Twitches, Blinks, and Fidgets: Important Generators of Ongoing Neural Activity

Abstract

Animals and humans continuously engage in small, spontaneous motor actions, such as blinking, whisking, and postural adjustments (“fidgeting”). These movements are accompanied by changes in neural activity in sensory and motor regions of the brain. The frequency of these motions varies in time, is affected by sensory stimuli, arousal levels, and pathology. These fidgeting behaviors can be entrained by sensory stimuli. Fidgeting behaviors will cause distributed, bilateral functional activation in the 0.01 to 0.1 Hz frequency range that will show up in functional magnetic resonance imaging and wide-field calcium neuroimaging studies, and will contribute to the observed functional connectivity among brain regions. However, despite the large potential of these behaviors to drive brain-wide activity, these fidget-like behaviors are rarely monitored. We argue that studies of spontaneous and evoked brain dynamics in awake animals and humans should closely monitor these fidgeting behaviors. Differences in these fidgeting behaviors due to arousal or pathology will “contaminate” ongoing neural activity, and lead to apparent differences in functional connectivity. Monitoring and accounting for the brain-wide activations by these behaviors is essential during experiments to differentiate fidget-driven activity from internally driven neural dynamics.

Movement and Performance Explain Widespread Cortical Activity in a Visual Detection Task

“…These modulatory transmitter pathways can have both rapid (10 s of msec) and slow (seconds) effects on activity in cortical and thalamocortical networks (Muñoz and Rudy 2014;Zagha and McCormick 2014). For example, the activation of nicotinic receptors by acetylcholine may rapidly activate layer 1 VIP-containing interneurons, resulting in the inhibition of somatostatin containing inhibitory cells and the disinhibition of pyramidal neurons (Lee et al 2013;Pi et al 2013;Hangya et al 2014;Zhang et al 2014), thereby participating in the rapid changes associated with microarousals, or short duration movements (McGinley et al 2015b;Drew et al 2018). Through the activation of metabotropic receptors, noradrenergic and cholinergic systems can also have broad effects on the patterns of cortical and thalamocortical networks by altering neuronal excitability (e.g., depolarization) and neuronal firing pattern, among other effects (McCormick 1992; Lee and Dan 2012; Zagha and McCormick 2014).…”

“…Mice frequently engage in spontaneous behaviors (e.g., movements, changes in arousal) that alter brain dynamics and sensory evoked activity (McGinley et al 2015b;Drew et al 2018;Musall et al 2019;Stringer et al 2019). Furthermore, the poststimulus behavioral response of rodents is difficult to control, and responses are sometimes much more complicated than necessary for reward (Kawai et al 2015).…”

Movement and performance predict widespread cortical activity in a visual detection task

“…For example, the activation of nicotinic receptors by acetylcholine may rapidly activate layer 1 VIP-containing interneurons, resulting in the inhibition of somatostatin containing inhibitory cells and the disinhibition of pyramidal neurons (Pi et al 2013;S. Lee et al 2013;Hangya et al 2014), thereby participating in the rapid changes associated with microarousals, or short duration movements Drew, Winder, and Zhang 2018). Through the activation of metabotropic receptors, noradrenergic and cholinergic systems can also have broad effects on the patterns of cortical and thalamocortical networks by altering neuronal excitability (e.g.…”

“…Mice frequently engage in spontaneous behaviors (e.g. movements, changes in arousal) that alter brain dynamics and sensory evoked activity Stringer et al 2019;Musall et al 2019;Drew, Winder, and Zhang 2018). Furthermore, the post-stimulus behavioral response of rodents is difficult to control, and responses are sometimes much more complicated than necessary for reward .…”

An oligarchy of NO-producing interneurons controls basal and evoked blood flow in the cortex

“…We measured arteriole diameter dynamics driven by locomotion, as behavior is the primary driver of hemodynamic signals in the awake brain ( Fig. 1D) 7,27 , and because sensory stimulation in awake animals invariably elicits movement 31,32 . During bouts of voluntary locomotion, neural activity increased substantially in the forelimb/hindlimb (FL/HL) representation in somatosensory cortex, as measured by changes in firing rate or power in the gamma-band of the LFP (Fig.…”