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.
Significance Statement A fundamental belief among neuroscientists across diverse fields is that a larger brain response to a sensory stimulus corresponds to a stronger sensation of that stimulus. In the current study, however, we present evidence that this conventional view needs to be revised. Untangling the distinct neural correlates of sensory input and instantaneous brain states in human somatosensory perception, we show and explain why high-excitability states may result in smaller magnitudes of the first cortical EEG potential leading to increases in the perceived stimulus intensity. This seemingly counter-intuitive observation allows novel insights into the underlying mechanisms of neural variability: Cortical excitability is manifested in modulations of post-synaptic membrane potentials, jointly linking pre-stimulus oscillatory state, stimulus-related brain responses, and the behavioral outcome.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
↵¶ Now at Department of Psychology, University of Potsdam, Potsdam, Germany, 14476
title updated; further control analyses added; figures revised (tried to improve visual appearance).