Skip to main content
Top
Published in: Brain Structure and Function 7/2017

01-09-2017 | Original Article

Behavioral inhibition system sensitivity enhances motor cortex suppression when watching fearful body expressions

Authors: Sara Borgomaneri, Francesca Vitale, Alessio Avenanti

Published in: Brain Structure and Function | Issue 7/2017

Login to get access

Abstract

Influential theories suggest that a defensive behavioral inhibition system (BIS) supports the inhibition of action tendencies when facing potential threats. However, little is known about threat-related inhibitory mechanisms in humans and their relations to inter-individual differences in BIS sensitivity. To address this issue, we used paired-pulse TMS to investigate early human motor cortex (M1) responses to social signals of potential threats, like another’s fearful body posture. In two experiments, participants observed pictures of fearful and happy postures, and neutral postures that were either dynamic (in Exp1) or static (in Exp2). To test suppression of M1 excitatory activity, we assessed intracortical facilitation (ICF) in an early phase of threat monitoring by administering TMS pulses at 100–125 ms from picture onset. We investigated the motor representation of hand and arm muscles that are differentially involved in flexion, extension, and abduction. As a control, we also assessed corticospinal excitability and short intracortical inhibition. In both experiments, and independently of the muscle, watching fearful bodies suppressed ICF relative to watching happy and non-emotional (dynamic or static) body expressions. Remarkably, greater fear-related ICF suppression was found in participants who scored higher on a self-report questionnaire assessing BIS sensitivity. These findings suggest that observing fearful body language activates a defensive suppression of M1 excitatory activity that is influenced by the personality disposition to experience fear and anxiety when facing potential threats. This BIS-related motor suppression may have the functional role of transiently suppressing action tendencies to promote threat monitoring and, ultimately, survival.
Appendix
Available only for authorised users
Literature
go back to reference Avenanti A, Bueti D, Galati G, Aglioti SM (2005) Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain. Nat Neurosci 8:955–960. doi:10.1038/nn1481 PubMedCrossRef Avenanti A, Bueti D, Galati G, Aglioti SM (2005) Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain. Nat Neurosci 8:955–960. doi:10.​1038/​nn1481 PubMedCrossRef
go back to reference Borgomaneri S, Gazzola V, Avenanti A (2015a) Transcranial magnetic stimulation reveals two functionally distinct stages of motor cortex involvement during perception of emotional body language. Brain Struct Funct 220:2765–2781. doi:10.1007/s00429-014-0825-6 PubMedCrossRef Borgomaneri S, Gazzola V, Avenanti A (2015a) Transcranial magnetic stimulation reveals two functionally distinct stages of motor cortex involvement during perception of emotional body language. Brain Struct Funct 220:2765–2781. doi:10.​1007/​s00429-014-0825-6 PubMedCrossRef
go back to reference Chen R, Classen J, Gerloff C et al (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403PubMedCrossRef Chen R, Classen J, Gerloff C et al (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403PubMedCrossRef
go back to reference Cherbuin N, Windsor TD, Anstey KJ et al (2008) Hippocampal volume is positively associated with behavioural inhibition (BIS) in a large community-based sample of mid-life adults: the PATH through life study. Soc Cogn Affect Neurosci 3:262–269. doi:10.1093/scan/nsn018 PubMedPubMedCentralCrossRef Cherbuin N, Windsor TD, Anstey KJ et al (2008) Hippocampal volume is positively associated with behavioural inhibition (BIS) in a large community-based sample of mid-life adults: the PATH through life study. Soc Cogn Affect Neurosci 3:262–269. doi:10.​1093/​scan/​nsn018 PubMedPubMedCentralCrossRef
go back to reference Cools R, Calder AJ, Lawrence AD et al (2005) Individual differences in threat sensitivity predict serotonergic modulation of amygdala response to fearful faces. Psychopharmacology (Berl) 180:670–679. doi:10.1007/s00213-005-2215-5 CrossRef Cools R, Calder AJ, Lawrence AD et al (2005) Individual differences in threat sensitivity predict serotonergic modulation of amygdala response to fearful faces. Psychopharmacology (Berl) 180:670–679. doi:10.​1007/​s00213-005-2215-5 CrossRef
go back to reference Coombes SA, Tandonnet C, Fujiyama H et al (2009) Emotion and motor preparation: a transcranial magnetic stimulation study of corticospinal motor tract excitability. Cogn Affect Behav Neurosci 9:380–388. doi:10.3758/CABN.9.4.380 PubMedCrossRef Coombes SA, Tandonnet C, Fujiyama H et al (2009) Emotion and motor preparation: a transcranial magnetic stimulation study of corticospinal motor tract excitability. Cogn Affect Behav Neurosci 9:380–388. doi:10.​3758/​CABN.​9.​4.​380 PubMedCrossRef
go back to reference Di Lazzaro V, Oliviero A, Meglio M et al (2000) Direct demonstration of the effect of lorazepam on the excitability of the human motor cortex. Clin Neurophysiol 111:794–799PubMedCrossRef Di Lazzaro V, Oliviero A, Meglio M et al (2000) Direct demonstration of the effect of lorazepam on the excitability of the human motor cortex. Clin Neurophysiol 111:794–799PubMedCrossRef
go back to reference Fiori F, Chiappini E, Soriano M, et al (2016) Long-latency modulation of motor cortex excitability by ipsilateral posterior inferior frontal gyrus and pre-supplementary motor area. Sci Rep 6:1–11. doi:10.1038/srep38396 CrossRef Fiori F, Chiappini E, Soriano M, et al (2016) Long-latency modulation of motor cortex excitability by ipsilateral posterior inferior frontal gyrus and pre-supplementary motor area. Sci Rep 6:1–11. doi:10.​1038/​srep38396 CrossRef
go back to reference Gray JA (1987) The psychology of fear and stress. Cambridge University Press, Cambridge Gray JA (1987) The psychology of fear and stress. Cambridge University Press, Cambridge
go back to reference Gray JA (1994) Three fundamental emotion systems. In: Ekman P, Davidson RJ (eds) The nature of emotion: fundamental questions. Oxford University Press, New York, pp 243–247 Gray JA (1994) Three fundamental emotion systems. In: Ekman P, Davidson RJ (eds) The nature of emotion: fundamental questions. Oxford University Press, New York, pp 243–247
go back to reference Gray JA, McNaughton N (1996) The neuropsychology of anxiety: reprise. Nebraska Symp Motiv 43:61–134 Gray JA, McNaughton N (1996) The neuropsychology of anxiety: reprise. Nebraska Symp Motiv 43:61–134
go back to reference Grèzes J, Valabrègue R, Gholipour B, Chevallier C (2014) A direct amygdala-motor pathway for emotional displays to influence action: a diffusion tensor imaging study. Hum Brain Mapp 35:5974–5983. doi:10.1002/hbm.22598 PubMedCrossRef Grèzes J, Valabrègue R, Gholipour B, Chevallier C (2014) A direct amygdala-motor pathway for emotional displays to influence action: a diffusion tensor imaging study. Hum Brain Mapp 35:5974–5983. doi:10.​1002/​hbm.​22598 PubMedCrossRef
go back to reference Leone L, Perugini M, Bagozzi RP et al (2001) Construct validity and generalizability of the Carver—White behavioural inhibition system/behavioural activation system scales. Eur J Pers 15:373–390. doi:10.1002/per.415 CrossRef Leone L, Perugini M, Bagozzi RP et al (2001) Construct validity and generalizability of the Carver—White behavioural inhibition system/behavioural activation system scales. Eur J Pers 15:373–390. doi:10.​1002/​per.​415 CrossRef
go back to reference Li W, Zinbarg RE, Boehm SG, Paller KA (2008) Neural and behavioral evidence for affective priming from unconsciously perceived emotional facial expressions and the influence of trait anxiety. J Cogn Neurosci 20:95–107. doi:10.1162/jocn.2008.20006 PubMedCrossRef Li W, Zinbarg RE, Boehm SG, Paller KA (2008) Neural and behavioral evidence for affective priming from unconsciously perceived emotional facial expressions and the influence of trait anxiety. J Cogn Neurosci 20:95–107. doi:10.​1162/​jocn.​2008.​20006 PubMedCrossRef
go back to reference Maier MA, Hepp-Reymond MC (1995) EMG activation patterns during force production in precision grip. I. Contribution of 15 finger muscles to isometric force. Exp Brain Res 103:108–122. doi:10.1007/BF00241969 PubMedCrossRef Maier MA, Hepp-Reymond MC (1995) EMG activation patterns during force production in precision grip. I. Contribution of 15 finger muscles to isometric force. Exp Brain Res 103:108–122. doi:10.​1007/​BF00241969 PubMedCrossRef
go back to reference Oliveri M, Babiloni C, Filippi MM et al (2003) 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. doi:10.1007/s00221-002-1346-8 PubMedCrossRef Oliveri M, Babiloni C, Filippi MM et al (2003) 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. doi:10.​1007/​s00221-002-1346-8 PubMedCrossRef
go back to reference Quay HC (1988) The behavioral reward and inhibition system in childhood behavior disorder. In: Attention deficit disorder Bloomingdale LM. Spectrum, New York, pp 176–186 Quay HC (1988) The behavioral reward and inhibition system in childhood behavior disorder. In: Attention deficit disorder Bloomingdale LM. Spectrum, New York, pp 176–186
go back to reference Rossini PM, Burke D, Chen R et al (2015) Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 126:1071–1107. doi:10.1016/j.clinph.2015.02.001 PubMedCrossRef Rossini PM, Burke D, Chen R et al (2015) Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 126:1071–1107. doi:10.​1016/​j.​clinph.​2015.​02.​001 PubMedCrossRef
go back to reference Spielberger CD (1983) Manual for the state-trait anxiety inventory. Consulting Psychologist Press, Palo Alto Spielberger CD (1983) Manual for the state-trait anxiety inventory. Consulting Psychologist Press, Palo Alto
go back to reference Spielberger CD, Pedrabissi L, Santinello M (2012) STAI, State-trait anxiety inventory, Forma Y: manuale. Giunti OS, Firenze Spielberger CD, Pedrabissi L, Santinello M (2012) STAI, State-trait anxiety inventory, Forma Y: manuale. Giunti OS, Firenze
go back to reference Urban PP, Solinski M, Best C et al (2004) Different short-term modulation of cortical motor output to distal and proximal upper-limb muscles during painful sensory nerve stimulation. Muscle Nerve 29:663–669. doi:10.1002/mus.20011 PubMedCrossRef Urban PP, Solinski M, Best C et al (2004) Different short-term modulation of cortical motor output to distal and proximal upper-limb muscles during painful sensory nerve stimulation. Muscle Nerve 29:663–669. doi:10.​1002/​mus.​20011 PubMedCrossRef
go back to reference Vuilleumier P, Richardson MP, Armony JL et al (2004) Distant influences of amygdala lesion on visual cortical activation during emotional face processing. Nat Neurosci 7:1271–1278. doi:10.1038/nn1341 PubMedCrossRef Vuilleumier P, Richardson MP, Armony JL et al (2004) Distant influences of amygdala lesion on visual cortical activation during emotional face processing. Nat Neurosci 7:1271–1278. doi:10.​1038/​nn1341 PubMedCrossRef
go back to reference Whalen PJ, Rauch SL, Etcoff NL et al (1998) Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 18:411–418PubMed Whalen PJ, Rauch SL, Etcoff NL et al (1998) Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 18:411–418PubMed
Metadata
Title
Behavioral inhibition system sensitivity enhances motor cortex suppression when watching fearful body expressions
Authors
Sara Borgomaneri
Francesca Vitale
Alessio Avenanti
Publication date
01-09-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 7/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-017-1403-5

Other articles of this Issue 7/2017

Brain Structure and Function 7/2017 Go to the issue