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Influence of the supplementary motor area on primary motor cortex excitability during movements triggered by neutral or emotionally unpleasant visual cues

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Abstract

The stronger anatomo-functional connections of the supplementary motor area (SMA), as compared with premotor area (PM), with regions of the limbic system, suggest that SMA could play a role in the control of movements triggered by visual stimuli with emotional content. We addressed this issue by analysing the modifications of the excitability of the primary motor area (M1) in a group of seven healthy subjects, studied with transcranial magnetic stimulation (TMS), after conditioning TMS of SMA, during emotional and non-emotional visually cued movements. Conditioning TMS of the PM or of contralateral primary motor cortex (cM1) were tested as control conditions. Single-pulse TMS over the left M1 was randomly intermingled with paired TMS, in which a conditioning stimulation of the left SMA, left PM or right M1 preceded test stimulation over the left M1. The subjects carried out movements in response to computerised visual cues (neutral pictures and pictures with negative emotional content). The amplitudes of motor-evoked potentials (MEPs) recorded from the right first dorsal interosseous muscle after paired TMS were measured and compared with those obtained after single-pulse TMS of the left M1 under the various experimental conditions. Conditioning TMS of the SMA in the paired-pulse paradigm selectively enhanced MEP amplitudes in the visual-emotional triggered movement condition, compared with single-pulse TMS of M1 alone or with paired TMS during presentation of neutral visual cues. On the other hand, conditioning TMS of the PM or cM1 did not differentially influence MEP amplitudes under visual-emotional triggered movement conditions. This pattern of effects was related to the intensity of the conditioning TMS over the SMA, being most evident with intensities ranging from 110% to 80% of motor threshold. These results suggest that the SMA in humans could interface the limbic and the motor systems in the transformation of emotional experiences into motor actions.

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References

  • Ball T, Schreiber A, Feige B, Wagner M, Lucking CH, Kristeva-Feige R (1999) The role of higher-order motor areas in voluntary movement as revealed by high-resolution EEG and fMRI. Neuroimage 10:682–694

    CAS  PubMed  Google Scholar 

  • Brasil-Neto JP, Cohen LG, Panizza M, Nilsson J, Roth BJ, Hallett M (1992). Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse, and stimulus intensity. J Clin Neurophysiol 9:132–136

    CAS  PubMed  Google Scholar 

  • Caltagirone C, Zoccolotti P, Originale G, Daniele A, Mammuccari A (1989) Autonomic reactivity and facial expression of emotion in brain-damaged patients. In: Caltagirone C, Gainotti G (eds) Emotions and the dual brain. Springer-Verlag, Berlin Heidelberg New York, pp 204–221

  • Carretie L, Iglesias J, Garcia T, Ballesteros M (1997) N300, P300 and the emotional processing of visual stimuli. Electroencephalogr Clin Neurophysiol 103:298–303

    Article  CAS  PubMed  Google Scholar 

  • Chen DF, Hyland B, Maier V, Palmeri A, Wiesendanger M (1991) Comparison of neural activity in the supplementary motor area and in the primary motor cortex in monkeys. Somatosens Mot Res 8:27–44

    CAS  PubMed  Google Scholar 

  • Civardi C, Cantello R, Asselman P, Rothwell JC (2001) Transcranial magnetic stimulation can be used to test connections to primary motor areas from frontal and medial cortex in humans. Neuroimage 14:1444–1453

    Article  CAS  PubMed  Google Scholar 

  • Cuthbert BN, Schupp HT, Bradley MM, Birbaumer N, Lang PJ (2000) Brain potentials in affective picture processing: covariation with autonomic arousal and affective report. Biol Psychol 52:95–111

    Article  CAS  PubMed  Google Scholar 

  • Damasio AR (1994) Descarte's error: emotion, reason, and the human brain. New York, Grosset/Putnam.

  • Damasio AR (1995) On some functions of the human prefrontal cortex. Ann N Y Acad Sci 769:241–251

    CAS  PubMed  Google Scholar 

  • Damasio AR (1997) Towards a neuropathology of emotion and mood. Nature 386:769–770

    CAS  PubMed  Google Scholar 

  • Day BL, Dressler D, Maertens de Noordhout A, Marsden CD, Nakashima K, Rothwell JC, et al. (1988) Differential effect of cutaneous stimuli on responses to electrical or magnetic stimulation of human brain. J Physiol (Lond) 399:68P

    Google Scholar 

  • Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118:279–306

    PubMed  Google Scholar 

  • Filippi MM, Oliveri M, Vernieri F, Pasqualetti P, Rossini PM (2000) Are autonomic signals influencing cortico-spinal motor excitability? A study with transcranial magnetic stimulation. Brain Res 881:159–164

    Article  CAS  PubMed  Google Scholar 

  • Fox P, Ingham R, George MS, Mayberg H, Ingham J, Roby J, Martin C, Jerabek P (1997) Imaging human intra-cerebral connectivity by PET during TMS. Neuroreport 8:2787–2791

    CAS  PubMed  Google Scholar 

  • George MS, Ketter T, Parekh P, Horwitz B, Herscovitch P, Post R (1995) Brain activity during transient sadness and happiness in healthy women. Am J Psychiatry 152:341–351

    CAS  PubMed  Google Scholar 

  • Gerschlager W, Siebner HR, Rothwell JC (2001) Decreased corticospinal excitability after subthreshold 1-Hz rTMS over lateral premotor cortex. Neurology 57:449–455

    CAS  PubMed  Google Scholar 

  • Goldberg G (1985) Supplementary motor area structure and function: review and hypotheses. Behav Brain Sci 8:567–616

    Google Scholar 

  • Hyman SE (1998) A new image for fear and emotion. Nature 393:417–418

    Article  CAS  PubMed  Google Scholar 

  • Ilmoniemi RJ, Virtanen J, Ruohonen J, Karhu J, Aronen HJ, Naatanen R, Katila T (1997) Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport 8:3537–3540

    CAS  PubMed  Google Scholar 

  • Lane RD, Reimann EM, Ahern GL, Schwartz GE, Davidson RJ (1997a) Neuroanatomical correlates of happiness, sadness, and disgust. Am J Psychiatry 154:926–933

    CAS  PubMed  Google Scholar 

  • Lane RD, Reimann EM, Bradley M, Lang PJ, Ahern GL, Davidson RJ, Schwartz GE (1997b) Neuroanatomical correlates of pleasant and unpleasant emotion. Neuropsychologia 35:1437–1444

    Article  CAS  PubMed  Google Scholar 

  • LeDoux J (1987) Emotion. In: Plum F (ed) Handbook of physiology. American Psychological Society, Bethesda, Md, pp 419–460

  • Luppino G, Matelli M, Camarda R, Rizzolatti G (1993) Corticortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J Comp Neurol 338:114–140

    CAS  PubMed  Google Scholar 

  • Mariorenzi R, Zarola F, Caramia MD, Paradiso C, Rossini PM (1991) Non-invasive evaluation of central motor tract excitability changes following peripheral nerve stimulation in healthy humans. Electroencephalogr Clin Neurophysiol 81:90–101

    CAS  PubMed  Google Scholar 

  • Morecraft RJ, Van Hoesen GW (1992) Cinglulate input to the primary and supplementary motor cortices in the rhesus monkey: evidence for somatotopy in areas 24c and 23c. J Comp Neurol 322:471–489

    CAS  PubMed  Google Scholar 

  • Morecraft RJ, Van Hoesen GW (1998) Convergence of limbic input to the cingulate motor cortex in the rhesus monkey. Brain Res Bull 45:209–232

    Article  CAS  PubMed  Google Scholar 

  • Munchau A, Bloem BR, Irlbacher K, Trimble MR, Rothwell JC (2002) Functional connectivity of human premotor and motor cortex explored with repetitive transcranial magnetic stimulation. J Neurosci 22:554–561

    CAS  PubMed  Google Scholar 

  • Muri RM, Rivaud S, Vermersch AI, Leger JM, Pierrot-Deseilligny C (1995) Effects of transcranial magnetic stimulation over the region of the supplementary motor area during sequences of memory-guided saccades. Exp Brain Res 104:163–166

    CAS  PubMed  Google Scholar 

  • Netz J (1999) Asymmetry in transcallosal inhibition. Electroencephalogr Clin Neurophysiol Suppl 51:137–144

    CAS  PubMed  Google Scholar 

  • Northoff G, Richter A, Gessner M, Schlagenhauf F, Fell J, Baumgart F, Kaulisch T, Kotter R, Stephan KE, Leschinger A, Hagner T, Bargel B, Witzel T, Hinrichs H, Bogerts B, Scheich H, Heinze HH (2000) Functional dissociation between medial and lateral prefrontal cortical spatiotemporal activation in negative and positive emotions: a combined fMRI/MEG study. Cereb Cortex 10:93–107

    Article  CAS  PubMed  Google Scholar 

  • Ohara S, Ikeda A, Kunieda T, Yazawa S, Baba K, Nagamine T, Tal W, Hashimoto N, Mihara T, Shibasaki H (2000) Movement-related change of electrocortiographic activity in the human supplementary motor area proper. Brain 123:1203–1215

    PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    CAS  PubMed  Google Scholar 

  • Paradiso S, Johnson DL, Andreasen NC, O'Leary DS, Watkins GL, Boles Ponto LL, Hichwa RD (1999) Cerebral blood flow changes associated with attribution of emotional valence to pleasant, unpleasant and neutral visual stimuli in a PET study of normal subjects. Am J Psychiatry 156:1618–1629

    CAS  PubMed  Google Scholar 

  • Reimann EM, Lane RD, Ahern G, Schwartz G, Davidson RJ, Friston KJ, Yun L, Chen K (1997) Neuroanatomical correlates of externally and internally generated emotions. Am J Psychiatry 154:918–925

    PubMed  Google Scholar 

  • Rossini PM, Zarola F, Stalberg E, Caramia M (1988) Pre-movement facilitation of motor evoked potentials in man during transcranial stimulation of the central motor pathways. Brain Res 458:20–30

    CAS  PubMed  Google Scholar 

  • Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, et al. (1994) Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 91:79–92

    CAS  PubMed  Google Scholar 

  • Schluter ND, Rushworth MF, Passingham RE, Mills KR (1998) Temporary interference in human lateral premotor cortex suggests dominance for the selection of movements: a study using transcranial magnetic stimulation. Brain 121:785–799

    PubMed  Google Scholar 

  • Spence S, Shapiro D, Zaidel E (1996) The role of the right hemisphere in the physiological and cognitive components of emotional processing. Psychophysiology 33:112–122

    CAS  PubMed  Google Scholar 

  • Starr A, Caramia M, Zarola F, Rossini PM (1988) Enhancement of motor cortical excitability in humans by non-invasive electrical stimulation appears prior to voluntary movement. Electroencephalogr Clin Neurophysiol 70:26–32

    CAS  PubMed  Google Scholar 

  • Tormos JM, Canete C, Tarazona F, Català MD, Pascual-Leone Pascual A, Pascual-Leone A (1997) Lateralized effects of self-induced sadness and happiness on corticospinal excitability. Neurology 49:487–491

    CAS  PubMed  Google Scholar 

  • Wiesendanger M, Hummelsheim H, Bianchetti M, Chen DF, Hylan B, Maier V, Wiesendanger R (1987) Input and output organization of the supplementary motor area. Ciba Found Symp 132:40–62

    CAS  PubMed  Google Scholar 

  • Ziemann U, Tergau U, Netz J, Homberg V (1997) Delay in simple reaction time after focal transcranial magnetic stimulation of the human brain occurs at the final motor output stage. Brain Res 744:32–40

    CAS  PubMed  Google Scholar 

  • Zoccolotti P, Scabini D, Violani C (1982) Electrodermal responses in patients with unilateral brain damage. J Clin Neuropsychol 4:143–150

    CAS  PubMed  Google Scholar 

  • Zoccolotti P, Caltagirone C, Benedetti N, Gainotti G (1986) Vegetative responses to emotional stimuli in unilateral brain-damaged patients. Encephale 12:263–268

    CAS  PubMed  Google Scholar 

Download references

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Oliveri, M., Babiloni, C., Filippi, M.M. et al. Influence of the supplementary motor area on primary motor cortex excitability during movements triggered by neutral or emotionally unpleasant visual cues. Exp Brain Res 149, 214–221 (2003). https://doi.org/10.1007/s00221-002-1346-8

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  • DOI: https://doi.org/10.1007/s00221-002-1346-8

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