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When defeat leaves a bad taste in the mouth: Modulation of tongue corticobulbar output during monetary loss in a gambling task

  • Carmelo M. Vicario
    Correspondence
    Corresponding author.
    Affiliations
    Department of Cognitive Sciences, Psychology, Education and Cultural Studies, University of Messina, 98122, Messina, Italy
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  • Sonia Turrini
    Affiliations
    Center for Studies and Research in Cognitive Neuroscience, Department of Psychology “Renzo Canestrari”, Alma Mater Studiorum Università di Bologna, Cesena Campus, 47521, Cesena, Italy
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  • Chiara Lucifora
    Affiliations
    Institute of Technologies and Cognitive Sciences (ISTC-CNR), 00185, Rome, Italy
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  • Laura Culicetto
    Affiliations
    Department of Cognitive Sciences, Psychology, Education and Cultural Studies, University of Messina, 98122, Messina, Italy
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  • Francesca Ferraioli
    Affiliations
    Department of Cognitive Sciences, Psychology, Education and Cultural Studies, University of Messina, 98122, Messina, Italy
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  • Alessandra Falzone
    Affiliations
    Department of Cognitive Sciences, Psychology, Education and Cultural Studies, University of Messina, 98122, Messina, Italy
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  • Michael A. Nitsche
    Affiliations
    Department of Psychology and Neurosciences, Leibniz Research Centre for Working Environment and Human Factors, 44139, Dortmund, Germany
    Bielefeld University, University Hospital OWL, Protestant Hospital of Bethel Foundation, University Clinic of Psychiatry and Psychotherapy and University Clinic of Child and Adolescent Psychiatry and Psychotherapy, 33617, Bielefeld, Germany
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  • Alessio Avenanti
    Affiliations
    Center for Studies and Research in Cognitive Neuroscience, Department of Psychology “Renzo Canestrari”, Alma Mater Studiorum Università di Bologna, Cesena Campus, 47521 Cesena, Italy
    Neuropsicology and Cognitive Neuroscience Research Center (CINPSI Neurocog), Universidad Católica Del Maule, 3460000 Talca, Chile
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Open AccessPublished:October 31, 2022DOI:https://doi.org/10.1016/j.brs.2022.10.010
      The tongue is a crucial effector involved in most everyday behaviors. Due to its complex nature (i.e., as a muscle and somatosensory/gustatory organ) the tongue is endowed with a multifunctional integration capacity that makes it an unique and important actor for survival. Neurons of the cortical representation of the tongue within the primary motor cortex (tnM1) show a specific pattern of connectivity with cortical and subcortical regions involved in reward processing [
      • Bono D.
      • Belyk M.
      • Longo M.R.
      • Dick F.
      Beyond language: the unspoken sensory-motor representation of the tongue in non-primates, non-human and human primates.
      ,
      • Alipour M.
      • Chen Y.
      • Jürgens U.
      Anterograde projections of the motorcortical tongue area in the saddle-back tamarin (Saguinus fuscicollis).
      ], suggesting a role of tnM1 neurons in processing reward-related stimuli/outcomes and internal (physiological and mental) states [
      • Vicario C.M.
      • Nitsche M.A.
      • Avenanti A.
      Tongue motor cortex: the back door of the reward system.
      ,
      • Vicario C.M.
      • Komeilipoor N.
      • Cesari P.
      • Rafal R.D.
      • Nitsche M.A.
      Enhanced corticobulbar excitability in chronic smokers during visual exposure to cigarette smoking cues.
      ]. In line with this, we have previously shown that visual stimuli representing core disgust and social signs of disgust (i.e., rotten food and distasted faces) reduce corticobulbar excitability of the human tnM1, as measured via motor-evoked potentials (MEPs) induced by tnM1 transcranial magnetic stimulation (TMS) [
      • Vicario C.M.
      • Rafal R.D.
      • Borgomaneri S.
      • Paracampo R.
      • Kritikos A.
      • Avenanti A.
      Pictures of disgusting foods and disgusted facial expressions suppress the tongue motor cortex.
      ]. Similar findings of reduced tnM1 corticobulbar motor outputs were found when participants were exposed to social scenarios eliciting indignation for moral violations [
      • Vicario C.M.
      • Rafal R.D.
      • di Pellegrino G.
      • Lucifora C.
      • Salehinejad M.A.
      • Nitsche M.A.
      • Avenanti A.
      Indignation for moral violations suppresses the tongue motor cortex: preliminary TMS evidence.
      ], suggesting shared mechanisms underly core, social and moral disgust [
      • Vicario C.M.
      • Rafal R.D.
      • Martino D.
      • Avenanti A.
      Core, social and moral disgust are bounded: a review on behavioral and neural bases of repugnance in clinical disorders.
      ]. Furthermore, we have recently shown that tnM1 downregulation via transcranial direct current stimulation (tDCS) reduces hunger in healthy humans [
      • Vicario C.M.
      • Salehinejad M.A.
      • Mosayebi-Samani M.
      • Maezawa H.
      • Avenanti A.
      • Nitsche M.A.
      Transcranial direct current stimulation over the tongue motor cortex reduces appetite in healthy humans.
      ]. All this work suggests a relevance of tnM1 for appetitive and defensive motivational systems. Yet, whether this role is generally relevant for experiences along the reward-punishing continuum, or rather exquisitely associated with oral dimensions, is still unclear.
      To address this issue, we administered TMS of the tnM1 in healthy volunteers undergoing an established gambling protocol [
      • Vicario C.M.
      • Rafal R.D.
      • Avenanti A.
      Counterfactual thinking affects the excitability of the motor cortex.
      ], to investigate whether reward-related experiences associated with monetary win and loss induce consistent modulations of tnM1 corticobulbar excitability (Fig. S1). Eleven participants (5 males, age mean 24.45 year, SD 3.74) performed 96 trials (48 trials per muscle) and were asked to guess which one of two keys on a keyboard would be rewarded with a monetary win. Upon key pression, participants were presented with one of the following outcomes: in 16 trials (win trials) banknotes associated with the sentence “You win” were presented; in 16 trials (lose trials) banknotes associated with the sentence “You lost” were presented; in 16 trials (neutral trials) scrambled banknotes without any win/loss outcome were presented. After the feedback presentation, we recorded MEPs from the tongue and the extensor carpi radialis (ERC) muscles. Thus, 16 MEPs per muscle and condition were obtained and stored for offline analysis (for details see the Supplemental Materials). The experimental procedures were approved by the local ethics committee at the University of Bologna and were carried out in accordance with the principles of the 1964 Helsinki Declaration.
      MEPs were log-transformed to reduce skewness, averaged for each muscle and condition, and then submitted to an ANOVA with the within-subjects factors Monetary outcome (win, lose, neutral) and Muscle (tongue, ECR). In line with our previous findings [
      • Vicario C.M.
      • Rafal R.D.
      • Avenanti A.
      Counterfactual thinking affects the excitability of the motor cortex.
      ] showing higher corticospinal excitability following a monetary loss, we found a significant main effect of Monetary outcome (F2,20 = 9.35, p = 0.001, ηp2 = 0.48), with higher MEPs following a loss (mean raw MEP amplitude in mV ± standard deviation: 1.39 ± 0.48) compared to the win (1.25 ± 0.42; p = 0.001, Cohen's d = 1.42) and neutral (1.27 ± 0.43; p = 0.023, d = 0.97) outcomes, which in turn did not differ from one each other (p = 0.40). The main effect of the factor Muscle (F1,10 = 2.44, p = 0.15, ηp2 = 0.20) or the Muscle x Monetary Outcome interaction (F2,20 = 0.39, p = 0.69, ηp2 = 0.04) were not significant (Fig. 1).
      Fig. 1
      Fig. 1A. The main effect of the gambling task monetary outcome showed an overall larger MEPs response when a loss outcome followed the choice, compared to the win and the neutral (no win/no loss) conditions. Asterisks indicate significant results of the pairwise comparisons: ∗p ≤ 0.05, ∗∗p ≤ 0.005. Vertical bars denote standard errors. B./C. Violin plots of single-trial MEPs from the tongue and ECR muscles across individuals.
      Stepwise regression analyses between emotional (i.e., happiness, anger, fear, disgust, regret, disappointment) ratings (measured via visual analogue scale) associated with the three monetary outcomes (see caption to Fig. S1 for details on data collection) and the respective MEP amplitudes revealed a significant model for loss trials (R2adj = 0.64, F1,9 = 18.64, p = 0.002) showing a strong negative relation (β = −0.82, p = 0.002; f2 = 2.07; Fig. S2) between regret rating and tongue MEP amplitudes. No further significant results were found (see Table S1) and the relation between regret and MEPs remained specific for tongue when contrasting tongue (β = −0.79, p = 0.005, f2 = 1.68) and ECR MEPs (β = −0.09, p = 0.67, f2 < 0.01).
      The present findings support and expand our previous work [
      • Vicario C.M.
      • Rafal R.D.
      • Avenanti A.
      Counterfactual thinking affects the excitability of the motor cortex.
      ] by showing that when participants are active agents of monetary loss in a gambling task (but not when they passively observe monetary outcomes [
      • Vicario C.M.
      • Rafal R.D.
      • Avenanti A.
      Counterfactual thinking affects the excitability of the motor cortex.
      ]), corticospinal excitability (ECR) and corticobulbar excitability (tongue) are increased. This points to a link between negative emotions, sense of responsibility, and functional modulation of the motor cortex [
      • Vicario C.M.
      • Rafal R.D.
      • Avenanti A.
      Counterfactual thinking affects the excitability of the motor cortex.
      ]. We also provide preliminary evidence that tnM1 excitability during loss trials predicts the experience of regret – an emotion arising from counterfactual thinking of what would have happened had participants made a different choice. The negative relation between regret ratings and tnM1 excitability suggests a mapping of specific aspects of the experience of monetary loss.
      The increased excitability of tnM1 in response to monetary loss, which was independent of the specific muscle representation, might reflect generalized action monitoring processes activated by an “erroneous” decision carrying negative consequences in the gambling task and is associated with widespread activation of mediofrontal and motor cortices [
      • van Schie H.T.
      • Mars R.B.
      • Coles M.G.
      • Bekkering H.
      Modulation of activity in medial frontal and motor cortices during error observation.
      ], leading to enhanced MEPs from the two target muscles. Motor response was variable across individuals (Fig. 1B and C) and associated with affective self-reported ratings (Fig. S2). While our study cannot clarify directly whether aspects of the subjective experience of monetary loss contributed to enhanced corticospinal or corticobulbar excitability, our findings suggest nevertheless that the tnM1 excitability enhancement due to monetary loss tends to attenuate in participants who experience larger regret as a result of their choice. This tongue-specific attenuation might reflect aversion towards the negative monetary outcome associated with retrospective counterfactual thinking and might derive from a pattern of neural connectivity between tnM1 and the anterior cingulate-insular cortex network [
      • Bono D.
      • Belyk M.
      • Longo M.R.
      • Dick F.
      Beyond language: the unspoken sensory-motor representation of the tongue in non-primates, non-human and human primates.
      ,
      • Alipour M.
      • Chen Y.
      • Jürgens U.
      Anterograde projections of the motorcortical tongue area in the saddle-back tamarin (Saguinus fuscicollis).
      ,
      • Vicario C.M.
      • Nitsche M.A.
      • Avenanti A.
      Tongue motor cortex: the back door of the reward system.
      ], which is known to be involved in aversion processing [
      • Vicario C.M.
      • Rafal R.D.
      • Martino D.
      • Avenanti A.
      Core, social and moral disgust are bounded: a review on behavioral and neural bases of repugnance in clinical disorders.
      ]. This interpretation is also in line with prior work [
      • Vicario C.M.
      • Rafal R.D.
      • Borgomaneri S.
      • Paracampo R.
      • Kritikos A.
      • Avenanti A.
      Pictures of disgusting foods and disgusted facial expressions suppress the tongue motor cortex.
      ,
      • Vicario C.M.
      • Rafal R.D.
      • di Pellegrino G.
      • Lucifora C.
      • Salehinejad M.A.
      • Nitsche M.A.
      • Avenanti A.
      Indignation for moral violations suppresses the tongue motor cortex: preliminary TMS evidence.
      ] showing that perceiving aversion in response to pictures of rotten foods or moral violations was associated with reduction of tnM1 corticobulbar excitability. The expression “defeat leaves a bad taste in the mouth” may be more than a metaphor when describing the experience of regret, an aversive state perceived by individuals for their wrong choices or when they have failed to achieve a goal.

      Funding

      C.M.V. is supported by Bial Foundation (protocol number 160/18); A.A is supported by Bial Foundation (347/18), Fondazione del Monte di Bologna e Ravenna (1402bis/2021) and Ministero Istruzione Università e Ricerca (2017N7WCLP). M.A.N. is supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation)—Project Number 316803389—SFB 1280, project A6.

      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.

      Appendix A. Supplementary data

      The following is the Supplementary data to this article:

      References

        • Bono D.
        • Belyk M.
        • Longo M.R.
        • Dick F.
        Beyond language: the unspoken sensory-motor representation of the tongue in non-primates, non-human and human primates.
        Neurosci Biobehav Rev. 2022 Aug; 139: 104730
        • Alipour M.
        • Chen Y.
        • Jürgens U.
        Anterograde projections of the motorcortical tongue area in the saddle-back tamarin (Saguinus fuscicollis).
        Brain Behav Evol. 2002; 60: 101-116
        • Vicario C.M.
        • Nitsche M.A.
        • Avenanti A.
        Tongue motor cortex: the back door of the reward system.
        Neurosci Biobehav Rev. 2022 Aug 6; 141: 104820
        • Vicario C.M.
        • Komeilipoor N.
        • Cesari P.
        • Rafal R.D.
        • Nitsche M.A.
        Enhanced corticobulbar excitability in chronic smokers during visual exposure to cigarette smoking cues.
        J Psychiatry Neurosci. 2014 Jul; 39: 232-238
        • Vicario C.M.
        • Rafal R.D.
        • Borgomaneri S.
        • Paracampo R.
        • Kritikos A.
        • Avenanti A.
        Pictures of disgusting foods and disgusted facial expressions suppress the tongue motor cortex.
        Soc Cognit Affect Neurosci. 2017 Feb 1; 12: 352-362
        • Vicario C.M.
        • Rafal R.D.
        • di Pellegrino G.
        • Lucifora C.
        • Salehinejad M.A.
        • Nitsche M.A.
        • Avenanti A.
        Indignation for moral violations suppresses the tongue motor cortex: preliminary TMS evidence.
        Soc Cognit Affect Neurosci. 2022 Feb 3; 17: 151-159
        • Vicario C.M.
        • Rafal R.D.
        • Martino D.
        • Avenanti A.
        Core, social and moral disgust are bounded: a review on behavioral and neural bases of repugnance in clinical disorders.
        Neurosci Biobehav Rev. 2017 Sep; 80: 185-200
        • Vicario C.M.
        • Salehinejad M.A.
        • Mosayebi-Samani M.
        • Maezawa H.
        • Avenanti A.
        • Nitsche M.A.
        Transcranial direct current stimulation over the tongue motor cortex reduces appetite in healthy humans.
        Brain Stimul. 2020 Jul-Aug; 13: 1121-1123
        • Vicario C.M.
        • Rafal R.D.
        • Avenanti A.
        Counterfactual thinking affects the excitability of the motor cortex.
        Cortex. 2015 Apr; 65: 139-148
        • van Schie H.T.
        • Mars R.B.
        • Coles M.G.
        • Bekkering H.
        Modulation of activity in medial frontal and motor cortices during error observation.
        Nat Neurosci. 2004 May; 7: 549-554