Fear-specific enhancement of tactile perception is disrupted after amygdala lesion.


Journal

Journal of neuropsychology
ISSN: 1748-6653
Titre abrégé: J Neuropsychol
Pays: England
ID NLM: 101468753

Informations de publication

Date de publication:
03 2020
Historique:
received: 28 05 2018
revised: 13 11 2018
pubmed: 5 2 2019
medline: 16 6 2021
entrez: 5 2 2019
Statut: ppublish

Résumé

Tactile perception on one's own face is enhanced when viewing a fearful face being touched - as opposed to just approached - by fingers, compared to viewing other expressions, a phenomenon known as the emotional modulation of Visual Remapping of Touch (eVRT). This effect seems to be related to a preferential activation of the somatosensory system in response to threat. To test the contribution of the amygdala to this mechanism, a group of patients with unilateral lesions to the amygdala, a control group of patients with lesions in the extra-temporal regions, and a group of healthy participants completed an eVRT paradigm. They were required to detect bilateral tactile stimulation on their own cheeks, while viewing fearful, happy, or neutral faces being touched or just approached by fingers. Healthy participants and control patients confirmed that viewing a neutral face being touched - as opposed to just approached - by fingers increases tactile detection on one's own face (i.e., the typical VRT effect) and that this effect is enhanced for fearful faces, compared to neutral and happy faces. However, in patients with amygdala lesion, although the standard VRT effect was preserved for neutral faces, this was disrupted for fearful faces. This result indicates that the preferential activation of the somatosensory cortices in response to threat relies on structural integrity of the amygdala.

Identifiants

pubmed: 30714317
doi: 10.1111/jnp.12178
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

165-182

Informations de copyright

© 2019 The British Psychological Society.

Références

Abivardi, A., & Bach, D. R. (2017). Deconstructing white matter connectivity of human amygdala nuclei with thalamus and cortex subdivisions in vivo. Human Brain Mapping, 38, 3927-3940. https://doi.org/10.1002/hbm.23639
Achenbach, T. M., & Rescorla, L. A. (2001). Manual for ASEBA school-age forms & profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth, & Families.
Adolphs, R. (2002). Neural systems for recognizing emotion. Current Opinion in Neurobiology, 12(2), 169-177. https://doi.org/10.1016/S0959-4388(02)00301-X
Adolphs, R. (2013). The biology of fear. Current Biology, 23(2), R79-R93. https://doi.org/10.1016/j.cub.2012.11.055
Adolphs, R., Damasio, H., Tranel, D., Cooper, G., & Damasio, A. R. (2000). A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 20, 2683-2690. https://doi.org/10.1523/JNEUROSCI.20-07-02683.2000
Adolphs, R., Damasio, H., Tranel, D., & Damasio, A. R. (1996). Cortical systems for the recognition of emotion in facial expressions. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 16, 7678-7687. https://doi.org/10.1523/JNEUROSCI.16-23-07678.1996
Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. (1994). Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature, 372, 669-672. https://doi.org/10.1038/372669a0
Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. R. (1995). Fear and the human amygdala. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 15, 5879-5891. https://doi.org/10.1523/JNEUROSCI.15-09-05879.1995
Amaral, D. G., & Price, J. L. (1984). Amygdalo-cortical projections in the monkey (Macaca fascicularis). The Journal of Comparative Neurology, 230(4), 465-496. https://doi.org/10.1002/cne.902300402
Amaral, D. G., Price, J. L., & Carmichael, S. T. (1992). Anatomical organization of the primate amygdaloid complex. In J. P. Aggleton (Ed.), The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction (pp. 1-66). New York, NY: Wiley-Liss.
Anderson, A. K., Christoff, K., Panitz, D., De Rosa, E., & Gabrieli, J. D. E. (2003). Neural correlates of the automatic processing of threat facial signals. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 23, 5627-5633. https://doi.org/10.1523/JNEUROSCI.23-13-05627.2003
Anderson, A. K., Spencer, D. D., Fulbright, R. K., & Phelps, E. A. (2000). Contribution of the anteromedial temporal lobes to the evaluation of facial emotion. Neuropsychology, 14(4), 526-536. https://doi.org/10.1037/0894-4105.14.4.526
Atkinson, A. P., & Adolphs, R. (2011). The neuropsychology of face perception: Beyond simple dissociations and functional selectivity. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 366, 1726-1738. https://doi.org/10.1098/rstb.2010.0349
Bates, E., Wilson, S. M., Saygin, A. P., Dick, F., Sereno, M. I., Knight, R. T., & Dronkers, N. F. (2003). Voxel-based lesion-symptom mapping. Nature Neuroscience, 6, 448-450.
Beck, B., Bertini, C., Scarpazza, C., & Làdavas, E. (2013). Observed touch on a non-human face is not remapped onto the human observer's own face. PLoS ONE, 8(11), e73681. https://doi.org/10.1371/journal.pone.0073681
Beck, A., Steer, R., & Brown, G. (2014). Manual for the beck depression inventory-II. San Antonio, TX: Psychological Corporation; 1996.
Blakemore, S.-J., Bristow, D., Bird, G., Frith, C., & Ward, J. (2005). Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia. Brain: A Journal of Neurology, 128(Pt 7), 1571-1583. https://doi.org/10.1093/brain/awh500
Brunner, E., & Munzel, U. (2000). The nonparametric Behrens-fisher problem: Asymptotic theory and a small-sample approximation. Biometrical Journal, 42(1), 17-25. https://doi.org/10.1002/(SICI)1521-4036(200001)42:1<17:AID-BIMJ17>3.0.CO;2-U
Cardini, F., Bertini, C., Serino, A., & Ladavas, E. (2012). Emotional modulation of visual remapping of touch. Emotion (Washington, D.C.), 12, 980-987. https://doi.org/10.1037/a0027351
Cardini, F., Costantini, M., Galati, G., Romani, G. L., Làdavas, E., & Serino, A. (2011). Viewing one's own face being touched modulates tactile perception: An fMRI study. Journal of Cognitive Neuroscience, 23, 503-513. https://doi.org/10.1162/jocn.2010.21484
Carr, L., Iacoboni, M., Dubeau, M.-C., Mazziotta, J. C., & Lenzi, G. L. (2003). Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas. Proceedings of the National Academy of Sciences, 100, 5497-5502. https://doi.org/10.1073/pnas.0935845100
Cheng, B., Forkert, N. D., Zavaglia, M., Hilgetag, C. C., Golsari, A., Siemonsen, S., … Thomalla, G. (2014). Influence of stroke infarct location on functional outcome measured by the modified rankin scale. Stroke, 45, 1695-1702. https://doi.org/10.1161/STROKEAHA.114.005152
Cianchetti, C., & Fancello, G. S. (2001). SAFA: Self report psychiatric questionnaire for childhood and adolescence. Florence, Italy: Organizzazioni Speciali.
Davis, M. (1994). The role of the amygdala in emotional learning. International Review of Neurobiology, 36, 225-266. https://doi.org/10.1016/S0074-7742(08)60305-0
Dienes, Z. (2011). Bayesian versus orthodox statistics: Which side are you on? Perspectives on Psychological Science, 6, 274-290. https://doi.org/10.1177/1745691611406920
Dimberg, U., Thunberg, M., & Elmehed, K. (2000). Unconscious facial reactions to emotional facial expressions. Psychological Science, 11(1), 86-89. https://doi.org/10.1111/1467-9280.00221
Ebisch, S. J. H., Perrucci, M. G., Ferretti, A., Del Gratta, C., Romani, G. L., & Gallese, V. (2008). The sense of touch: Embodied simulation in a visuotactile mirroring mechanism for observed animate or inanimate touch. Journal of Cognitive Neuroscience, 20, 1611-1623. https://doi.org/10.1162/jocn.2008.20111
Ekman, P., & Friesen, W. (1976). Picture of facial affect. Palo Alto, CA: Consulting Psychologists Press.
Fusar-Poli, P., Placentino, A., Carletti, F., Landi, P., Allen, P., Surguladze, S., & Politi, P. (2009). Functional atlas of emotional faces processing: A voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry and Neuroscience, 34, 418-432.
Gallese, V., & Sinigaglia, C. (2011). What is so special about embodied simulation? Trends in Cognitive Sciences, 15, 512-519. https://doi.org/10.1016/j.tics.2011.09.003
Gläscher, J., Rudrauf, D., Colom, R., Paul, L. K., Tranel, D., Damasio, H., & Adolphs, R. (2010). Distributed neural system for general intelligence revealed by lesion mapping. Proceedings of the National Academy of Sciences, 107, 4705-4709. https://doi.org/10.1073/pnas.0910397107
Goldman, A. I., & Sripada, C. S. (2005). Simulationist models of face-based emotion recognition. Cognition, 94, 193-213. https://doi.org/10.1016/j.cognition.2004.01.005
Graham, R., Devinsky, O., & Labar, K. S. (2007). Quantifying deficits in the perception of fear and anger in morphed facial expressions after bilateral amygdala damage. Neuropsychologia, 45(1), 42-54. https://doi.org/10.1016/j.neuropsychologia.2006.04.021
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. Human Brain Mapping, 35, 5974-5983. https://doi.org/10.1002/hbm.22598
Hamann, S. B., Stefanacci, L., Squire, L. R., Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. (1996). Recognizing facial emotion. Nature, 379, 497. https://doi.org/10.1038/379497a0
Hussey, E., & Safford, A. (2009). Perception of facial expression in somatosensory cortex supports simulationist models. Journal of Neuroscience, 29(2), 301-302. https://doi.org/10.1523/JNEUROSCI.5205-08.2009
Jabbi, M., Swart, M., & Keysers, C. (2007). Empathy for positive and negative emotions in the gustatory cortex. NeuroImage, 34, 1744-1753. https://doi.org/10.1016/j.neuroimage.2006.10.032
Jacobs, R. H. A. H., Renken, R., Aleman, A., & Cornelissen, F. W. (2012). The amygdala, top-down effects, and selective attention to features. Neuroscience and Biobehavioral Reviews, 36, 2069-2084. https://doi.org/10.1016/j.neubiorev.2012.05.011
Jarosz, A. F., & Wiley, J. (2014). What are the odds? A practical guide to computing and reporting bayes factors? Journal of Problem Solving, 7, 2. https://doi.org/10.7771/1932-6246.1167
JASP Team (2018). JASP (Version 0.9)[Computer software]. https://jasp-stats.org/faq/how-do-i-cite-jasp/
Kapp, B. S., Frysinger, R. C., Gallagher, M., & Haselton, J. R. (1979). Amygdala central nucleus lesions: Effect on heart rate conditioning in the rabbit. Physiology and Behavior, 23, 1109-1117. https://doi.org/10.1016/0031-9384(79)90304-4
Kapp, B., Whalen, P. J., Supple, W. F., & Pascoe, J. P. (1992). Amygdaloid contributions to conditioned arousal and sensory information processing. In J. P. Aggleton (Ed.), The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction (pp. 229-254). New York, NY: Wiley-Liss.
Keysers, C., Wicker, B., Gazzola, V., Anton, J.-L., Fogassi, L., & Gallese, V. (2004). A touching sight: SII/PV activation during the observation and experience of touch. Neuron, 42(2), 335-346. https://doi.org/10.1016/S0896-6273(04)00156-4
Kim, M. J., Mattek, A. M., Bennett, R. H., Solomon, K. M., Shin, J., & Whalen, P. J. (2017). Human amygdala tracks a feature-based valence signal embedded within the facial expression of surprise. Journal of Neuroscience, 37, 9510-9518. https://doi.org/10.1523/JNEUROSCI.1375-17.2017
Kim, H., Somerville, L. H., Johnstone, T., Alexander, A. L., & Whalen, P. J. (2003). Inverse amygdala and medial prefrontal cortex responses to surprised faces. NeuroReport, 14, 2317-2322. https://doi.org/10.1097/00001756-200312190-00006
LeDoux, J. (2014). Coming to terms with fear. Proceedings of the National Academy of Sciences, 111, 2871-2878. https://doi.org/10.1073/pnas.1400335111
Macaluso, E. (2006). Multisensory processing in sensory-specific cortical areas. The Neuroscientist, 12(4), 327-338. https://doi.org/10.1177/1073858406287908
Maren, S. (2001). Neurobiology of pavlovian fear conditioning. Annual Review of Neuroscience, 24, 897-931. https://doi.org/10.1146/annurev.neuro.24.1.897
McClelland, S., Garcia, R. E., Peraza, D. M., Shih, T. T., Hirsch, L. J., Hirsch, J., & Goodman, R. R. (2006). Facial emotion recognition after curative nondominant temporal lobectomy in patients with mesial temporal sclerosis. Epilepsia, 47, 1337-1342. https://doi.org/10.1111/j.1528-1167.2006.00557.x
Mende-Siedlecki, P., Verosky, S. C., Turk-Browne, N. B., & Todorov, A. (2013). Robust selectivity for faces in the human amygdala in the absence of expressions. Journal of Cognitive Neuroscience, 25, 2086-2106. https://doi.org/10.1162/jocn_a_00469
Meyer, S., Kessner, S. S., Cheng, B., Bonstrup, M., Schulz, R., Hummel, F. C., … Verheyden, G. (2015). Voxel-based lesion-symptom mapping of stroke lesions underlying somatosensory deficits. NeuroImage Clinical, 10, 257-266. http://doi.org/10.1016/j.nicl.2015.12.005
Morris, J. S., Frith, C. D., Perrett, D. I., Rowland, D., Young, A. W., Calder, A. J., & Dolan, R. J. (1996). A differential neural response in the human amygdala to fearful and happy facial expressions. Nature, 383, 812. https://doi.org/10.1038/383812a0
Morris, J. S., Öhman, A., & Dolan, R. J. (1999). A subcortical pathway to the right amygdala mediating “unseen” fear. Proceedings of the National Academy of Sciences, 96, 1680-1685. https://doi.org/10.1073/pnas.96.4.1680
Niedenthal, P. M. (2007). Embodying emotion. Science, 316, 1002-1005. https://doi.org/10.1126/science.1136930
Niedenthal, P. M., Augustinova, M., & Rychlowska, M. (2010). Body and mind: Zajonc's (Re)introduction of the motor system to emotion and cognition. Emotion Review, 2(4), 340-347. https://doi.org/10.1177/1754073910376423
Phan, K. L., Wager, T., Taylor, S. F., & Liberzon, I. (2002). Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI. NeuroImage, 16(2), 331-348. https://doi.org/10.1006/nimg.2002.1087
Phelps, E. A. (2006). Emotion and cognition: Insights from studies of the human amygdala. Annual Review of Psychology, 57(1), 27-53. https://doi.org/10.1146/annurev.psych.56.091103.070234
Pitcher, D., Garrido, L., Walsh, V., & Duchaine, B. C. (2008). Transcranial magnetic stimulation disrupts the perception and embodiment of facial expressions. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 28, 8929-8933. https://doi.org/10.1523/JNEUROSCI.1450-08.2008
Pourtois, G., Sander, D., Andres, M., Grandjean, D., Reveret, L., Olivier, E., & Vuilleumier, P. (2004). Dissociable roles of the human somatosensory and superior temporal cortices for processing social face signals. The European Journal of Neuroscience, 20, 3507-3515. https://doi.org/10.1111/j.1460-9568.2004.03794.x
Raftery, A. (1995). Bayesian model selection in social research. Sociological Methodology, 25, 111-196. https://doi.org/10.2307/271063
Rorden, C., Bonilha, L., & Nichols, T. E. (2007). Rank-order versus mean based statistics for neuroimaging. NeuroImage, 35, 1531-1537. https://doi.org/10.1016/j.neuroimage.2006.12.043
Rorden, C., & Brett, M. (2000). Stereotaxic display of brain lesions. Behavioural Neurology, 12, 191-200. https://doi.org/10.1155/2000/421719
Scarpazza, C., di Pellegrino, G., & Làdavas, E. (2014). Emotional modulation of touch in alexithymia. Emotion (Washington, D.C.), 14, 602-610. https://doi.org/10.1037/a0035888
Scarpazza, C., Làdavas, E., & Cattaneo, L. (2017). Invisible side of emotions: Somato-motor responses to affective facial displays in alexithymia. Experimental Brain Research, 236, 195-206. https://doi.org/10.1007/s00221-017-5118-x
Scarpazza, C., Làdavas, E., & di Pellegrino, G. (2015). Dissociation between emotional remapping of fear and disgust in alexithymia. PLoS ONE, 10(10), e0140229. https://doi.org/10.1371/journal.pone.0140229
Serino, A., Pizzoferrato, F., & Làdavas, E. (2008). Viewing a face (especially one's own face) being touched enhances tactile perception on the face. Psychological Science, 19(5), 434-438. https://doi.org/10.1111/j.1467-9280.2008.02105.x
Siebert, M., Markowitsch, H. J., & Bartel, P. (2003). Amygdala, affect and cognition: Evidence from 10 patients with Urbach-Wiethe disease. Brain, 126, 2627-2637. https://doi.org/10.1093/brain/awg271
Singer, T., Seymour, B., O'Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004). Empathy for pain involves the affective but not sensory components of pain. Science (New York, N.Y.), 303, 1157-1162. https://doi.org/10.1126/science.1093535
Spielberger, C. D., Gorsuch, R. L., Lushene, R., Vagg, P. R., & Jacobs, G. A. (1983). Manual for the state-trait anxiety inventory. Palo Alto, CA: Consulting Psychologists Press.
Spinnler, H., & Tognoni, G. (1987). Italian standardization and classification of Neuropsychological tests. The Italian Group on the Neuropsychological Study of Aging. Italian Journal of Neurological Sciences, (Suppl. 8), 1-120.
Sripanidkulchai, K., Sripanidkulchai, B., & Wyss, J. M. (1984). The cortical projection of the basolateral amygdaloid nucleus in the rat: A retrograde fluorescent dye study. The Journal of Comparative Neurology, 229(3), 419-431. https://doi.org/10.1002/cne.902290310
Todorov, A. (2012). The role of the amygdala in face perception and evaluation. Motivation and Emotion, 36(1), 16-26. https://doi.org/10.1007/s11031-011-9238-5
Tranel, D., Gullickson, G., Koch, M., & Adolphs, R. (2006). Altered experience of emotion following bilateral amygdala damage. Cognitive Neuropsychiatry, 11(3), 219-232. https://doi.org/10.1080/13546800444000281
Tressoldi, P. E., Vio, C., Gugliotta, M., Bisiacchi, P. S., & Cendron, M. (2005). BVN 5-11.: Battery for the neuropsychological evaluation during childhood. Con CD-ROM. Edizioni Erickson. https://doi.org/10.1016/S0896-6273(03)00679-2
Tsuchiya, N., Moradi, F., Felsen, C., Yamazaki, M., & Adolphs, R. (2009). Intact rapid detection of fearful faces in the absence of the amygdala. Nature Neuroscience, 12, 1224-1225. https://doi.org/10.1038/nn.2380
Vuilleumier, P., Richardson, M. P., Armony, J. L., Driver, J., & Dolan, R. J. (2004). Distant influences of amygdala lesion on visual cortical activation during emotional face processing. Nature Neuroscience, 7(11), 1271-1278. https://doi.org/10.1038/nn1341
Vytal, K., & Hamann, S. (2010). Neuroimaging support for discrete neural correlates of basic emotions: A voxel-based meta-analysis. Journal of Cognitive Neuroscience, 22, 2864-2885. https://doi.org/10.1162/jocn.2009.21366
Wagenmakers, E. J., Love, J., Marsman, M., Jamil, T., Ly, A., Verhagen, J., … Morey, R. D. (2018). Bayesian inference for psychology. Part II: Example applications with JASP. Psychonomic Bulletin and Review, 25, 58-76. https://doi.org/10.3758/s13423-017- 1323-7
Whalen, P. J. (1998). Fear, vigilance, and ambiguity: Initial neuroimaging studies of the human amygdala. Current Directions in Psychological Science, 7, 177-188. https://doi.org/10.1111/1467-8721.ep10836912
Whalen, P. J., Raila, H., Bennett, R., Mattek, A., Brown, A., Taylor, J., … Palmer, A. (2013). Neuroscience and facial expressions of emotion: The role of amygdala-prefrontal interactions. Emotion Review, 5(1), 78-83. https://doi.org/10.1177/1754073912457231
Wicker, B., Keysers, C., Plailly, J., Royet, J. P., Gallese, V., & Rizzolatti, G. (2003). Both of us disgusted in My insula: The common neural basis of seeing and feeling disgust. Neuron, 40, 655-664. https://doi.org/10.1016/S0896-6273(03)00679-2
Winston, J. S., O'Doherty, J., & Dolan, R. J. (2003). Common and distinct neural responses during direct and incidental processing of multiple facial emotions. NeuroImage, 20(1), 84-97. https://doi.org/10.1016/S1053-8119(03)00303-3
Young, M. P., Scannell, J. W., Burns, G. A., & Blakemore, C. (1994). Analysis of connectivity: Neural systems in the cerebral cortex. Reviews in the Neurosciences, 5(3), 227-250. https://doi.org/10.1515/REVNEURO.1994.5.3.227

Auteurs

Caterina Bertini (C)

Center for Studies and Research in Cognitive Neuroscience, University of Bologna, Italy.
Department of Psychology, University of Bologna, Italy.

Francesca Starita (F)

Center for Studies and Research in Cognitive Neuroscience, University of Bologna, Italy.
Department of Psychology, University of Bologna, Italy.

Claudia Passamonti (C)

Regional Center for Pediatric Epilepsy, Department of Neuropsychiatry, Ospedali Riuniti, Ancona, Italy.

Francesca Santoro (F)

Unit of Neurology, IRCCS - Institute of Neurological Sciences of Bologna, Bellaria Hospital, Bologna, Italy.

Nelia Zamponi (N)

Regional Center for Pediatric Epilepsy, Department of Neuropsychiatry, Ospedali Riuniti, Ancona, Italy.

Roberto Michelucci (R)

Unit of Neurology, IRCCS - Institute of Neurological Sciences of Bologna, Bellaria Hospital, Bologna, Italy.

Cristina Scarpazza (C)

Center for Studies and Research in Cognitive Neuroscience, University of Bologna, Italy.
Department of Psychology, University of Bologna, Italy.
Department of General Psychology, University of Padova, Italy.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH