Unconscious learning and automatic inhibition are accompanied by frontal theta and sensorimotor interactions

Abstract

Cognitive control of behavior is often accompanied by theta-band activity in the frontal cortex, and is crucial for overriding habits and producing desired actions. However, the functional role of theta activity in controlled behavior remains to be determined. Here, we used a behavioral task (Isabella et al., 2019) that covertly manipulated the ability to inhibit (and switch) motor responses using a repeating pattern of stimuli that reduced reaction times (RT) to probable over unexpected stimuli, without participants awareness of the pattern. We combined this task with concurrent measures of brain activity and pupil diameter (as a measure of cognitive activity) of 16 healthy adults during response preparation and inhibition during changes in stimulus probability. Observed RT provided evidence of pattern learning and pupillometry revealed parametric changes in cognitive activity with stimulus probability. Critically, reliable pupillary effects (Hedges g = 1.38) in the absence of RT differences (g = 0.10) indicated that cognitive activity increased without overt changes in behavior (RT). Such increased cognitive activity was accompanied by parametric increases in frontal theta and sensorimotor gamma. In addition, correlation between pre-stimulus beta and pre-response gamma in the motor cortex and post-stimulus frontal theta activity suggest bidirectional interactions between motor and frontal areas. These interactions likely underlie recruitment of preparatory and inhibitory neural activity during rapid motor control. Furthermore, pupillary and frontal theta effects during learned switches demonstrate that increases in inhibitory control of behavior can occur automatically, without conscious awareness.\n\nSignificance StatementGoal-directed control is crucial for overriding habits and producing desired actions, which can fail during errors and accidents, and may be impaired in addiction, attention-deficit disorders, or dementia. This type of control, including response inhibition, is typically accompanied by frontal theta-band activity. We examined the relationship between frontal theta and response inhibition during unconscious pattern learning. First, we found that frontal activity was sensitive to changes in control and correlated with reaction times. Second, insufficient motor preparation predicted greater frontal activity, reflecting a greater need for control, which in turn predicted greater response-related motor activity. These results link the frontal and motor cortices, providing possible mechanisms for controlled behavior while demonstrating that goal-directed control can proceed automatically and unconsciously.