Simon van Gaal

Unconscious Activation of the Prefrontal No-Go Network

Cognitive control processes involving prefrontal cortex allow humans to overrule and inhibit habitual responses to optimize performance in new and challenging situations, and traditional views hold that cognitive control is tightly linked with consciousness. We used functional magnetic resonance imaging to investigate to what extent unconscious “no-go” stimuli are capable of reaching cortical areas involved in inhibitory control, particularly the inferior frontal cortex (IFC) and the pre-supplementary motor area (pre-SMA). Participants performed a go/no-go task that included conscious (weakly masked) no-go trials, unconscious (strongly masked) no-go trials, as well as go trials. Replicating typical neuroimaging findings, response inhibition on conscious no-go stimuli was associated with a (mostly right-lateralized) frontoparietal “inhibition network.” Here, we demonstrate, however, that an unconscious no-go stimulus also can activate prefrontal control networks, most prominently the IFC and the pre-SMA. Moreover, if it does so, it brings about a substantial slowdown in the speed of responding, as if participants attempted to inhibit their response but just failed to withhold it completely. Interestingly, overall activation in this “unconscious inhibition network” correlated positively with the amount of slowdown triggered by unconscious no-go stimuli. In addition, neural differences between conscious and unconscious control are revealed. These results expand our understanding of the limits and depths of unconscious information processing in the human brain and demonstrate that prefrontal cognitive control functions are not exclusively influenced by conscious information.

Unconscious High-Level Information Processing Implication for Neurobiological Theories of Consciousness

Theories about the neural correlates and functional relevance of consciousness have traditionally assigned a crucial role to the prefrontal cortex in generating consciousness as well as in orchestrating high-level conscious control over behavior. However, recent neuroscientific findings show that prefrontal cortex can be activated unconsciously. The depth, direction, and scope of these activations depend on several top-down factors such as the task being probed (task-set, strategy) and on (temporal/spatial) attention. Regardless, such activations—when mediated by feedforward activation only—do not lead to a conscious sensation. Although unconscious, these prefrontal activations are functional, in the sense that they are associated with behavioral effects of cognitive control, such as response inhibition, task switching, conflict monitoring, and error detection. These findings challenge the pivotal role of the prefrontal cortex in consciousness. Instead, it appears that specific brain areas (or cognitive modules) may support specific cognitive functions but that consciousness is independent of this. Conscious sensations arise only when the brain areas involved engage in recurrent interactions enabling the long-lasting exchange of information between brain regions. Moreover, recent evidence suggests that also the state of consciousness, for example, in vegetative state patients or during sleep and anesthesia, is closely related to the scope and extent of residual recurrent interactions among brain regions.

Dissociating Consciousness from Inhibitory Control: Evidence for Unconsciously Triggered Response Inhibition in the Stop-Signal Task.

Theories about the functional relevance of consciousness commonly posit that higher order cognitive control functions, such as response inhibition, require consciousness. To test this assertion, the authors designed a masked stop-signal paradigm to examine whether response inhibition could be triggered and initiated by masked stop signals, which inform participants to stop an action they have begun. In 2 experiments, masked stop signals were observed to occasionally result in full response inhibition as well as to yield a slow down in the speed of responses that were not inhibited. The magnitude of this subliminally triggered response time slowing effect correlated with the efficiency measure (stop signal reaction time) of response inhibition across participants. Thus, response inhibition can be triggered unconsciously-more so in individuals who are good inhibitors and under conditions that are associated with efficient response inhibition. These results indicate that in contradiction to common theorizing, inhibitory control processes can operate outside awareness.

Unconsciously Triggered Conflict Adaptation

In conflict tasks such as the Stroop, the Eriksen flanker or the Simon task, it is generally observed that the detection of conflict in the current trial reduces the impact of conflicting information in the subsequent trial; a phenomenon termed conflict adaptation. This higher-order cognitive control function has been assumed to be restricted to cases where conflict is experienced consciously. In the present experiment we manipulated the awareness of conflict-inducing stimuli in a metacontrast masking paradigm to directly test this assumption. Conflicting response tendencies were elicited either consciously (through primes that were weakly masked) or unconsciously (strongly masked primes). We demonstrate trial-by-trial conflict adaptation effects after conscious as well as unconscious conflict, which could not be explained by direct stimulus/response repetitions. These findings show that unconscious information can have a longer-lasting influence on our behavior than previously thought and further stretch the functional boundaries of unconscious cognition.

Unconscious Errors Enhance Prefrontal-Occipital Oscillatory Synchrony

The medial prefrontal cortex (MFC) is critical for our ability to learn from previous mistakes. Here we provide evidence that neurophysiological oscillatory long-range synchrony is a mechanism of post-error adaptation that occurs even without conscious awareness of the error. During a visually signaled Go/No-Go task in which half of the No-Go cues were masked and thus not consciously perceived, response errors enhanced tonic (i.e., over 1–2 s) oscillatory synchrony between MFC and occipital cortex (OCC) leading up to and during the subsequent trial. Spectral Granger causality analyses demonstrated that MFC → OCC directional synchrony was enhanced during trials following both conscious and unconscious errors, whereas transient stimulus-induced occipital → MFC directional synchrony was independent of errors in the previous trial. Further, the strength of pre-trial MFC-occipital synchrony predicted individual differences in task performance. Together, these findings suggest that synchronous neurophysiological oscillations are a plausible mechanism of MFC-driven cognitive control that is independent of conscious awareness.

Dissociable brain mechanisms underlying the conscious and unconscious control of behavior

Cognitive control allows humans to overrule and inhibit habitual responses to optimize performance in challenging situations. Contradicting traditional views, recent studies suggest that cognitive control processes can be initiated unconsciously. To further capture the relation between consciousness and cognitive control, we studied the dynamics of inhibitory control processes when triggered consciously versus unconsciously in a modified version of the stop task. Attempts to inhibit an imminent response were often successful after unmasked (visible) stop signals. Masked (invisible) stop signals rarely succeeded in instigating overt inhibition but did trigger slowing down of response times. Masked stop signals elicited a sequence of distinct ERP components that were also observed on unmasked stop signals. The N2 component correlated with the efficiency of inhibitory control when elicited by unmasked stop signals and with the magnitude of slowdown when elicited by masked stop signals. Thus, the N2 likely reflects the initiation of inhibitory control, irrespective of conscious awareness. The P3 component was much reduced in amplitude and duration on masked versus unmasked stop trials. These patterns of differences and similarities between conscious and unconscious cognitive control processes are discussed in a framework that differentiates between feedforward and feedback connections in yielding conscious experience.

Dynamic Interactions between Large-Scale Brain Networks Predict Behavioral Adaptation after Perceptual Errors

Failures to perceive visual stimuli lead to errors in decision making. Different theoretical accounts implicate either medial frontal (MF) cognitive control processes or prestimulus occipital (OC) cortical oscillatory dynamics in errors during perceptual tasks. Here, we show that these 2 previously unconnected theoretical accounts can be reconciled, and the brain regions described by the 2 theories have complimentary and interactive roles in supporting error adaptation. Using a perceptual discrimination task and time–frequency network-based analyses of electroencephalography data, we show that perceptual anticipation and posterror top–down control mechanisms recruit distinct but interacting brain networks. MF sites were a hub for theta-band networks and theta–alpha coupling elicited after errors, whereas occipital sites were a network hub during stimulus anticipation and alpha–gamma coupling. Granger causality analyses revealed that these networks communicate in their preferred direction and frequency band: response-related MF → OC interactions occurred in the theta band, whereas stimulus anticipation-related OC → MF interactions occurred in the alpha band. Subjects with stronger network interactions were more likely to improve performance after errors. These findings demonstrate that multiple large-scale brain networks interact dynamically and in a directionally specific manner in different frequency bands to support flexible behavior adaptation during perceptual decision making.

The role of consciousness in cognitive control and decision making

Here we review studies on the complexity and strength of unconscious information processing. We focus on empirical evidence that relates awareness of information to cognitive control processes (e.g., response inhibition, conflict resolution, and task-switching), the life-time of information maintenance (e.g., working memory) and the possibility to integrate multiple pieces of information across space and time. Overall, the results that we review paint a picture of local and specific effects of unconscious information on various (high-level) brain regions, including areas in the prefrontal cortex. Although this neural activation does not elicit any conscious experience, it is functional and capable of influencing many perceptual, cognitive (control) and decision-related processes, sometimes even for relatively long periods of time. However, recent evidence also points out interesting dissociations between conscious and unconscious information processing when it comes to the duration, flexibility and the strategic use of that information for complex operations and decision-making. Based on the available evidence, we conclude that the role of task-relevance of subliminal information and meta-cognitive factors in unconscious cognition need more attention in future work.

Can the meaning of multiple words be integrated unconsciously

What are the limits of unconscious language processing? Can language circuits process simple grammatical constructions unconsciously and integrate the meaning of several unseen words? Using behavioural priming and electroencephalography (EEG), we studied a specific rule-based linguistic operation traditionally thought to require conscious cognitive control: the negation of valence. In a masked priming paradigm, two masked words were successively (Experiment 1) or simultaneously presented (Experiment 2), a modifier (‘not’/‘very’) and an adjective (e.g. ‘good’/‘bad’), followed by a visible target noun (e.g. ‘peace’/‘murder’). Subjects indicated whether the target noun had a positive or negative valence. The combination of these three words could either be contextually consistent (e.g. ‘very bad - murder’) or inconsistent (e.g. ‘not bad - murder’). EEG recordings revealed that grammatical negations could unfold partly unconsciously, as reflected in similar occipito-parietal N400 effects for conscious and unconscious three-word sequences forming inconsistent combinations. However, only conscious word sequences elicited P600 effects, later in time. Overall, these results suggest that multiple unconscious words can be rapidly integrated and that an unconscious negation can automatically ‘flip the sign’ of an unconscious adjective. These findings not only extend the limits of subliminal combinatorial language processes, but also highlight how consciousness modulates the grammatical integration of multiple words.

How awareness changes the relative weights of evidence during human decision-making

A combined behavioral and brain imaging study shows how sensory awareness and stimulus visibility can influence the dynamics of decision-making in humans.