Elsevier

Biological Psychology

Volume 114, February 2016, Pages 81-92
Biological Psychology

The effect of acute alcohol on motor-related EEG asymmetries during preparation of approach or avoid alcohol responses

https://doi.org/10.1016/j.biopsycho.2015.12.012Get rights and content

Highlights

  • Alcohol effects on approach-avoidance bias and cortical asymmetries were investigated.

  • Heavy and light drinking adolescents were compared after alcohol and placebo.

  • Heavy drinkers had greater beta-asymmetry while approaching control cues.

  • Beta-asymmetry was related to problems with the self-control of alcohol intake.

  • Alcohol-induced changes on the bias were related with future alcohol use.

Abstract

Alcohol-approach tendencies have been associated with heavy drinking and play a role in the transition to alcohol abuse. Such cognitive biases might predict future alcohol use better under a low dose of alcohol. The aim of this prospective study was to investigate both the magnitude and the predictive power of alcohol-induced changes on approach-avoidance bias and bias-related cortical asymmetries during response preparation across heavy and light drinking adolescents. In heavy drinking adolescents greater approach-related asymmetry index in the beta-band was observed for soft-drink cues compared to alcohol ones and this increase was associated with increase in difficulty to regulate alcohol intake. Earlier findings demonstrated that young heavy drinkers hold both positive and negative implicit alcohol associations, reflecting an ambiguity towards alcohol. The increase in approach related beta-lateralization for soft-drink cues measured in this study may represent a compensatory effort for the weaker S–R mapping (approaching soft drink). The MRAA findings in this study may highlight a mechanism related to overcompensation due to ambivalent attitudes towards drinking in our heavy drinking sample who had greater problems to limit their alcohol intake compared to light drinkers. Moreover, a relatively strong approach soft-drink and weak approach alcohol reaction-time bias after alcohol predicted decreasing drinking; suggesting that the capacity to control the bias under alcohol could be a protective factor.

Introduction

In recent years, researchers have shown an increasing interest in drug-related cognitive biases due to their value in predicting drug-related behaviours and clinical outcomes. Cognitive biases have been found in adolescents and young adults in attentional processes (e.g. Field, Christiansen, Cole, & Goudie, 2007), action tendencies (approach biases, Field, Kiernan, Eastwood, & Child, 2008; Wiers, Rinck, Dictus, & van den Wildenberg, 2009) and implicit memory associations (e.g. Thush et al., 2007). In adolescents these biases have been found to be predictive of drinking (memory bias: Thush and Wiers, 2007, Thush et al., 2008; approach bias: Peeters et al., 2013). Note that some of these studies involved high-risk groups, either defined by education (special education for adolescents with externalizing problems, Peeters et al., 2013) or by genotype (e.g., Wiers et al., 2009). Training varieties of these tasks have been found to change the bias and reduce relapse rates (Eberl et al., 2013, Schoenmakers and Wiers, 2010; Wiers, Eberl, Rinck, Becker, & Lindenmeyer, 2011). Such results have clinical implications but are also of theoretical interest. Studies in young samples may provide important insights for our understanding of the role of automatic motivational processes in the continuation of drug use later in life (i.e. Curtin, Barnett, Colby, Rohsenow, & Monti, 2005).

The approach avoidance task (AAT) assesses automatically activated action tendencies to approach or avoid a category of stimuli (Rinck and Becker, 2007, Wiers et al., 2009). Facilitations in response times when approaching alcohol-related stimuli compared to avoidance response indicates that alcohol stimuli are compatible with approach versus avoidance responses. These stimulus-response compatibility effects are thought to emerge when implicit action tendencies are in line with the instructed responses during congruent blocks and/or it is difficult to maintain a stimulus-response association during incongruent blocks. If indeed the motivational value of the alcohol cues drives the bias in the alcohol AAT, facilitation in approach alcohol responses might be related to subjects’ drinking profile. This was exemplified by the finding of a stronger approach bias in heavier drinkers (Field et al., 2008; especially in those with a g-allele in the OPRM1 gene, Wiers et al., 2009).

Stimulus-response compatibility effects on motor programs can be studied through the hand-related response preparation. Regarding hand-related neural activity, both during movement preparation and execution, the beta (14–30 Hz) and mu (8–12 Hz) amplitude, decrease in amplitude (event-related desynchronization, ERD) over the motor cortex contralateral to the movement limb (Doyle, Yarrow, & Brown, 2005; Gladwin, Lindsen, & de Jong, 2006; Gladwin, ’t Hart, de Jong, 2008; Pfurtscheller, Neuper, Pichler-Zalaudek, Edlinger, & Lopes da Silva, 2000; Poljac and Yeung, 2014, Stancák and Pfurtscheller, 1995). These movement-related amplitude asymmetries (MRAA) can be quantified according to the double subtraction rationale of the Lateralized Readiness Potentials in the time domain (LRP; Colebatch, 2007); by taking the difference in amplitude between contralateral and ipsilateral activity during preparation of right-hand response minus difference between ipsi- and contra-lateral activity during preparation of left-hand response (Gladwin et al., 2006). Given that the calculation of the MRAA eliminates motor-unrelated hemispheric lateralization, the remaining activity reflects motor-related preparatory lateralized activity. With repetitive alcohol use, cues associated with alcohol gain incentive salience and induce motivational responses (Robinson and Berridge, 1993, Robinson and Berridge, 2008). However, the process of preparing an action (approach/avoid) for conditioned cues with a specific affective connotation (alcohol vs. control cues, or positive vs. negative cues) requires mapping a motor response to a stimulus and in the case of approach tendencies this mapping is strengthened for approach responses on alcohol cues. Therefore both incentive motivations and pavlovian responses are likely to play a role in the approach bias. Compared to many other cognitive biases, stimulus-response associations are more central to approach tendencies, given that in this bias certain stimulus categories are inextricably linked with specific motor responses. To this end, studying MRAA indices allow us to differentiate tasks that require much skill and effort from automatically activated tasks; by comparing stimulus-response associations with different strengths. The first aim of the present study was to investigate the motor preparation in alcohol approach–avoidance bias by means of motor-related asymmetries as a function of drinking profile (light and heavy drinkers). Thus, we used a modified version of the AAT task that resembles the one used in our previous study (Korucuoglu, Gladwin, & Wiers, 2014), extending it by focusing on lateralized spectral analysis. In our previous study, preparatory activity was measured by presenting a warning (or a preparatory) stimulus before the presentation of an imperative stimulus (S2) to which the subject had to give a motor response. Contrary to our previous study where right-hand joystick movement was required for response, the task used in this study consisted of trials requiring both left and right hand approach or avoid responses for alcohol-related and control cues to allow the study of motor-related lateralization.

In an earlier study, we showed that a low dose of alcohol administration increased the parietal beta-ERD during preparation for the alcohol-compatible trials (‘approach-alcohol/avoid-control picture trials’) following alcohol administration (Korucuoglu et al., 2014), similar to facilitating effects of alcohol on appetitive processes (Duka & Townshend, 2004; Hodgson, Rankin, & Stockwell, 1979). A second aim of the current study was to assess whether acute alcohol would enhance asymmetries associated with drug-related approach/avoidance motivations. Finally, we tested whether alcohol-induced effects on lateralized power spectra would be related to alcohol consumption, problems, and motivations; and would predict alcohol escalation in a young sample.

Section snippets

Participants

Forty adolescents (age range = 16–20 years) were recruited from local high schools in Amsterdam. Prior to the testing sessions, participants were informed about the study restrictions by email. Participants were required to be minimally 16 years-old (minimum drinking age in Netherlands at the time of the study), with a minimum weight of 50 kg and to have had at least one full drink in their lifetime. Participants were requested not to drink any alcohol 24 h before testing and eat a meal or drink

Manipulation checks

For the Stimulation and Sedation subscales of B-BAES scores, results revealed a significant main effect of Dose for the sedation subscale (F(1, 32) = 5.016, p = .032, η2p = .15). Sedation scores were higher for the alcohol dose compared to the placebo dose, however post-hoc analysis with paired t-tests did not reveal any differences across conditions. All other main and interaction effects were not significant (p > .15).

Three subjects’ post-task BrAC data were lost, the analysis was completed with the

Discussion

In the current EEG study, we focused on motor-related lateralization during preparation for approach and avoidance behaviors in the context of alcohol cues and investigated the effects of a prime dose of alcohol on these neurophysiological measures in heavy and light drinking adolescents. As in previous studies of motor preparation, preparation of a left/right hand response during the alcohol approach-avoidance task led to an MRAA following the presentation of the imperative stimulus

Conflict of interest

All authors declare that they have no conflict of interest.

Acknowledgements

The authors are supported by VICI award 453.08.01 from the Netherlands National Science Foundation (N.W.O.). Thomas E. Gladwin is supported by ERAB grant EA 1239.

References (41)

  • C.S. Nam et al.

    Movement imagery-related lateralization of event-related (de)synchronization (ERD/ERS): motor-imagery duration effects

    Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology

    (2011)
  • G. Pfurtscheller et al.

    Do brain oscillations of different frequencies indicate interaction between cortical areas in humans?

    Neuroscience Letters

    (2000)
  • M. Rinck et al.

    Approach and avoidance in fear of spiders

    Journal of Behavior Therapy and Experimental Psychiatry

    (2007)
  • T.E. Robinson et al.

    The neural basis of drug craving: an incentive-sensitization theory of addiction

    Brain Research Reviews

    (1993)
  • A. Stancák et al.

    Desynchronization and recovery of β rhythms during brisk and slow self-paced finger movements in man

    Neuroscience Letters

    (1995)
  • C. Thush et al.

    Explicit and implicit alcohol-related cognitions and the prediction of future drinking in adolescents

    Addictive Behaviors

    (2007)
  • C. Thush et al.

    Interactions between implicit and explicit cognition and working memory capacity in the prediction of alcohol use in at-risk adolescents

    Drug and Alcohol Dependence

    (2008)
  • K.S. Birak et al.

    Conditioned tolerance to the effects of alcohol on inhibitory control in humans

    Alcohol and Alcoholism (Oxford, Oxfordshire)

    (2011)
  • K.S. Birak et al.

    Effect of cues associated with an alcoholic beverage on executive function

    Journal of Studies on Alcohol and Drugs

    (2010)
  • J.G. Colebatch

    Bereitschaftspotential and movement-related potentials: origin, significance, and application in disorders of human movement

    Movement Disorders

    (2007)
  • Cited by (13)

    • Is the posterior cingulate cortex an on-off switch for tinnitus?: A comparison between hearing loss subjects with and without tinnitus

      2021, Hearing Research
      Citation Excerpt :

      To identify the neural substrates associated with tinnitus in subjects with HL, we performed data acquisition and pre-processing procedures as previously reported (Han et al., 2018; Han et al., 2020a; Lee et al., 2019; Song et al., 2017; Vanneste et al., 2018a). Before measurement, the participants were asked not to drink alcohol for 24 h before EEG recording and to avoid caffeinated beverages on the day of recording to prevent alcohol-induced changes in the EEG signal (Korucuoglu et al., 2016) or caffeine-induced reductions in alpha and beta power (Siepmann et al., 2002). The EEGs were recorded with the patient seated upright with eyes closed for 5 min as in recent literature (Lan et al., 2020; Souza et al., 2020; Zhang et al., 2020a; Zhang et al., 2020b) using a tin-electrode cap (ElectroCap, Eaton, OH, USA) and a Mitsar amplifier (EEG-201; Mitsar, St. Petersburg, Russia) in a fully lit room shielded against sound and stray electric fields.

    • Neurophysiological correlates of alcohol-specific inhibition in alcohol use disorder and its association with craving and relapse

      2021, Clinical Neurophysiology
      Citation Excerpt :

      Following a different approach, this study used the change in craving from pre- to post-detoxification as a covariate, but did not observe any effects (Campanella et al., 2019a). However, in non-clinical samples, studies have reported NoGo-N2 amplitude increases for alcohol-related stimuli (Fleming and Bartholow, 2014, Korucuoglu et al., 2016) as well as food stimuli (Wolz et al., 2017) and have also linked these effects to craving (Wolz et al., 2017) or alcohol-sensitivity (Fleming and Bartholow, 2014). The finding that the conflict–sensitive NoGo-N2 is impacted by the stimulus type in participants with higher craving bears clinical relevance because it indicates that this enhanced conflict might be a potentially important target for therapeutic interventions.

    • How interindividual differences shape approach-avoidance behavior: Relating self-report and diagnostic measures of interindividual differences to behavioral measurements of approach and avoidance

      2020, Neuroscience and Biobehavioral Reviews
      Citation Excerpt :

      The exception is one study showing that drinking alcohol led to faster approach of sexual imagery and faster avoidance of contraception images (Simons et al., 2016). In another study, reported results were mixed depending on whether bias scores or reaction times were analyzed (Korucuoglu et al., 2016). Furthermore, administering alcohol seems to necessitate careful selection of the control condition due to potential placebo effects (Christiansen et al., 2013).

    • A dual process perspective on advances in cognitive science and alcohol use disorder

      2019, Clinical Psychology Review
      Citation Excerpt :

      IRT has been used to improve the measurement of memory biases assessed via free response (see Shono, Grenard, Ames, & Stacy, 2014), whereas the quad model has been used to disentangle the underlying (impulsive and control) processes in RT measures of memory bias, as measures of implicit biases are not process-pure (see O'Connor, Lopez-Vergara, & Colder, 2012). fMRI has also been used to study neural correlates of RT measures of memory bias (see Ames et al., 2014), and electroencephalographic (EEG) measures have been used to evaluate neurocognitive correlates of measures of automatic action tendencies and their relation to drinking escalation (Korucuoglu, Gladwin, & Wiers, 2014, 2016). Advances in measures of attentional bias include the integration of eye-tracking technology with extant attentional bias measures (e.g., visual probe tasks).

    • Alcohol and violent behavior among football spectators: An empirical assessment of Brazilian's criminalization

      2017, International Journal of Law, Crime and Justice
      Citation Excerpt :

      Behaviorists also find support in neuroscience. The anger arousal present in football riots, crowd disturbance and supporter fights with the police and with rivalry club's fans, it is positively associated to the experience of approach rather than withdrawal motivation from the stimulus in the anterior asymmetry of cerebral hemispheres (Harmon-Jones and Allen, 1998), and negative valence tendencies such as the sense of sadness, tension and stress implies behavioral inhibition, especially in heavy drinking fans who tends to develop a protective control mechanism due the difficulty to regulate alcohol intake (Korucuoglu et al., 2016). Thus, from both behaviorism and neuroscience arguments, it seems difficult to accept that the tension reduction induced by alcohol intake would be a crucial determinant for collective aggression by fans.

    View all citing articles on Scopus
    1

    Present address: Department of Psychological Sciences, University of Missouri, Columbia, MO 65211, USA.

    View full text