Skip to main content
Log in

Motor cortex excitability correlates with novelty seeking in social anxiety: a transcranial magnetic stimulation investigation

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Social anxiety disorder (SAD) is characterised by fear of scrutiny by other people, avoidance of social situations and vegetative/motor symptomatology. The correlation between reduced striatal dopaminergic (DA) function, SAD motor symptoms and the high occurrence of SAD in patients with Parkinson’s disease (PD), suggests a link between SAD and movement diseases caused by dopamine dysfunction. However, little is known about the electrophysiological aspects of SAD. We applied single- and paired-pulse transcranial magnetic stimulation (TMS) to investigate excitatory and inhibitory mechanisms of the primary motor cortex (M1) in 15 SAD patients and the relationship between these neurophysiological measures and clinical symptoms or temperamental traits. Data were compared with those obtained in 15 age- and sex-matched healthy volunteers. SAD patients showed significantly higher harm avoidance scores and lower novelty seeking scores when compared to controls. TMS measures did not significantly differ between groups. However, in SAD patients the cortical silent period (CSP) duration and the amount of long-interstimulus interval intracortical inhibition were significantly correlated with the NS score. Accordingly with NS reduction and CSP shortening reported in PD, the relationship between NS levels and the excitability of inhibitory circuits of the M1 may support the hypothesis that DA dysfunction could underlie NS deficits in SAD. Furthermore, these data suggest that "trait variables" (i.e., NS) are more closely related to neurophysiological measures than SAD symptoms, which represent “state variables” linked to social performance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Ruscio AM, Brown TA, Chiu WT, Sareen J, Stein MB, Kessler RC (2008) Social fears and social phobia in the USA: results from the National Comorbidity Survey Replication. Psychol Med 35:15–28

    Google Scholar 

  2. Burke KC, Burke JD Jr, Regier DA, Rae DS (1990) Age at onset of selected mental disorders in five community populations. Arch Gen Psychiatry 47(6):511–518

    CAS  PubMed  Google Scholar 

  3. Stein MB (1996) How shy is too shy? Lancet 347:1131–1132

    Article  CAS  PubMed  Google Scholar 

  4. Schneier FR (2006) Clinical practice. Social anxiety disorder. N Engl J Med 355:1029–1036

    Article  CAS  PubMed  Google Scholar 

  5. Amir N, Beard C, Przeworski A (2005) Resolving ambiguity: the effect of experience on interpretation of ambiguous events in generalized social phobia. J Abnorm Psychol 114(3):402–408

    Article  PubMed  Google Scholar 

  6. Liebowitz MR (1987) Social phobia. In: Klein DF (ed) Modern problems in pharmacopsychiatry: anxiety. Switzerland, Karger, pp 141–173

    Google Scholar 

  7. Schneier FR, Liebowitz MR, Abi-Dargham A, Zea-Ponce Y, Lin SH, Laruelle M (2000) Low dopamine D2 receptor binding potential in social phobia. Am J Psychiatry 157:457–459

    Article  CAS  PubMed  Google Scholar 

  8. Tiihonen J, Kuikka J, Bergstrom K, Lepola U, Koponen H, Leinonen E (1997) Dopamine reuptake site densities in patients with social phobia. Am J Psychiatry 154:239–242

    CAS  PubMed  Google Scholar 

  9. Stein MB, Heuser IJ, Juncos JL, Uhde TW (1990) Anxiety disorders in patients with Parkinson’s disease. Am J Psychiatry 147:217–220

    CAS  PubMed  Google Scholar 

  10. Hallett M (2000) Transcranial magnetic stimulation and the human brain. Nature 406:147–150

    Article  CAS  PubMed  Google Scholar 

  11. Tassinari CA, Cincotta M, Zaccara G, Michelucci R (2003) Transcranial magnetic stimulation and epilepsy. Clin Neurophysiol 114:777–798

    Article  PubMed  Google Scholar 

  12. Lefaucheur JP (2005) Motor cortex stimulation for Parkinson’s disease and dystonia: lessons from transcranial magnetic stimulation? A review of the literature. Rev Neurol (Paris) 161(1):27–41

    Google Scholar 

  13. Cantello R, Tarletti R, Civardi C (2002) Transcranial magnetic stimulation and Parkinson’s disease. Brain Res Brain Res Rev 38:309–327

    Article  PubMed  Google Scholar 

  14. Davidson RJ, Jackson DC, Larson CL (2000) Human electroencephalography. In: Cacioppo JT, Tassinary LG, Bernston GG (eds) Principles of psychophysiology, 2nd edn. Cambridge University Press, New York, pp 27–52

    Google Scholar 

  15. Crost NW, Pauls CA, Wacker J (2008) Defensiveness and anxiety predict frontal EEG asymmetry only in specific situational contexts. Biol Psychol 78(1):43–52

    Article  PubMed  Google Scholar 

  16. Wassermann EM, Greenberg BD, Nguyen MB, Murphy DL (2001) Motor cortex excitability correlates with an anxiety-related personality trait. Biol Psychiatry 50(5):377–382

    Article  CAS  PubMed  Google Scholar 

  17. Oathes DJ, Bruce JM, Nitschke JB (2008) Worry facilitates corticospinal motor response to transcranial magnetic stimulation. Depress Anxiety 25(11):969–976

    Article  PubMed  Google Scholar 

  18. Sachs G, Anderer P, Dantendorfer K, Saletu B (2004) EEG mapping in patients with social phobia. Psychiatry Res 131(3):237–247

    Article  PubMed  Google Scholar 

  19. Liebowitz MR (1987) Social phobia. Mod Probl Pharmacopsychiatry 22:141–173

    CAS  PubMed  Google Scholar 

  20. Cloninger CR (1994) The temperament and character inventory (TCI): a guide to its development and use. Center for Psychobiology of Personality, St. Louis

    Google Scholar 

  21. Cloninger CR, Adolfsson R, Svrakic NM (1996) Mapping genes for human personality. Nat Genet 12:3–4

    Article  CAS  PubMed  Google Scholar 

  22. Rossi S, De Capua A, Tavanti M, Calossi S, Polizzotto NR, Mantovani A, Falzarano V, Bossini L, Passero S, Bartalini S, Ulivelli M (2009) Dysfunctions of cortical excitability in drug-naïve posttraumatic stress disorder patients. Biol Psychiatry 66:54–61

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  24. Garvey MA, Ziemann U, Becker DA, Barker CA, Bartko JJ (2001) New graphical method to measure silent periods evoked by transcranial magnetic stimulation. Clin Neurophysiol 112:1451–1460

    Article  CAS  PubMed  Google Scholar 

  25. Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol (Lond.) 471:501–519

    CAS  Google Scholar 

  26. Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J (1999) Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol (Lond.) 517:591–597

    Article  CAS  Google Scholar 

  27. Inghilleri M, Berardelli A, Cruccu G, Manfredi M (1993) Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol 466:521–534

    CAS  PubMed  Google Scholar 

  28. Rossini PM, Rossi S (1998) Clinical applications of motor evoked potentials. Electroencephalogr Clin Neurophysiol 106:180–194

    Article  CAS  PubMed  Google Scholar 

  29. Cincotta M, Borgheresi A, Gambetti C, Balestrieri F, Rossi L, Zaccara G, Ulivelli M, Rossi S, Civardi C, Cantello R (2003) Suprathreshold 0.3 Hz repetitive TMS prolongs the cortical silent period: potential implications for therapeutic trials in epilepsy. Clin Neurophysiol 114:1827–1833

    Article  CAS  PubMed  Google Scholar 

  30. Siebner HR, Dressnandt J, Auer C, Conrad B (1998) Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve 21(9):1209–1212

    Article  CAS  PubMed  Google Scholar 

  31. Argyropoulos SV, Bell CJ, Nutt DJ (2001) Brain function in social anxiety disorder. Psychiatr Clin North Am 24(4):707–722

    Article  CAS  PubMed  Google Scholar 

  32. Cloninger CR (1987) A systematic method for clinical description and classification of personality variants. Arch Gen Psychiatry 44:573–588

    CAS  PubMed  Google Scholar 

  33. Benjamin J, Osher Y, Kotler M, Gritsenko I, Nemanov L, Belmaker RH, Ebstein RP (2000) Association between tridimensional personality questionnaire (TPQ) traits and three functional polymorphisms: dopamine receptor D4 (DRD4), serotonin transporter promoter region (5-HTTLPR) and catechol O-methyltransferase (COMT). Mol Psychiatry 5(1):96–100

    Article  CAS  PubMed  Google Scholar 

  34. Netter P, Henning J, Roed IS (1996) Serotonin and dopamine as mediators of sensation seeking behavior. Neurpsychobiology 34:155–165

    Article  CAS  Google Scholar 

  35. Zuckerman M (1994) In: Zuckerman M (ed) Behavioral expressions and biosocial bases of sensation seeking. Cambridge University Press, New York

    Google Scholar 

  36. Suhara T, Yasuno F, Sudo Y, Yamamoto M, Inoue M, Okubo Y, Suzuki K (2001) Dopamine D2 receptors in the insular cortex and the personality trait of novelty seeking. Neuroimage 13:891–895

    Article  CAS  PubMed  Google Scholar 

  37. Cantello R, Gianelli M, Bettucci D, Civardi C, De Angelis MS, Mutani R (1991) Parkinson’s disease rigidity: magnetic motor evoked potentials in a small hand muscle. Neurology 41(9):1449–1456

    CAS  PubMed  Google Scholar 

  38. Priori A, Berardelli A, Inghilleri M, Accornero N, Manfredi M (1994) Motor cortical inhibition and the dopaminergic system. Pharmacological changes in the silent period after transcranial brain stimulation in normal subjects, patients with Parkinson’s disease and drug induced Parkinsonism. Brain 117(Pt2):317–323

    Article  PubMed  Google Scholar 

  39. Valls-Solé J, Pascual-Leone A, Brasil-Neto JP, Cammarota A, McShane L, Hallett M (1994) Abnormal facilitation of the response to transcranial magnetic stimulation in patients with Parkinson’s disease. Neurology 44(4):735–741

    PubMed  Google Scholar 

  40. Berardelli A, Inghilleri M, Priori A, Marchetti P, Curra A, Rona S, Manfredi M (1996) Inhibitory cortical phenomena studied with the technique of transcranial stimulation. Electroencephalogr Clin Neurophysiol Suppl 46:343–349

    CAS  PubMed  Google Scholar 

  41. Pierantozzi M, Palmieri MG, Marciani MG, Bernardi G, Giacomini P, Stanzione P (2001) Effect of apomorphine on cortical inhibition in Parkinson’s disease patients: a transcranial magnetic stimulation study. Exp Brain Res 141(1):52–62

    Article  CAS  PubMed  Google Scholar 

  42. Robol E, Fiaschi A, Manganotti P (2004) Effects of citalopram on the excitability of the human motor cortex: a paired magnetic stimulation study. J Neurol Sci 221(1–2):41–46

    Article  CAS  PubMed  Google Scholar 

  43. Manganotti P, Bortolomasi M, Zanette G, Pawelzik T, Giacopuzzi M, Fiaschi A (2001) Intravenous clomipramine decreases excitability of human motor cortex. A study with paired magnetic stimulation. J Neurol Sci 184(1):27–32

    Article  CAS  PubMed  Google Scholar 

  44. Cornwell BR, Johnson L, Berardi L, Grillon C (2006) Anticipation of public speaking in virtual reality reveals a relationship between trait social anxiety and startle reactivity. Biol Psychiatry 59(7):664–666

    Article  PubMed  Google Scholar 

  45. Kimiskidis VK, Papagiannopoulos S, Sotirakoglou K, Kazis DA, Kazis A, Mills KR (2005) Silent period to transcranial magnetic stimulation: construction and properties of stimulus–response curves in healthy volunteers. Exp Brain Res 163(1):21–31

    Article  CAS  PubMed  Google Scholar 

  46. Strafella AP, Paus T, Barrett J, Dagher A (2001) Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J Neurosci. 21(15):RC157

    Google Scholar 

Download references

Acknowledgments

The authors acknowledge Dr Antonio Mantovani, MD, PhD Associate Research Scientist Department of Psychiatry, Division of Brain Stimulation and Therapeutic Modulation, New York State Psychiatric Institute 1051 Riverside Drive. The Unit of Neurology of the Florence Health Authority was supported by a grant from ‘Ente Cassa di Risparmio di Firenze’, Florence, Italy. The Clinical NeuroSciences Onlus (Florence, Italy) supported the clinical data collection and management.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stefano Pallanti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pallanti, S., Borgheresi, A., Pampaloni, I. et al. Motor cortex excitability correlates with novelty seeking in social anxiety: a transcranial magnetic stimulation investigation. J Neurol 257, 1362–1368 (2010). https://doi.org/10.1007/s00415-010-5533-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-010-5533-4

Keywords

Navigation