Elsevier

Brain and Cognition

Volume 145, November 2020, 105629
Brain and Cognition

Response inhibition to emotional faces is modulated by functional hemispheric asymmetries linked to handedness

https://doi.org/10.1016/j.bandc.2020.105629Get rights and content

Highlights

  • Handedness-related functional hemispheric asymmetries modulate response inhibition.

  • Stronger face-specific N170 over right hemisphere in right-handers, stronger N170 over left hemisphere in left-handers.

  • Better response inhibition to negative stimuli when projected to the right hemisphere.

  • Better response inhibition to positive stimuli wgen projected to the left hemisphere.

  • Frontal asymmetry modulates response inhibition depending on emotional valence.

Abstract

Effective response inhibition requires efficient bottom-up perceptual processing and effective top-down inhibitory control. To investigate the role of hemispheric asymmetries in these processes, 49 right- and 50 left-handers completed a tachistoscopic Go/Nogo task with positive and negative emotional faces while ERPs were recorded. Frontal resting state EEG asymmetry was assessed as a marker of individual differences in prefrontal inhibitory networks. Results supported a dependency of inhibitory processing on early lateralized processes. As expected, right-handers showed a stronger N170 over the right hemisphere, and better response inhibition when faces were projected to the right hemisphere. Left-handers showed a stronger N170 over the left hemisphere, and no behavioural asymmetry. Asymmetries in response inhibition were also valence-dependent, with better inhibition of responses to negative faces when projected to the right, and better inhibition of responses to positive faces when projected to the left hemisphere. Frontal asymmetry was not related to handedness, but did modulate response inhibition depending on valence. Consistent with the asymmetric inhibition model (Grimshaw & Carmel, 2014), greater right frontal activity was associated with better response inhibition to positive than to negative faces; subjects with greater left frontal activity showed an opposite trend. These findings highlight the interplay between bottom-up and top-down processes in explaining hemispheric asymmetries in response inhibition.

Introduction

In our daily lives we often need to override a habitual or prepotent response so we can achieve our goals. Such response inhibition can be particularly challenging when the triggers for our actions are emotional. Moreover, deficits in inhibiting a response to certain emotional information have been linked to psychopathology, e.g. depression (Goeleven, de Raedt, Baert, & Koster, 2006). Successful inhibition of a response depends on the interplay between bottom-up factors that determine the strength of the behavioural trigger, and the top-down implementation of inhibitory control. Both pathways have been shown to depend on lateralized brain networks, with hemispheric asymmetries in sensory, affective, and perceptual processing affecting the bottom-up pathway (Ocklenburg, Güntürkün, & Beste, 2011), and asymmetric activation in lateral prefrontal regions underpinning effective inhibitory control (Aron, Robbins, & Poldrack, 2004).

Much of what we know about these asymmetries is based on research with right-handers, because left-handers are commonly excluded from neuroscience research for the sake of sample homogeneity (Willems, Peelen, & Hagoort, 2010). This is of course a problem for the generalisability of conclusions and a lost opportunity because left-handers differ from right-handers in many aspects of lateralized processing, e.g., self-body recognition (Morita, Asada, & Naito, 2020), language and spatial attention (e.g., O'Regan and Serrien, 2018, van der Haegen and Brysbaert, 2018), and face and body processing in the visual system (Willems et al., 2010). Along these lines, investigating left-handers may yield unique insights into brain-behaviour relationships. In the present study, we used the natural variation in hemispheric asymmetry provided by studying both left- and right-handers to investigate the lateralized processes that support effective response inhibition.

In the lab, response inhibition is most commonly assessed using the Go/Nogo paradigm (Aron, 2007, Beck et al., 1956). In a typical task, participants are asked to respond to one kind of stimulus (the Go-stimulus) as quickly as possible, while withholding response to another kind (the Nogo-stimulus). In most experimental designs, a Go-response is demanded on the majority of trials, resulting in a prepotent tendency to respond and the need to recruit regulatory control to actively inhibit that response when the Nogo-stimulus is presented (e.g., Aron, 2007, Jones et al., 2002). As mentioned above, effective inhibitory control is especially relevant in the presence of emotional content (e.g., Padmala, Bauer, & Pessoa, 2011). Therefore, in the present study, we used emotional faces as the Go- and Nogo-stimuli to probe the mechanisms of inhibitory control under emotional conditions.

Behaviourally, the main measure of interest is the false alarm rate, reflecting the extent to which a person fails to inhibit a response. Along these lines, good inhibitory control will result in fewer false alarms than poor inhibitory control. Successful inhibition is also reflected in neuronal indices. In neuroimaging and patient studies, inhibitory control as elicited by the Go/Nogo-task is often localised to regions of the lateral prefrontal cortex (Casey et al., 1997, Chikazoe, 2010). In electrophysiological studies, two components of the event-related potential (ERP) have been associated with inhibitory control: the Nogo-N2 and the Nogo-P3. The Nogo-N2 is a negative peak in fronto-parietal areas within 200–300 ms after stimulus presentation that is typically found to be enhanced (i.e., more negative) in Nogo- compared to Go-trials (Eimer, 1993, Gemba and Sasaki, 1989, Jodo and Kayama, 1992, Pfefferbaum et al., 1985). The Nogo-N2 is commonly assumed to reflect inhibitory processes (Band and van Boxtel, 1999, Eimer, 1993), with more negative amplitudes related to better inhibitory performance, e.g., lower false alarm rates (Falkenstein, Hoormann, & Hohnsbein, 1999) and faster responses (van Boxtel, van der Molen, Jennings, & Brunia, 2001). The Nogo-P3 is a positive deflection that peaks within 300–600 ms after stimulus presentation and is also found to be more pronounced on Nogo- compared to Go-trials (Eimer, 1993). In contrast to the Nogo-N2, which is assumed to reflect the main phase of the inhibitory process (e.g., response inhibition), the later occurring Nogo-P3 is argued to reflect post-response processes (Bokura et al., 2001, Roche et al., 2005) such as evaluation of successful inhibition, error detection, and/or context updating (Roche et al., 2005).

From a bottom-up perspective, effective response inhibition depends on efficient processing of incoming sensory signals, which may depend on the hemisphere that dominates perceptual processing. As shown throughout a long history of neuroscientific research, the left and right hemisphere exhibit different functional specializations, and these functional hemispheric asymmetries can be observed for numerous cognitive abilities (for a comprehensive review, see Ocklenburg & Güntürkün, 2018). Whereas processing of language, for example, relies heavily on the left hemisphere (Vigneau et al., 2006), processing of faces seems to particularly engage the right hemisphere (Levine et al., 1988, Rossion et al., 2003). Given that response inhibition is modulated by bottom-up factors, the ability to inhibit a response might be influenced by the hemisphere that initially processes the Go or Nogo stimulus. Indeed, findings from Measso and Zaidel (1990) as well as from Ocklenburg et al. (2011) suggest that responses to words initially processed within the language-dominant left hemisphere are better inhibited than responses to words initially processed within the non-dominant right hemisphere. Similarly, initial processing of faces in the face-dominant right hemisphere facilitates behavioural and neural indices of response inhibition (Ocklenburg, Ness, Güntürkün, Suchan, & Beste, 2013), indicating that this principle is not specific to the language domain.

Compared to right-handers, left-handers often show reduced, or even reversed, functional asymmetries (Knecht et al., 2000). For example, although most left-handers have the same left hemisphere specialization for language processing as right-handers, as a group they are less lateralized, and individuals are more likely to demonstrate a reversed right hemisphere specialization (e.g., Knecht et al., 2000). Similar differences are observed in face processing, with left-handers showing less pronounced right – or even left – hemispheric dominance (Badzakova-Trajkov et al., 2010, Willems et al., 2010). If our assumption is correct that response inhibition is modulated by hemispheric differences in early stages of processing, differing hemispheric asymmetries in right- and left-handers should modulate their inhibitory performance accordingly.

To examine the consequences of early visual lateralization on behavioural and neural indices of inhibitory control, we restricted initial processing to one hemisphere through tachistoscopic presentation of visual stimuli (Bourne, 2006), i.e., the Go or Nogo stimulus was briefly presented in either the left or right visual field (RVF; LVF). Given the anatomy of the visual pathway, visual stimuli presented in the LVF are initially processed in the right hemisphere, while stimuli presented in the RVF are initially processed in the left hemisphere. To examine laterality for face processing in our sample of left- and right-handers, we used the N170, an ERP component linked to the encoding of faces (Herrmann et al., 2005, Rossion et al., 2003). If tachistoscopic presentation works as intended, we would expect a more negative N170 over the right hemisphere after LVF presentation, and a more negative N170 over the left hemisphere after RVF presentation. Additionally, assuming right hemispheric dominance for faces in right-handers, for the right-handed participants we expected a more negative N170 overall over the right hemisphere than over the left. Assuming less pronounced right (or potentially even left) hemispheric dominance in left-handers, for the left-handed participants we would expect a less pronounced N170 over the right hemisphere (or potentially even a more pronounced N170 over the left).

If this hemispheric difference in early face processing affects subsequent inhibitory control, we should expect to see fewer false alarms in right-handers after processing the faces within the dominant right hemisphere (LVF presentation), while for left-handers we would expect no lateral differences, or potentially even fewer false alarms after processing in the left hemisphere (RVF presentation). Likewise, for the Nogo-N2, we expected right-handers to show increased negativity after processing in the non-dominant left hemisphere (reflecting greater conflict), while for left-handers we expected this laterality effect to be less pronounced or even a reversed effect. Finally, as an index of successful inhibition, the Nogo-P3 for right-handers should be stronger after initial processing in the dominant right hemisphere, while again for left-handers we would expect a less pronounced or even reversed laterality effect.

In addition to these hemispheric asymmetries in bottom-up stimulus processing, top-down response inhibition is also suggested to depend on trait asymmetries in prefrontal activation (Aron et al., 2004, Gable et al., 2015, Gable et al., 2018, Grimshaw and Carmel, 2014). In EEG studies, this frontal asymmetry (FA) can be measured by comparing alpha power generated by left versus right frontal cortices during a resting phase. Alpha power (visible as 8–12 Hz frequency in the EEG) is assumed to reflect the inverse of regional neuronal activity, so less alpha power over right than left frontal cortices indicates greater right frontal activity (FA), and less alpha power over left than right frontal cortices indicates greater left FA (e.g., Coan and Allen, 2004, Cook et al., 1998, Davidson et al., 1990). Stable, individual differences in resting state FA have been linked to a number of cognitive, affective, and personality factors (e.g., Harmon-Jones and Gable, 2018, Keune et al., 2018, Thibodeau et al., 2006). With respect to inhibitory control, two models suggest a relationship between FA and response inhibition. The revised behavioural inhibition model (r-BIS) associates the right frontal hemisphere with a regulatory control system, and thus predicts that greater rightward FA should result in better inhibitory performance (Aron et al., 2004, Gable et al., 2015, Gable et al., 2018). In contrast, the asymmetric inhibition model (AIM; Grimshaw & Carmel, 2014) suggests that hemispheric differences in inhibitory control are modulated by valence, with greater right FA associated with better inhibition of positive information, and greater left FA associated with better inhibition of negative information. Our experimental paradigm allows us to test the predictions arising from both models. If the r-BIS is valid, we would expect a main effect of frontal asymmetry on inhibitory performance, i.e., greater rightward FA should be associated with fewer false alarms. According to the AIM, we would expect an interaction of frontal asymmetry and valence on inhibitory performance, i.e., greater rightward FA should be associated with fewer false alarms in response to positive versus negative stimuli, and greater leftward FA should be associated with fewer false alarms in response to negative versus positive stimuli.

Concerning handedness, little is known about FA in left- versus right-handers. Some findings suggest that in comparison to consistent right-handers, participants with no clear hand preference show greater right frontal activity (Ocklenburg et al., 2019, Propper et al., 2012). In the absence of a clear theoretical rationale, we consider analyses involving handedness to be exploratory.

Section snippets

Sample

In total, 106 participants took part in the experiment, of which seven had to be excluded due to the following reasons: incomplete data sets because of technical problems (three), current intake of antidepressants (one), insufficient EEG data quality (two), and task performance at chance level based on d’ values (one). The final sample of 49 self-reported right-handers (35 women and 14 men, mean age = 25.57 years, SD = 6.45, range 19–54 years) and 50 self-reported left-handers (35 women and 15

Results

Regarding overall task performance, participants showed a mean response time of 517 ms (SD = 61) in Go-trials, with a mean hit rate of 86.88% (SD = 11.09). The correct rejection rate was 77.01% (SD = 13.12). Self-reported left- and right-handers did not differ significantly in overall task performance (left-handers: mean response time = 510 ms (SD = 61), mean hit rate = 88.72 (SD = 10.20), mean false alarm rate = 23.13 (SD = 13.34); right-handers: mean response time = 526 ms (SD = 61), mean hit

Discussion

The present study investigated the role of functional hemispheric asymmetries in both perceptual and inhibitory processes. Importantly, we used the natural variation in hemispheric asymmetry provided by handedness to investigate the lateralized processes that support effective response inhibition in the context of emotional stimuli. We also recorded resting-state EEG asymmetry in frontal cortex as a marker of individual differences in prefrontal networks associated with inhibitory control.

As

Conclusion

The present findings make a strong claim for the proposed dependency of executive functions on early lateralized processes. They confirm theories of differential lateralisation of early face processing in right- and left-handers, and extend the existing literature by showing that those natural hemispheric differences influence the higher cognitive process of response inhibition on a behavioural level. Moreover, our study postulates that response inhibition is not only influenced by early

Funding information

This work was partly supported by a grant to support scientific and technological collaboration between Germany and New Zealand awarded to S.O. and J.P. by the Federal Ministry of Education and Research Germany (Bundesministerium für Bildung und Forschung, BMBF), and by a complementary grant from the Royal Society of New Zealand Catalyst Fund to G.G.

CRediT authorship contribution statement

Elisabeth Schrammen: Writing - original draft, Formal analysis. Gina M. Grimshaw: Writing - review & editing, Conceptualization, Methodology. Adam Berlijn: Writing - review & editing, Formal analysis. Sebastian Ocklenburg: Writing - review & editing, Conceptualization, Methodology, Project administration. Jutta Peterburs: Writing - review & editing, Visualization, Conceptualization, Methodology, Supervision, Project administration.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References (87)

  • M. Eimer

    Effects of attention and stimulus probability on ERPs in a Go/Nogo task

    Biological Psychology

    (1993)
  • M. Falkenstein et al.

    ERP components in Go/Nogo tasks and their relation to inhibition

    Acta Psychologica

    (1999)
  • H. Gemba et al.

    Potential related to no-go reaction of go/no-go hand movement task with color discrimination in human

    Neuroscience Letters

    (1989)
  • E. Goeleven et al.

    Deficient inhibition of emotional information in depression

    Journal of Affective Disorders

    (2006)
  • E. Jodo et al.

    Relation of a negative ERP component to response inhibition in a Go/No-go task

    Electroencephalography and Clinical Neurophysiology

    (1992)
  • S. Klöppel et al.

    The effect of handedness on cortical motor activation during simple bilateral movements

    NeuroImage

    (2007)
  • S.C. Levine et al.

    Face recognition: A general or specific right hemisphere capacity?

    Brain and Cognition

    (1988)
  • G. Measso et al.

    Effect of response programming on hemispheric differences in lexical decision

    Neuropsychologia

    (1990)
  • T. Morita et al.

    Right-hemispheric dominance in self-body recognition is altered in left-handed individuals

    Neuroscience

    (2020)
  • H. Nakata et al.

    Effects of a go/nogo task on event-related potentials following somatosensory stimulation

    Clinical Neurophysiology

    (2004)
  • L.B. Neal et al.

    Neurophysiological markers of multiple facets of impulsivity

    Biological Psychology

    (2016)
  • S. Ocklenburg et al.

    Lateralized neural mechanisms underlying the modulation of response inhibition processes

    NeuroImage

    (2011)
  • R.C. Oldfield

    The assessment and analysis of handedness: The Edinburgh inventory

    Neuropsychologia

    (1971)
  • F. Perrin et al.

    Spherical splines for scalp potential and current density mapping

    Electroencephalography and Clinical Neurophysiology

    (1989)
  • A. Pfefferbaum et al.

    ERPs to response production and inhibition

    Electroencephalography and Clinical Neurophysiology

    (1985)
  • P.A. Reuter-Lorenz et al.

    Hemispheric specialization and the perception of emotion: Evidence from right-handers and from inverted and non-inverted left-handers

    Neuropsychologia

    (1983)
  • B. Rossion et al.

    Does physical interstimulus variance account for early electrophysiological face sensitive responses in the human brain? Ten lessons on the N170

    NeuroImage

    (2008)
  • B. Rossion et al.

    Early lateralization and orientation tuning for face, word, and object processing in the visual cortex

    NeuroImage

    (2003)
  • D.L. Santesso et al.

    Frontal EEG asymmetry and sensation seeking in young adults

    Biological Psychology

    (2008)
  • E.E. Smith et al.

    Assessing and conceptualizing frontal EEG asymmetry: An updated primer on recording, processing, analyzing, and interpreting frontal alpha asymmetry

    International journal of psychophysiology: Official journal of the International Organization of Psychophysiology

    (2017)
  • J.L. Smith et al.

    Movement-related potentials in the Go/NoGo task: The P3 reflects both cognitive and motor inhibition

    Clinical Neurophysiology

    (2008)
  • A. Starr et al.

    Readiness to respond in a target detection task: Pre- and post-stimulus event-related potentials in normal subjects

    Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section

    (1995)
  • D. Tanner et al.

    On high-pass filter artifacts (they're real) and baseline correction (it's a good idea) in ERP/ERMF analysis

    Journal of Neuroscience Methods

    (2016)
  • P. Thoma et al.

    BESST (Bochum Emotional Stimulus Set)–a pilot validation study of a stimulus set containing emotional bodies and faces from frontal and averted views

    Psychiatry Research

    (2013)
  • G.J.M. van Boxtel et al.

    A psychophysiological analysis of inhibitory motor control in the stop-signal paradigm

    Biological Psychology

    (2001)
  • M. Vigneau et al.

    Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing

    NeuroImage

    (2006)
  • R. Voegler et al.

    Electrophysiological correlates of performance monitoring under social observation in patients with social anxiety disorder and healthy controls

    Biological Psychology

    (2018)
  • T.D. Wager et al.

    Valence, gender, and lateralization of functional brain anatomy in emotion: A meta-analysis of findings from neuroimaging

    NeuroImage

    (2003)
  • N. Adelhöfer et al.

    How perceptual ambiguity affects response inhibition processes

    Journal of neurophysiology

    (2019)
  • H. Aguinis et al.

    Best-practice recommendations for estimating cross-level interaction effects using multilevel modeling

    Journal of Management

    (2013)
  • J.J.B. Allen et al.

    The stability of resting frontal electroencephalographic asymmetry in depression

    Psychophysiology

    (2004)
  • D.M. Amodio et al.

    Neurocognitive components of the behavioral inhibition and activation systems: Implications for theories of self-regulation

    Psychophysiology

    (2008)
  • A.R. Aron

    The neural basis of inhibition in cognitive control

    The Neuroscientist: A Review Journal Bringing Neurobiology, Neurology and Psychiatry

    (2007)
  • 1

    These authors contributed equally.

    View full text