Threat imminence modulates neural gain in attention and motor relevant brain circuits in humans.
Adolescent
Adult
Affect
/ physiology
Attention
/ physiology
Autonomic Nervous System
/ physiology
Beta Rhythm
/ physiology
Cortical Synchronization
/ physiology
Evoked Potentials, Visual
/ physiology
Fear
/ physiology
Female
Heart Rate
/ physiology
Humans
Male
Middle Aged
Motor Cortex
/ physiology
Nerve Net
/ physiology
Parietal Lobe
/ physiology
Pattern Recognition, Visual
/ physiology
Young Adult
Journal
Psychophysiology
ISSN: 1540-5958
Titre abrégé: Psychophysiology
Pays: United States
ID NLM: 0142657
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
revised:
15
04
2021
received:
18
11
2020
accepted:
28
04
2021
pubmed:
26
5
2021
medline:
4
2
2022
entrez:
25
5
2021
Statut:
ppublish
Résumé
Different levels of threat imminence elicit distinct computational strategies reflecting how the organism interacts with its environment in order to guarantee survival. Thereby, parasympathetically driven orienting and inhibition of on-going behavior in post-encounter situations and defense reactions in circa-strike conditions associated with sympathetically driven action preparation are typically observed across species. Here, we show that healthy humans are characterized by markedly variable individual orienting or defense response tendencies as indexed by differential heart rate (HR) changes during the passive viewing of unpleasant pictures. Critically, these HR response tendencies predict neural gain modulations in cortical attention and preparatory motor circuits as measured by neuromagnetic steady-state visual evoked fields (ssVEFs) and induced beta-band (19-30 Hz) desynchronization, respectively. Decelerative HR orienting responses were associated with increased ssVEF power in the parietal cortex and reduced beta-band desynchronization in pre-motor and motor areas. However, accelerative HR defense response tendencies covaried with reduced ssVEF power in the parietal cortex and lower beta-band desynchronization in cortical motor circuits. These results show that neural gain in attention- and motor-relevant brain areas is modulated by HR indexed threat imminence during the passive viewing of unpleasant pictures. The observed mutual ssVEF and beta-band power modulations in attention and motor brain circuits support the idea of two prevalent response tendencies characterized by orienting and motor inhibition or reduced stimulus processing and action initiation tendencies at different perceived threat imminence levels.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13849Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2021 The Authors. Psychophysiology published by Wiley Periodicals LLC on behalf of Society for Psychophysiological Research.
Références
Antov, M. I., Plog, E., Bierwirth, P., Keil, A., & Stockhorst, U. (2020). Visuocortical tuning to a threat-related feature persists after extinction and consolidation of conditioned fear. Scientific Reports, 10(1), 3926. https://doi.org/10.1038/s41598-020-60597-z
Ashrafulla, S., Pantazis, D., Mosher, J., Hamalainen, M., Liu, B., & Leahy, R. M. (2011). Viability of Sharing MEG Data using Minimum-Norm Imaging. Medical Imaging 2011: Advanced Pacs-Based Imaging Informatics and Therapeutic Applications, 7967. https://doi.org/10.1117/12.879111
Barratt, E. L., Francis, S. T., Morris, P. G., & Brookes, M. J. (2018). Mapping the topological organisation of beta oscillations in motor cortex using MEG. NeuroImage, 181, 831-844. https://doi.org/10.1016/j.neuroimage.2018.06.041
Bolles, R. C. (1970). Species-specific defense reactions and avoidance learning. Psychological Review, 77, 32-48. https://doi.org/10.1037/h0028589
Bradley, M. M. (2009). Natural selective attention: Orienting and emotion. Psychophysiology, 46(1), 1-11. https://doi.org/10.1111/j.1469-8986.2008.00702.x
Bradley, M. M., Codispoti, M., Cuthbert, B. N., & Lang, P. J. (2001). Emotion and motivation I: defensive and appetitive reactions in picture processing. Emotion, 1(3), 276-298. https://doi.org/10.1037/1528-3542.1.3.276
Bradley, M. M., Keil, A., & Lang, P. J. (2012). Orienting and emotional perception: Facilitation, attenuation, and interference. Frontiers in Psychology, 3, 493. https://doi.org/10.3389/fpsyg.2012.00493
Codispoti, M., & De Cesarei, A. (2007). Arousal and attention: Picture size and emotional reactions. Psychophysiology, 44(5), 680-686. https://doi.org/10.1111/j.1469-8986.2007.00545.x
Collins, D. L., Zijdenbos, A. P., Kollokian, V., Sled, J. G., Kabani, N. J., Holmes, C. J., & Evans, A. C. (1998). Design and construction of a realistic digital brain phantom. IEEE Transactions on Medical Imaging, 17(3), 463-468. https://doi.org/10.1109/42.712135
Corbetta, M., Patel, G., & Shulman, G. L. (2008). The reorienting system of the human brain: From environment to theory of mind. Neuron, 58(3), 306-324. https://doi.org/10.1016/j.neuron.2008.04.017
Fanselow, M. S. (1994). Neural organization of the defensive behavior system responsible for fear. Psychonomic Bulletin & Review, 1, 429-438. https://doi.org/10.3758/BF03210947
Fanselow, M. S., & Lester, L. S. (1988). A functional behavioristic approach to aversively motivated behavior: Predatory imminence as a determinant of the topography of defensive behavior. In R. C. Bolles, & M. D. Beecher (Eds.), Evolution and learning (pp. 185-212). Lawrence Erlbaum Associates Inc.
Gavazzeni, J., Wiens, S., & Fischer, H. (2008). Age effects to negative arousal differ for self-report and electrodermal activity. Psychophysiology, 45(1), 148-151. https://doi.org/10.1111/j.1469-8986.2007.00596.x
Graham, F. K., & Clifton, R. K. (1966). Heart-rate change as a component of the orienting response. Psychological Bulletin, 65(5), 305-320. https://doi.org/10.1037/h0023258
Gramfort, A., Luessi, M., Larson, E., Engemann, D. A., Strohmeier, D., Brodbeck, C., Parkkonen, L., & Hämäläinen, M. S. (2014). MNE software for processing MEG and EEG data. NeuroImage, 86, 446-460. https://doi.org/10.1016/j.neuroimage.2013.10.027
Grühn, D., & Scheibe, S. (2008). Age-related differences in valence and arousal ratings of pictures from the International Affective Picture System (IAPS): Do ratings become more extreme with age? Behavior Research Methods, 40(2), 512-521. https://doi.org/10.3758/brm.40.2.512
Haagenars, M. A., Mesbah, R., & Cremers, H. (2015). Mental imagery affects subsequent autonomic defense responses. Frontiers in Psychiatry, 6, 73. https://doi.org/10.3389/fpsyt.2015.00073
Hajcak, G., MacNamara, A., Foti, D., Ferri, J., & Keil, A. (2013). The dynamic allocation of attention to emotion: Simultaneous and independent evidence from the late positive potential and steady state visual evoked potentials. Biological Psychology, 92(3), 447-455. https://doi.org/10.1016/j.biopsycho.2011.11.012
Hamm, A. O., & Vaitl, D. (1996). Affective learning: Awareness and aversion. Psychophysiology, 33(6), 698-710. https://doi.org/10.1111/j.1469-8986.1996.tb02366.x
Hare, R. D. (1972). Cardiovascular components of orienting and defensive responses. Psychophysiology, 9(6), 606-614. https://doi.org/10.1111/j.1469-8986.1972.tb00770.x
Hare, R. D., & Blevings, G. (1975). Defensive responses to phobic stimuli. Biological Psychology, 3(1), 1-13. https://doi.org/10.1016/0301-0511(75)90002-2
Hermans, E. J., Henckens, M. J., Roelofs, K., & Fernandez, G. (2013). Fear bradycardia and activation of the human periaqueductal grey. NeuroImage, 66, 278-287. https://doi.org/10.1016/j.neuroimage.2012.10.063
Hodes, R. L., Cook, E. W. 3rd, & Lang, P. J. (1985). Individual differences in autonomic response: Conditioned association or conditioned fear? Psychophysiology, 22(5), 545-560. https://doi.org/10.1111/j.1469-8986.1985.tb01649.x
Huang, M. X., Mosher, J. C., & Leahy, R. M. (1999). A sensor-weighted overlapping-sphere head model and exhaustive head model comparison for MEG. Physics in Medicine & Biology, 44(2), 423-440. https://doi.org/10.1088/0031-9155/44/2/010
Jennings, J. R., & van der Molen, M. W. (2005). Preparation for speeded action as a psychophysiological concept. Psychological Bulletin, 131(3), 434-459. https://doi.org/10.1037/0033-2909.131.3.434
Jennings, J. R., van der Molen, M. W., Somsen, R. J., & Terezis, C. (1990). On the shift from anticipatory heart rate deceleration to acceleratory recovery: Revisiting the role of response factors. Psychophysiology, 27(4), 385-395. https://doi.org/10.1111/j.1469-8986.1990.tb02332.x
Jennings, J. R., & Woods, C. C. (1977). Cardiac cycle time effects on performance, phasic cardiac responses, and their intercorrelation in choice reaction time. Psychophysiology, 14(3), 297-307. https://doi.org/10.1111/j.1469-8986.1977.tb01179.x
Keil, A., Gruber, T., Muller, M. M., Moratti, S., Stolarova, M., Bradley, M. M., & Lang, P. J. (2003). Early modulation of visual perception by emotional arousal: Evidence from steady-state visual evoked brain potentials. Cognitive, Affective, & Behavioural Neuroscience, 3(3), 195-206. https://doi.org/10.3758/CABN.3.3.195
Keil, A., Moratti, S., Sabatinelli, D., Bradley, M. M., & Lang, P. J. (2005). Additive effects of emotional content and spatial selective attention on electrocortical facilitation. Cerebral Cortex, 15(8), 1187-1197. https://doi.org/10.1093/cercor/bhi001
Keil, A., Sabatinelli, D., Ding, M., Lang, P. J., Ihssen, N., & Heim, S. (2009). Re-entrant projections modulate visual cortex in affective perception: Evidence from Granger causality analysis. Human Brain Mapping, 30(2), 532-540. https://doi.org/10.1002/hbm.20521
Keil, A., Smith, J. C., Wangelin, B. C., Sabatinelli, D., Bradley, M. M., & Lang, P. J. (2008). Electrocortical and electrodermal responses covary as a function of emotional arousal: A single-trial analysis. Psychophysiology, 45(4), 516-523. https://doi.org/10.1111/j.1469-8986.2008.00667.x
Koelewijn, T., van Schie, H. T., Bekkering, H., Oostenveld, R., & Jensen, O. (2008). Motor-cortical beta oscillations are modulated by correctness of observed action. NeuroImage, 40(2), 767-775. https://doi.org/10.1016/j.neuroimage.2007.12.018
Lacey, B. C., & Lacey, J. I. (1980). Cognitive modulation of time-dependent primary bradycardia. Psychophysiology, 17(3), 209-221. https://doi.org/10.1111/j.1469-8986.1980.tb00137.x
Lachert, P., Janusek, D., Pulawski, P., Liebert, A., Milej, D., & Blinowska, K. J. (2017). Coupling of Oxy- and Deoxyhemoglobin concentrations with EEG rhythms during motor task. Scientific Reports, 7(1), 15414. https://doi.org/10.1038/s41598-017-15770-2
Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1997). Motivated attention: affect, activation, and action. In P. J. Lang, R. F. Simons, & M. T. Balaban (Eds.), Attention and orienting: Sensory and motivational processes (pp. 97-135). Lawrence Erlbaum Associates.
Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2005). International affective picture system (IAPS): Affective ratings of pictures and instruction manual. Technical Report A-6.
Mobbs, D., Headley, D. B., Ding, W., & Dayan, P. (2020). Space, time, and fear: Survival computations along defensive circuits. Trends in Cognitive Sciences, 24(3), 228-241. https://doi.org/10.1016/j.tics.2019.12.016
Mobbs, D., Marchant, J. L., Hassabis, D., Seymour, B., Tan, G., Gray, M., Petrovic, P., Dolan, R. J., & Frith, C. D. (2009). From threat to fear: The neural organization of defensive fear systems in humans. Journal of Neuroscience, 29(39), 12236-12243. https://doi.org/10.1523/JNEUROSCI.2378-09.2009
Mobbs, D., Petrovic, P., Marchant, J. L., Hassabis, D., Weiskopf, N., Seymour, B., Dolan, R. J., & Frith, C. D. (2007). When fear is near: Threat imminence elicits prefrontal-periaqueductal gray shifts in humans. Science, 317(5841), 1079-1083. https://doi.org/10.1126/science.1144298
Moratti, S., & Keil, A. (2005). Cortical activation during Pavlovian fear conditioning depends on heart rate response patterns: An MEG study. Cognitive Brain Research, 25(2), 459-471. https://doi.org/10.1016/j.cogbrainres.2005.07.006
Moratti, S., Keil, A., & Miller, G. A. (2006). Fear but not awareness predicts enhanced sensory processing in fear conditioning. Psychophysiology, 43(2), 216-226. https://doi.org/10.1111/j.1464-8986.2006.00386.x
Moratti, S., Keil, A., & Stolarova, M. (2004). Motivated attention in emotional picture processing is reflected by activity modulation in cortical attention networks. NeuroImage, 21(3), 954-964. https://doi.org/10.1016/j.neuroimage.2003.10.030
Moratti, S., Rubio, G., Campo, P., Keil, A., & Ortiz, T. (2008). Hypofunction of right temporoparietal cortex during emotional arousal in depression. Archives of General Psychiatry, 65(5), 532-541. https://doi.org/10.1001/archpsyc.65.5.532
Moratti, S., Saugar, C., & Strange, B. A. (2011). Prefrontal-occipitoparietal coupling underlies late latency human neuronal responses to emotion. Journal of Neuroscience, 31(47), 17278-17286. https://doi.org/10.1523/JNEUROSCI.2917-11.2011
Moratti, S., Strange, B., & Rubio, G. (2015). Emotional arousal modulation of right temporoparietal cortex in depression depends on parental depression status in women: First evidence. Journal of Affective Disorders, 178, 79-87. https://doi.org/10.1016/j.jad.2015.02.031
Nichols, T. E., & Holmes, A. P. (2002). Nonparametric permutation tests for functional neuroimaging: A primer with examples. Human Brain Mapping, 15(1), 1-25. https://doi.org/10.1002/hbm.1058
Obrist, P. A. (1968). Heart rate and somatic-motor coupling during classical aversive conditioning in humans. Journal of Experimental Psychology, 77(2), 180-193. https://doi.org/10.1037/h0025814
Park, G., & Thayer, J. F. (2014). From the heart to the mind. Cardiac vagal tone modulates top-down and bottom-up visual perception and attention to emotional stimuli. Frontiers in Psychology, 1(5), 278. https://doi.org/10.3389/fpsyg.2014.00278
Park, H. D., Bernasconi, F., Salomon, R., Tallon-Baudry, C., Spinelli, L., Seeck, M., Schaller, K., & Blanke, O. (2018). Neural sources and underlying mechanisms of neural responses to heartbeats, and their role in bodily self-consciousness: An intracranial EEG study. Cerebral Cortex, 28, 2351-2364. https://doi.org/10.1093/cercor/bhx136
Park, H., Kim, J. S., & Chung, C. K. (2013). Differential beta-band event-related desynchronization during categorical action sequence planning. PLoS One, 8(3), e59544. https://doi.org/10.1371/journal.pone.0059544
Perakakis, P., Joffily, M., Taylor, M., Guerra, P., & Vila, J. (2010). KARDIA: A Matlab software for the analysis of cardiac interbeat intervals. Computer Methods and Programs in Biomedicine, 98(1), 83-89. https://doi.org/10.1016/j.cmpb.2009.10.002
Perusini, J. N., & Fanselow, M. S. (2015). Neurobehavioral perspectives on the distinction between fear and anxiety. Learning & Memory, 22(9), 417-425. https://doi.org/10.1101/lm.039180.115
Pfurtscheller, G., & Aranibar, A. (1979). Evaluation of event-related desynchronization (ERD) preceding and following voluntary self-paced movement. Electroencephalography and Clinical Neurophysiology, 46(2), 138-146. https://doi.org/10.1016/0013-4694(79)90063-4
Pfurtscheller, G., & Lopes da Silva, F. H. (1999). Event-related EEG/MEG synchronization and desynchronization: Basic principles. Clinical Neurophysiology, 110(11), 1842-1857. https://doi.org/10.1016/s1388-2457(99)00141-8
Pourtois, G., Schwartz, S., Seghier, M. L., Lazeyras, F., & Vuilleumier, P. (2006). Neural systems for orienting attention to the location of threat signals: An event-related fMRI study. NeuroImage, 31(2), 920-933. https://doi.org/10.1016/j.neuroimage.2005.12.034
Pfurtscheller, G., Solis-Escalante, T., Barry, R. J., Klobassa, D. S., Neuper, C., & Muller-Putz, G. R. (2013). Brisk heart rate and EEG changes during execution and withholding of cue-paced foot motor imagery. Front Hum Neurosci, 7, 379. https://doi.org/10.3389/fnhum.2013.00379.
Reyes del Paso, G. A., & Vila, J. (1998). The continuing problem of incorrect heart rate estimation in psychophysiological studies: An off-line solution for cardiotachometer users. Biological Psychology, 48(3), 269-279. https://doi.org/10.1016/s0301-0511(98)00039-8
Roelofs, K. (2017). Freeze for action: Neurobiological mechanisms in animal and human freezing. Philosophical Transactions of the Royal Society B-Biological Sciences, 372(1718), https://doi.org/10.1098/rstb.2016.0206
Rossiter, H. E., Davis, E. M., Clark, E. V., Boudrias, M. H., & Ward, N. S. (2014). Beta oscillations reflect changes in motor cortex inhibition in healthy ageing. NeuroImage, 91, 360-365. https://doi.org/10.1016/j.neuroimage.2014.01.012
Rössler, L., & Gamer, M. (2019). Freezing of gaze during action preparation under threat imminence. Scientific Reports, 9(1), 17215. https://doi.org/10.1038/s41598-019-53683-4
Sagaspe, P., Schwartz, S., & Vuilleumier, P. (2011). Fear and stop: A role for the amygdala in motor inhibition by emotional signals. NeuroImage, 55(4), 1825-1835. https://doi.org/10.1016/j.neuroimage.2011.01.027
Sanchez-Navarro, J. P., Martinez-Selva, J. M., Maldonado, E. F., Carrillo-Verdejo, E., Pineda, S., & Torrente, G. (2018). Autonomic reactivity in blood-injection-injury and snake phobia. Journal of Psychosomatic Research, 115, 117-124. https://doi.org/10.1016/j.jpsychores.2018.10.018
Schwerdtfeger, A. R., Schwarz, G., Pfurtscheller, K., Thayer, J. F., Jarczok, M. N., & Pfurtscheller, G. (2020). Clinical Neurophysiology, 131, 676-693. https://doi.org/10.1016/j.clinph.2019.11.013
Sokolov, E. N. (1963). Perception and the conditioned reflex. Pergamon.
Tadel, F., Baillet, S., Mosher, J. C., Pantazis, D., & Leahy, R. M. (2011). Brainstorm: A user-friendly application for MEG/EEG analysis. Computational Intelligence and Neuroscience, 2011, 879716. https://doi.org/10.1155/2011/879716
Thayer, J. F. (2006). On the importance of inhibition: Central and peripheral manifestations of nonlinear inhibitory processes in neural systems. Dose-Response, 4(1), 2-21. https://doi.org/10.2203/dose-response.004.01.002.Thayer
Thayer, J. F., & Lane, R. D. (2009). Claude Bernard and the heart-brain connection: Further elaboration of a model of neurovisceral integration. Neuroscience and Biobehavioral Reviews, 33, 81-88. https://doi.org/10.1016/j.neubiorev.2008.08.004
Tumati, S., Paulus, M. P., & Northoff, G. (2021). Out-of-step: Brain-heart desynchronization in anxiety disorders. Molecular Psychiatry. Epub ahead of print. https://doi.org/10.1038/s41380-021-01029-w
Tzagarakis, C., West, S., & Pellizzer, G. (2015). Brain oscillatory activity during motor preparation: Effect of directional uncertainty on beta, but not alpha, frequency band. Frontiers in Neuroscience, 9, 246. https://doi.org/10.3389/fnins.2015.00246
Vieira, J. B., Schellhaas, S., Enström, E., & Olsson, A. (2020). Help or flight? Increased threat imminence promotes defensive helping in humans. Proceedings of the Royal Society B: Biological Sciences, 287(1933), 20201473. https://doi.org/10.1098/rspb.2020.1473
Weerts, T. C., & Lang, P. J. (1978). Psychophysiology of fear imagery - Differences between focal phobia and social performance anxiety. Journal of Consulting and Clinical Psychology, 46(5), 1157-1159. https://doi.org/10.1037/0022-006x.46.5.1157
Yuan, M., Gimenez-Fernandez, T., Mendez-Bertolo, C., & Moratti, S. (2018). Ultrafast cortical gain adaptation in the human brain by trial-to-trial changes of associative strength in fear learning. Journal of Neuroscience, 38(38), 8262-8276. https://doi.org/10.1523/JNEUROSCI.0977-18.2018