Local networks from different parts of the human cerebral cortex generate and share the same population dynamic

Abstract

A major goal of neuroscience is to reveal mechanisms supporting collaborative actions of neurons in local and larger-scale networks. However, no clear overall principle of operation has emerged despite decades-long experimental efforts. Here we used an unbiased method to extract and identify the dynamics of local postsynaptic network states contained in the cortical field potential. Field potentials were recorded by depth electrodes targeting a wide selection of cortical regions during spontaneous activities, and sensory, motor, and cognitive experimental tasks. Despite different architectures and different activities, all local cortical networks generated the same type of dynamic confined to one region only of state space. Surprisingly, within this region state trajectories expanded and contracted continuously during all brain activities and generated a single expansion followed by a contraction in a single trial. This behavior deviates from known attractors and attractor networks. The state-space contractions of particular subsets of brain regions cross-correlated during perceptive, motor and cognitive tasks. Our results imply that the cortex does not need to change its dynamic to shift between different activities, making task-switching inherent in the dynamic of collective cortical operations. Our results provide a mathematically described general explanation of local and larger-scale cortical dynamic.

How far neuroscience is from understanding brains

“…However, when the afferent stimulation ceases, the spiking activity dies out. Mammalian brains, and most likely also insect and zebrafish CNS, have eigen activity as ever-changing ongoing spiking and membrane currents no matter whether they are stimulated or not, awake or at sleep (Rudolph et al, 2007 ; Yap et al, 2017 ; Stringer et al, 2019 ; Davis et al, 2020 ; Marques et al, 2020 ; McCormick et al, 2020 ; Siegle et al, 2021 ; Willumsen et al, 2022 ).…”

“…These results are well known and indicate that 85%−95% of the spikes in a brain are autonomous. A recent large-scale study showed that external stimuli and various experimental conditions could modify fluctuations in the (multidimensional) human cortical field potential, but not perturb the underlying dynamics generating the fluctuations (Willumsen et al, 2022 ).…”

“…For example, in humans and other primates exposed to rhythmic visual or auditory stimuli, each stimulus produces a single time-locked oscillation. These time-locked oscillations can spread, with different lags, to cover the whole cortex (Besle et al, 2011 ; Gomez-Ramirez et al, 2011 ; Spaak et al, 2014 ; Merchant and Averbeck, 2017 ; Willumsen et al, 2022 ). Also, unexpected stimuli may elicit spreading excitation and spiking globally over cortical areas (Ferezou et al, 2007 ; Salkoff et al, 2020 ).…”

“…In vivo studies of different spiking networks in the cerebral cortex but also spinal, hypothalamic, and thalamo-cortical networks show the collective spiking dynamics of the network neurons progress as trajectories along low-dimensional, stable manifolds in state space (Churchland et al, 2010 ; Gallego et al, 2017 ; Lindén et al, 2022 ). On the post-synaptic side, field potential, MEG, and EEG studies show state space dynamics like that of strange (chaotic) higher dimensional attractors (Babloyantz and Destexhe, 1986 ; Stam, 1996 ; Baria et al, 2017 ; Willumsen et al, 2022 ). This dynamic may be identical for all local networks in the human cerebral cortex.…”

“…This dynamic may be identical for all local networks in the human cerebral cortex. However, since the trajectories expand and contract, the dynamic is incompatible with the mathematical definition of attractors (Strogatz, 2018 ; Willumsen et al, 2022 ).…”