Neural excitability and sensory input determine intensity perception with opposing directions in initial cortical responses

Abstract

Perception of sensory information is determined by stimulus features (e.g., intensity) and instantaneous neural states (e.g., excitability). Commonly, it is assumed that both are reflected similarly in evoked brain potentials, that is, higher evoked activity leads to a stronger percept of a stimulus. We tested this assumption in a somatosensory discrimination task in humans, simultaneously assessing (i) single-trial excitatory post-synaptic currents inferred from short-latency somatosensory evoked potentials (SEP), (ii) pre-stimulus alpha oscillations (8-13 Hz), and (iii) peripheral nerve measures. Fluctuations of neural excitability shaped the perceived stimulus intensity already during the very first cortical response (at ∼20 ms) yet demonstrating opposite neural signatures as compared to the effect of presented stimulus intensity. We reconcile this discrepancy via a common framework based on modulations of electro-chemical membrane gradients linking neural states and responses, which calls for reconsidering conventional interpretations of brain potential magnitudes in stimulus intensity encoding.

Cortical response variability is driven by local excitability changes with somatotopic organization

“…Moment-to-moment fluctuations of neural responses to sensory stimuli play a critical role in how we perceive the external world. Commonly, it is assumed that instantaneous neural states influence the stimulus-related brain responses, which in turn shape the perceptual outcome (e.g., Arieli et al, 1996; McCormick et al, 2020; Sadaghiani et al, 2010; Stephani et al, 2021). Specifically, this may be achieved through the modulation of cortical excitability, which is assumed to shift the sensory threshold of stimulus perception (Samaha et al, 2020).…”

“…Specifically, this may be achieved through the modulation of cortical excitability, which is assumed to shift the sensory threshold of stimulus perception (Samaha et al, 2020). Using electroencephalography (EEG) or magneto-encephalography (MEG), this phenomenon can be observed in various sensory modalities in humans, such as the visual (Busch et al, 2009; Iemi et al, 2017), auditory (Henry et al, 2016; Müller et al, 2013), and somatosensory domain (Baumgarten et al, 2016; Craddock et al, 2017; Forschack et al, 2020; Stephani et al, 2021), where instantaneous neural states have typically been quantified by prestimulus oscillatory activity in the alpha frequency range (8-13 Hz), a common marker of the excitability state of a given cortical brain region (Jensen and Mazaheri, 2010; Klimesch et al, 2007; Romei et al, 2008). Noteworthy, in the somatosensory domain, also activity in the beta frequency range (15–30 Hz) may have a similar modulatory effect on sensory processing (Anderson and Ding, 2011; Jones et al, 2010; van Ede et al, 2011).…”

“…Given that both sensory and motor processing reflect activity of broad neural circuitries, understanding neural response variability requires a proper specification of where and when these changes in excitability states take place. In this context, it has been found for the somatosensory domain that fluctuations of cortical excitability emerge already at earliest cortical processing in primary sensory regions (Stephani et al, 2020), with behaviorally relevant effects on stimulus intensity perception (Stephani et al, 2021). However, the spatial organization of these neural dynamics is not understood well yet, leaving open the question of whether instantaneous changes of excitability at earliest cortical processing follow local fluctuations or reflect a global state of the primary somatosensory cortex.…”

Respiration, heartbeat, and conscious tactile perception

“…For the visuospatial perception task by Perl et al (2019), decreased alpha power has been observed in postcentral and parahippocampal gyrus during inspiration compared to expiration. Analogously, lower pre-stimulus alpha power in central brain areas (Mu rhythm) has been associated with higher neural excitability reflected in improved conscious tactile perception (Schubert et al, 2009; Nierhaus et al, 2015; Craddock et al, 2017; Forschack et al, 2020; Stephani et al, 2021).…”

“…In a recent study, the course of alpha power – known to be inversely related to excitability – across the respiratory cycle has been shown to have a minimum around expiration onset (Kluger et al, 2021) – the time period when in our study most stimuli were timed. Also for tactile stimuli, it has been shown that alpha power in central brain areas is related to conscious detection (Schubert et al, 2009; Nierhaus et al, 2015; Craddock et al, 2017; Forschack et al, 2020; Stephani et al, 2021). Taken together, respiration phase locking might be used to increase the likelihood to detect faint stimuli in a phase of highest cortical excitability (attention).…”