Dissociable neural oscillatory mechanisms underlying unconscious priming of externally and intentionally initiated inhibition
Introduction
Suppressing externally and intentionally initiated impulsive movements is a hallmark of human action control (Hommel and Wiers, 2017). This contributes to physical survival (e.g., braking immediately when a cyclist swerves into a lane to avoid a traffic accident), as well as social interdependency (e.g., stopping the urge to rebuke a work partner to refrain from interpersonal problems) (Aron et al., 2007; Aron and Poldrack, 2006; Haggard, 2008). Increasing evidence indicates that the neural substrates of externally and intentionally initiated inhibition are substantially distinct (Filevich et al., 2012; Schel et al., 2014a). Specifically, externally initiated inhibition, which is termed as “response inhibition”, denotes the active suppression of imperative movements induced by exogenous No-Go or Stop signals (Aron et al., 2014; Bokura et al., 2001; Verbruggen and Logan, 2008). Moreover, it is associated with a lateral premotor frontal network, including the inferior frontal cortex (IFC) and the pre-supplementary motor area (pre-SMA) (Blasi et al., 2006; Chikazoe et al., 2009; Simmonds et al., 2008; van Gaal et al., 2010). Contrastingly, intentionally initiated inhibition, which is termed as “intentional inhibition”, involves voluntarily withholding pre-potent actions at the last moment (Brass and Haggard, 2007, Brass and Haggard, 2008; Kuhn et al., 2009). Further, it is related to a medial frontal system, including the dorsal fronto-median cortex, pre-SMA, rostral cingulated zone, and anterior insular cortex (Brass and Haggard, 2007, Brass and Haggard, 2010; Kuhn and Brass, 2009; Kuhn et al., 2009; Schel et al., 2014b).
However, recent electrophysiological research has reported an association of the N2 component over the prefrontal cortex (PFC) with externally and intentionally generated inhibition (Parkinson and Haggard, 2015). The inconsistency between high temporal- and spatial-resolution electrophysiological (e.g., event-related potentials [ERPs]) and neuroanatomical findings (e.g., functional magnetic resonance imaging [fMRI]), respectively, indicates the need to identify effective neural markers for distinguishing externally and intentionally initiated inhibition. Analyzing neural oscillatory dynamics is a potential candidate. Compared with ERPs based on evoked cortical responses to task-relevant stimuli, neural oscillatory dynamics, which are considered to be characterized by induced cortical responses, are thought to present more extensive information and delineate more realistic brain activity patterns (Cohen, 2017; Engel and Fries, 2010). Furthermore, compared with fMRI, analyzing neural oscillatory dynamics allows for the detection of transient cognitive process variations (Walsh et al., 2010). Neuroscience studies on the neural oscillatory features of externally or intentionally initiated inhibition have yielded convincing evidence suggesting that the different inhibitory processes may involve distinct neural oscillatory mechanisms. For example, studies on externally triggered inhibitory processes have reported more pronounced theta band oscillatory power (4–8 Hz) over the PFC in response to No-Go or Stop signals (compared with the Go signal) (Barry, 2009; Harper et al., 2014; Yamanaka and Yamamoto, 2010). This is consistent with the notion that theta band oscillation is indicative of the need for high-level control processes and can be employed to implement such control (Cavanagh & Frank, 2014). Contrastingly, heightened event-related synchronization/desynchronization (ERS/ERD) of alpha/low-beta band oscillation (8–24 Hz) occurs when an individual intentionally cancels the keypress compared with when the keypress is committed in a time-judgment task, suggesting that alpha/low-beta band oscillation may be involved in intentionally generated inhibition (Walsh et al., 2010).
Notably, these studies explored the inhibitory processes only when task-relevant stimuli appeared above the subjective consciousness threshold, which is consistent with the conventional perspective that inhibitory processes require consciousness (Dehaene and Naccache, 2001; Eimer and Schlaghecken, 2003). However, this has been refuted by recent findings showing that unconsciously presented primes can activate inhibitory processes without accessing conscious awareness (Hughes et al., 2009; Parkinson and Haggard, 2014; van Gaal et al., 2008; van Gaal et al., 2010). For example, van Gaal et al., 2008, van Gaal et al., 2010 reported that the “unconscious priming of externally initiated inhibition” using an unconscious version of Go/No-Go tasks. Specifically, individuals presented a more prolonged response on the (forced) Go target following a No-Go prime compared with following a Go prime. Furthermore, the neural substrates of conscious and unconscious externally initiated inhibition involved similar spatiotemporal patterns of brain activity (e.g., the IFC, pre-SMA, and P3 component). Additionally, Parkinson and Haggard (2014) reported “unconscious priming of intentionally initiated inhibition” using an unconscious version of the Go/No-Go/Choose task. Here, participants showed a slower response when deciding to commit a “Go” response and an increased likelihood of withholding the keypress following a No-Go prime compared with a Go prime. However, the neural mechanisms underlying the unconscious priming of intentionally initiated inhibition remain unclear. Moreover, it is unknown whether there is a discrepancy between the unconscious priming of externally and intentionally initiated inhibition.
To address these issues, we developed an unconscious version of the Go/No-Go/Choose task adapted from Parkinson and Haggard (2014) and van Gaal et al. (2010). This comprised of forced and free-choice Go/No-Go targets following unconsciously presented Go, Neutral, and No-Go primes. We aimed to delineate the neural oscillatory dynamics of unconscious priming of externally and intentionally initiated inhibition using EEG technology. Based on previous findings (Barry, 2009; Harper et al., 2014; Walsh et al., 2010; Yamanaka and Yamamoto, 2010), we hypothesized that theta band oscillation may represent prime-induced modulation of externally initiated inhibition, whereas alpha/low-beta band oscillation may represent prime-induced modulation of intentionally generated inhibition.
Section snippets
Participants
We enrolled 24 undergraduate Chinese students (14 females) aged between 18 and 24 years (M = 20.96, SD = 1.71) from Ningbo University with remuneration. All the participants were right-handed, had normal or corrected-to-normal vision, and had no history of physical or mental illness. Two participants were excluded for having above-chance discrimination of the primes. Finally, we analyzed data from 22 participants (12 females, M = 21.14, SD = 1.64). This study complied with the applicable
Prime discrimination
Prime discrimination was calculated to determine whether the employed primes were truly presented unconsciously. Here, we calculated the mean accuracy rate across participants in the discrimination task and compared it with the chance-level of accuracy (33.3%). Moreover, we calculated the discriminability index (d′) for each prime type and compared it with the chance-level (i.e., 0 value) using a series of single-sample t-tests.
Mean reaction times (RTs)
We excluded trials with erroneous responses and RTs > ±3 SD from
Prime discrimination
In the discrimination task, a mean percentage of 33.95% (SD = 0.03) of the trials was correctly discriminated, which did not significantly differ from the chance-level (33.3%; t(21) = 0.89, p = .39). Further, we calculated the discriminability index (d′) for each prime type and compared these values against the 0 value using a series of single-sample t-tests, which revealed no significant effect (−0.054 ≤ d′ ≤ −0.039, ps > .29). This confirmed that the primes were presented unconsciously (the
Discussion
Several neuroimaging studies have suggested distinct mechanisms between externally and intentionally initiated inhibition, which are thought to operate unconsciously. However, the neural oscillatory dynamics underlying both types of unconscious priming of inhibitory processes and whether they share similar neural mechanisms remain unclear. To address this, we used the unconscious version of the Go/No-Go/Choose task, which masked Go, Neutral, and No-Go primes with visible forced and free-choice
Acknowledgements
We thank Jun Jiang (Third Military Medical University) for his help in data analysis. This work was supported by National Natural Science Foundation of China (Grant No. 71942002), Ministry of Education of Humanities and Social Science Project of China (Grant No. 20YJC190003), and sponsored K.C. Wong Magna Fund of Ningbo University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Liuting Diao and Wenping Li contributed equally to this work.