses

“…In neuronal systems, criticality seems to be a general organization principle reflecting a dynamic equilibrium between coordinated (ordered) and uncoordinated (disordered) neuronal activity: Power-law dynamics indicating proximity to the critical state have been found in the size and duration of neuronal avalanches in rat brain slices (Beggs & Plenz, 2003;Friedman et al, 2012), monkeys (Petermann et al, 2009;Priesemann, Munk, & Wibral, 2009;Yu et al, 2017), cats (Hahn et al, 2010), zebrafish larvae (Ponce-Alvarez, Jouary, Privat, Deco, & Sumbre, 2018), as well as humans (Arviv, Goldstein, & Shriki, 2015;Priesemann, Valderrama, Wibral, & van Quyen, 2013;Shriki et al, 2013). Furthermore, when focusing on the temporal domain, power-law dynamics can be found in human resting-state fMRI networks (Tagliazucchi et al, 2013), as well as in amplitude fluctuations of alpha band activity in the MEG (Linkenkaer-Hansen, Nikouline, Palva, & Ilmoniemi, 2001;Palva et al, 2013).…”