Misinterpreting Electrophysiology in Human Cognitive Neuroscience

An axiomatic view in contemporary neuroscience is that EEG components such as event-related brain potentials (ERPs) and oscillations are directly interpretable as manifestations of biological processes that support sensory, motor, and cognitive constructs of interest. This premise justifies and propels research programs in laboratories worldwide, but with a substantial social and economic cost, warranted by the potential for basic-science discovery and the resulting bench-to-bedside transfer for health and disease. But a different premise would be more fruitful. This article proposes that, in psychophysiological experiments relying on vision, EEG components (e.g., P1-N170, LPP, and alpha oscillations) relate to cognition indirectly through their more direct relationship with oculomotor action. The common experimental design that includes a baseline ocular fixation period preceding stimulus presentation provides an excellent template with which to develop the present proposal. Electrophysiological and eye-tracking evidence (3 published and 4 new data sets: 7 experiments, N_total = 421, in the context of face and affective picture viewing, reading, listening, rest, microsleep and eye movements under closed eye lids), together with simulations grounded in empirically observed oculomotor dynamics, demonstrate how and why common conclusions, and reliance on them in clinical practice/treatment efficacy and drug development studies, are at best premature. Results indicate that the oculomotor system plays a mediating role between such EEG phenomena and cognition. Present evidence supports a complementary view of how EEG can shape the development of a broader thought horizon in psychophysiological theory and practice.