Oculomotor freezing tracks perception and is immune to decision bias

The appearance of a salient stimulus rapidly inhibits saccadic eye movements. Curiously, this "oculomotor freezing" reflex is triggered only by stimuli that the participant reports seeing (White & Rolfs, 2016). But is oculomotor freezing linked to the participant's sensory experience, or their decision that a stimulus was present? If it were decision-related, oculomotor freezing should become less prevalent when the participant is induced to have a conservative decision criterion and reports seeing a stimulus less often. Here we manipulated decision criterion in two ways: by adjusting monetary payoffs and stimulus probability in a detection task. These bias manipulations greatly affected participants' explicit reports but did not affect the degree to which microsaccades were inhibited by stimulus presence. In addition, the link between oculomotor freezing and explicit reports was stronger when the decision criterion was conservative rather than liberal. The simplest explanation is that conservative reports of stimulus presence are more often based on a strong sensory signal that also inhibits microsaccades. We conclude that the sensory threshold for oculomotor freezing is independent of decision bias. To the extent that conscious experience is also unaffected by such bias, oculomotor freezing provides an involuntary, implicit indication that a stimulus has entered awareness.

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

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 (Hedge’s 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.Significance 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.

Multifaceted adaptation of the neural decision process with prior knowledge of time constraints and stimulus probability

When selecting actions in response to noisy sensory stimuli, the brain can exploit prior knowledge of time constraints, stimulus discriminability and stimulus probability to hone the decision process. Although behavioral models typically explain such effects through adjustments to decision criteria only, the full range of underlying neural process adjustments remains to be established. Here, we draw on human neurophysiological signals reflecting decision formation to construct and constrain a multi-tiered model of prior-informed motion discrimination, in which a motor-independent representation of cumulative evidence feeds build-to-threshold motor signals that receive additional dynamic urgency and bias signal components. The neurally-informed model not only provides a superior quantitative fit to prior-biased behavior across three distinct task regimes (easy, time-pressured and weak evidence), but also reveals adjustments to evidence accumulation rate, urgency rate, and the timing of accumulation onset and motor execution which go undetected or are discrepant in more standard diffusion-model analysis of behavior.

Brain Signals Related to Change Detection

This chapter discusses, in the context of the predictive-coding framework, evoked responses to various changes in the environment and describes how the responses are related to variations in stimulus probability and the subject’s expectations. The focus is on three well-known responses: (a) the mismatch negativity peaking at 100 to 250 ms and elicited to changes in stimulus attributes, even when the stimuli are not attended to, (b) the P300 response peaking about 300 ms after attended low-probability “oddball” stimuli, and (c) the N400 peaking about 400 ms after semantic or lexical violations of sentences presented either visually or auditorily. Continent negative variation and error-related negativity are introduced as well.