Fear bradycardia and activation of the human periaqueductal grey

Hermans, Erno J.; Henckens, Marloes J.A.G.; Roelofs, Karin; Fernández, Guillén

doi:10.1016/j.neuroimage.2012.10.063

Cited by 151Memory and Neural MechanismsHeart Rate Variability and Autonomic ControlNeural and Behavioral Psychology Studies

Fear bradycardia and activation of the human periaqueductal grey

Hermans, Erno J., Henckens, Marloes J.A.G., Roelofs, Karin, Fernández, Guillén·2013·NeuroImage

DOI 10.1016/j.neuroimage.2012.10.063

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Abstract

Animal models of predator defense distinguish qualitatively different behavioral modes that are activated at increasing levels of predation threat. A defense mode observed at intermediate threat levels is freezing: a cessation of locomotion that is characterized by a parasympathetically dominated autonomic nervous system response that causes heart rate deceleration, or fear bradycardia. Studies in rodents have shown that freezing depends on amygdalar projections to the periaqueductal grey (PAG). In humans, freezing-like behaviors are implicated in development and maintenance of psychopathology, but neural mechanisms underlying freezing or its characteristic autonomic response profile have not been identified. Here, we combined event-related blood oxygenation level-dependent functional MRI (BOLD-fMRI) with autonomic response measures in a picture viewing paradigm to probe activity and interconnectivity within the amygdala-PAG pathway and test for an association with parasympathetic as opposed to sympathetic activation. In response to negatively arousing pictures, we observed parasympathetic (bradycardia) and sympathetic (pupil dilation) autonomic responses, BOLD responses in the amygdala and PAG, and effective connectivity between these regions. Critically, BOLD responses in the PAG to negative pictures correlated on a trial-by-trial basis with bradycardia but not pupil dilation. This correlation with bradycardia remained significant when partialling out pupil dilation. Additionally, activity in regions associated with motor planning and inhibition mirrored the PAG response. Thus, our findings implicate the human PAG in a parasympathetically dominated defense mode that subserves a state of attentive immobility. Mechanistic insight into this qualitatively distinct defense mode may importantly advance translational models of anxiety disorders.

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Similar brain regions may be involved in human freezing.
“Recent neuroimaging studies in humans have indicated that similar brain regions may be involved in human freezing.”
From Freeze for action: neurobiological mechanisms in animal and human freezing (2017) · cites this paper as [77]
In humans, brain structures similar to those observed in animals are implicated in freezing.
“Neuroimaging studies in humans have indicated that, in humans, brain structures similar to those previously observed in animals (rodents and primates) are implicated in freezing.”
From Freeze for action: neurobiological mechanisms in animal and human freezing (2017) · cites this paper as [77]
Heart rate deceleration associated with aversive versus neutral picture-viewing in an MRI scanner is associated with increased activity in the periaqueductal grey and increased connectivity between the amygdala and the periaqueductal grey.
“Heart rate deceleration associated with aversive versus neutral picture-viewing in an MRI scanner was associated with increased activity in the PAG and increased connectivity between the amygdala and the PAG.”
From Freeze for action: neurobiological mechanisms in animal and human freezing (2017) · cites this paper as [77]
In animals and humans, the parasympathetic state of freezing has been associated with increased activation of and connectivity between the amygdala and the periaqueductal grey.
“In animals and humans, the parasympathetic state of freezing has been associated with increased activation of and connectivity between the amygdala and the PAG.”
From Freeze for action: neurobiological mechanisms in animal and human freezing (2017) · cites this paper as [77]
The increased threat-induced periaqueductal grey activity is specifically related to the parasympathetically driven heart rate reduction and not to sympathetic index.
“On the basis of trial-by-trial correlations, the authors showed that the increased threat-induced PAG activity was specifically related to the parasympathetically driven heart rate reduction and did not occur as a function of sympathetic index (i.e. pupil dilation).”
From Freeze for action: neurobiological mechanisms in animal and human freezing (2017) · cites this paper as [77]

Cognitive Therapy for Depression
(2012) · PsycEXTRA Dataset · doi:10.1037/e675542012-001 · Cited by 9,678 · see citing works
Measuring emotion: The self-assessment manikin and the semantic differential
Bradley, M. M., & Lang, P. J. (1994) · Journal of Behavior Therapy and Experimental Psychiatry · doi:10.1016/0005-7916(94)90063-9 · Cited by 9,538 · see citing works
A fast diffeomorphic image registration algorithm
Ashburner, J. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.07.007 · Cited by 8,122 · see citing works
Unified segmentation
Ashburner, J., & Friston, K. J. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.02.018 · Cited by 7,507 · see citing works
Dissociable intrinsic connectivity networks for salience processing and executive control
Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., Reiss, A. L., & Greicius, M. D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5587-06.2007 · Cited by 7,426 · see citing works
Generalized autocalibrating partially parallel acquisitions (GRAPPA)
Griswold, M. A., Jakob, P. M., Heidemann, R. M., Nittka, M., Jellús̆, V., Wang, J., Kiefer, B., & Haase, A. (2002) · Magnetic Resonance in Medicine · doi:10.1002/mrm.10171 · Cited by 5,311 · see citing works
Handbook of Affective Sciences
(2002) · doi:10.1093/oso/9780195126013.001.0001 · Cited by 5,104 · see citing works
Cognitive Therapy of Depression
HOLLON, S. D., & BECK, A. T. (1979) · Cognitive-Behavioral Interventions · doi:10.1016/b978-0-12-404480-7.50012-5 · Cited by 4,685 · see citing works
Psychophysiological and Modulatory Interactions in Neuroimaging
Friston, K. J., Buechel, C., Fink, G. R., Morris, J., Rolls, E., & Dolan, R. J. (1997) · NeuroImage · doi:10.1006/nimg.1997.0291 · Cited by 3,097 · see citing works
The amygdala: vigilance and emotion
Davis, M., & Whalen, P. J. (2001) · Molecular Psychiatry · doi:10.1038/sj.mp.4000812 · Cited by 2,882 · see citing works
The emotional Stroop task and psychopathology
Williams, J. M. G., Mathews, A., & MacLeod, C. (1996) · Psychological Bulletin · doi:10.1037/0033-2909.120.1.3 · Cited by 2,420 · see citing works
The pupil as a measure of emotional arousal and autonomic activation
Bradley, M. M., Miccoli, L., Escrig, M. A., & Lang, P. J. (2008) · Psychophysiology · doi:10.1111/j.1469-8986.2008.00654.x · Cited by 1,919 · see citing works
Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans
Aron, A. R., Fletcher, P. C., Bullmore, E. T., Sahakian, B. J., & Robbins, T. W. (2003) · Nature Neuroscience · doi:10.1038/nn1003 · Cited by 1,771 · see citing works
Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear
LeDoux, J., Iwata, J., Cicchetti, P., & Reis, D. (1988) · The Journal of Neuroscience · doi:10.1523/jneurosci.08-07-02517.1988 · Cited by 1,580 · see citing works
Do threatening stimuli draw or hold visual attention in subclinical anxiety?
Fox, E., Russo, R., Bowles, R., & Dutton, K. (2001) · Journal of Experimental Psychology: General · doi:10.1037/0096-3445.130.4.681 · Cited by 1,469 · see citing works
Double Dissociation of Conditioning and Declarative Knowledge Relative to the Amygdala and Hippocampus in Humans
Bechara, A., Tranel, D., Damasio, H., Adolphs, R., Rockland, C., & Damasio, A. R. (1995) · Science · doi:10.1126/science.7652558 · Cited by 1,400 · see citing works
From Reactive to Proactive and Selective Control: Developing a Richer Model for Stopping Inappropriate Responses
Aron, A. R. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.07.024 · Cited by 1,236 · see citing works
Functional grouping and cortical–subcortical interactions in emotion: a meta-analysis of neuroimaging studies
Kober, H., Barrett, L. F., Joseph, J., Bliss-Moreau, E., Lindquist, K., & Wager, T. D. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.03.059 · Cited by 1,144 · see citing works
The neuroanatomical and neurochemical basis of conditioned fear
Fendt, M., & Fanselow, M. S. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00016-0 · Cited by 1,092 · see citing works
Emotion, motivation, and anxiety: brain mechanisms and psychophysiology
Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1998) · Biological Psychiatry · doi:10.1016/s0006-3223(98)00275-3 · Cited by 1,043 · see citing works
Cognitive Approaches to Emotion and Emotional Disorders
Mathews, A., & MacLeod, C. (1994) · Annual Review of Psychology · doi:10.1146/annurev.ps.45.020194.000325 · Cited by 1,023 · see citing works
Neural organization of the defensive behavior system responsible for fear
Fanselow, M. S. (1994) · Psychonomic Bulletin & Review · doi:10.3758/bf03210947 · Cited by 1,000 · see citing works
When fear is near: threat imminence elicits prefrontal periaqueductal gray shifts in humans.
Mobbs, D., Petrovic, P., Marchant, J. L., Hassabis, D., Weiskopf, N., Seymour, B., Dolan, R. J., & Frith, C. D. (2007) · Science · doi:10.1126/science.1144298 · Cited by 951 · see citing works
Genetic dissection of an amygdala microcircuit that gates conditioned fear
Haubensak, W., Kunwar, P. S., Cai, H., Ciocchi, S., Wall, N. R., Ponnusamy, R., Biag, J., Dong, H.-W., Deisseroth, K., Callaway, E. M., et al. (2010) · Nature · doi:10.1038/nature09553 · Cited by 840 · cited 1× · see citing works
“Rodent studies have shown that the amygdala plays a key role in orchestrating defensive behavior and transitioning between defensive modes (Davis and Whalen, 2001; Fendt and Fanselow, 1999; Gozzi et al., 2010; Haubensak et al., 2010).”
Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution
Gitelman, D. R., Penny, W. D., Ashburner, J., & Friston, K. J. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00058-2 · Cited by 799 · see citing works
Functional connectivity of the human amygdala using resting state fMRI
Roy, A. K., Shehzad, Z., Margulies, D. S., Kelly, A. M. C., Uddin, L. Q., Gotimer, K., Biswal, B. B., Castellanos, F. X., & Milham, M. P. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.11.030 · Cited by 749 · see citing works
Selective attention to threat in the dot probe paradigm: differentiating vigilance and difficulty to disengage
Koster, E. H. W., Crombez, G., Verschuere, B., & De Houwer, J. (2004) · Behaviour Research and Therapy · doi:10.1016/j.brat.2003.08.001 · Cited by 709 · see citing works
Fears, Phobias, and Rituals. Panic, Anxiety, and Their Disorders.
(1987) · Annals of Internal Medicine · doi:10.7326/0003-4819-107-4-607_3 · Cited by 665 · see citing works
Impaired fear conditioning following unilateral temporal lobectomy in humans
LaBar, K., LeDoux, J., Spencer, D., & Phelps, E. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-10-06846.1995 · Cited by 631 · see citing works
Stress-related noradrenergic activity prompts large-scale neural network reconfiguration
Hermans, E. J., van Marle, H. J. F., Ossewaarde, L., Henckens, M. J. A. G., Qin, S., van Kesteren, M. T. R., Schoots, V. C., Cousijn, H., Rijpkema, M., Oostenveld, R., et al. (2011) · Science · doi:10.1126/science.1209603 · Cited by 627 · see citing works
Self-citation
Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear.
Kim, J. J., Rison, R. A., & Fanselow, M. S. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.6.1093 · Cited by 615 · see citing works
Amygdala central nucleus lesions: Effect on heart rate conditioning in the rabbit
Kapp, B. S., Frysinger, R. C., Gallagher, M., & Haselton, J. R. (1979) · Physiology & Behavior · doi:10.1016/0031-9384(79)90304-4 · Cited by 590 · see citing works
Central circuits mediating patterned autonomic activity during active vs. passive emotional coping
Bandler, R., Keay, K. A., Floyd, N., & Price, J. (2000) · Brain Research Bulletin · doi:10.1016/s0361-9230(00)00313-0 · Cited by 582 · see citing works
Executive "Brake Failure" following Deactivation of Human Frontal Lobe
Chambers, C. D., Bellgrove, M. A., Stokes, M. G., Henderson, T. R., Garavan, H., Robertson, I. H., Morris, A. P., & Mattingley, J. B. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/089892906775990606 · Cited by 544 · see citing works
Executive “Brake Failure” following Deactivation of Human Frontal Lobe
Chambers, C. D., Bellgrove, M. A., Stokes, M. G., Henderson, T. R., Garavan, H., Robertson, I. H., Morris, A. P., & Mattingley, J. B. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.3.444 · Cited by 544 · see citing works
From threat to fear: the neural organization of defensive fear systems in humans.
Mobbs, D., Marchant, J. L., Hassabis, D., Seymour, B., Tan, G., Gray, M., Petrovic, P., Dolan, R. J., & Frith, C. D. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2378-09.2009 · Cited by 476 · see citing works
Mouse defensive behaviors: pharmacological and behavioral assays for anxiety and panic
Blanchard, D. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00009-4 · Cited by 461 · see citing works
Trauma films, information processing, and intrusive memory development
Holmes, E. A., Brewin, C. R., & Hennessy, R. G. (2004) · Journal of Experimental Psychology: General · doi:10.1037/0096-3445.133.1.3 · Cited by 457 · see citing works
Autonomic cardiac control. III. Psychological stress and cardiac response in autonomic space as revealed by pharmacological blockades
Berntson, G. G., Cacioppo, J. T., Binkley, P. F., Uchino, B. N., Quigley, K. S., & Fieldstone, A. (1994) · Psychophysiology · doi:10.1111/j.1469-8986.1994.tb02352.x · Cited by 442 · see citing works
Comparative aspects of amygdala connectivity
PRICE, J. L. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07070.x · Cited by 442 · see citing works
Functional neuroimaging studies of human emotions
Phan, K. L., Wager, T. D., Taylor, S. F., & Liberzon, I. (2004) · CNS Spectrums · doi:10.1017/s1092852900009196 · Cited by 433 · see citing works
Amygdaloid and basal forebrain direct connections with the nucleus of the solitary tract and the dorsal motor nucleus
Schwaber, J. S., Kapp, B. S., Higgins, G. A., & Rapp, P. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-10-01424.1982 · Cited by 426 · see citing works
Characterizing Stimulus–Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments
Büchel, C., Holmes, A. P., Rees, G. E., & Friston, K. J. (1998) · NeuroImage · doi:10.1006/nimg.1998.0351 · Cited by 415 · see citing works
Emotion, motivation, and the brain: Reflex foundations in animal and human research
Lang, P. J., & Davis, M. (2006) · Progress in Brain Research · doi:10.1016/s0079-6123(06)56001-7 · Cited by 410 · see citing works
Neuroimaging of the periaqueductal gray: State of the field
Linnman, C., Moulton, E. A., Barmettler, G., Becerra, L. R., & Borsook, D. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.11.095 · Cited by 402 · see citing works
Forebrain pain mechanisms
Neugebauer, V., Galhardo, V., Maione, S., & Mackey, S. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.12.014 · Cited by 353 · see citing works
Neural activity associated with monitoring the oscillating threat value of a tarantula
Mobbs, D., Yu, R., Rowe, J. B., Eich, H., FeldmanHall, O., & Dalgleish, T. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009076107 · Cited by 332 · see citing works
A freezing‐like posture to pictures of mutilation
Azevedo, T. M., Volchan, E., Imbiriba, L. A., Rodrigues, E. C., Oliveira, J. M., Oliveira, L. F., Lutterbach, L. G., & Vargas, C. D. (2005) · Psychophysiology · doi:10.1111/j.1469-8986.2005.00287.x · Cited by 320 · see citing works
Ambulatory measurement of respiratory sinus arrhythmia and respiration rate
de Geus, E. J. C., Willemsen, G. A. H. M., Klaver, C. H. A. M., & van Doornen, L. J. P. (1995) · Biological Psychology · doi:10.1016/0301-0511(95)05137-6 · Cited by 314 · see citing works
Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex
Verbruggen, F., Aron, A. R., Stevens, M., & Chambers, C. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1001957107 · Cited by 310 · see citing works
Pupillary and Cardiac Activity During Visual Attention
Libby, W. L., Lacey, B. C., & Lacey, J. I. (1973) · Psychophysiology · doi:10.1111/j.1469-8986.1973.tb00526.x · Cited by 308 · see citing works
Stressed Memories: How Acute Stress Affects Memory Formation in Humans
Henckens, M. J. A. G., Hermans, E. J., Pu, Z., Joëls, M., & Fernández, G. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1184-09.2009 · Cited by 295 · see citing works
Self-citation
Die hard: A blend of freezing and fleeing as a dynamic defense—implications for the control of defensive behavior
Eilam, D. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.027 · Cited by 292 · see citing works
Facing Freeze: Social Threat Induces Bodily Freeze in Humans
Roelofs, K., Hagenaars, M. A., & Stins, J. (2010) · Psychological Science · doi:10.1177/0956797610384746 · Cited by 288 · see citing works
Brain mediators of cardiovascular responses to social threat, part II: prefrontal–subcortical pathways and relationship with anxiety
Wager, T. D., van Ast, V. A., Hughes, B. L., Davidson, M. L., Lindquist, M. A., & Ochsner, K. N. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.05.044 · Cited by 264 · see citing works
Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress
van Marle, H. J. F., Hermans, E. J., Qin, S., & Fernández, G. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.05.070 · Cited by 251 · see citing works
Self-citation
Mesencephalic central gray lesions and fear-motivated behavior in rats
Liebman, J. M., Mayer, D. J., & Liebeskind, J. C. (1970) · Brain Research · doi:10.1016/0006-8993(70)90062-4 · Cited by 241 · see citing works
A double dissociation in the affective modulation of startle in humans: effects of unilateral temporal lobectomy
Funayama, E. S., Grillon, C., Davis, M., & Phelps, E. A. (2001) · Journal of Cognitive Neuroscience · doi:10.1162/08989290152541395 · Cited by 225 · see citing works
Use of concurrent pupil dilation assessment to inform interpretation and analysis of fMRI data
Siegle, G. J., Steinhauer, S. R., Stenger, V. A., Konecky, R. O., & Carter, C. S. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00298-2 · Cited by 220 · see citing works
A neural switch for active and passive fear
Gozzi, A., Jain, A., Giovanelli, A., Bertollini, C., Crestan, V., Schwarz, A. J., Tsetsenis, T., Ragozzino, D., Gross, C. T., & Bifone, A. (2010) · Neuron · doi:10.1016/j.neuron.2010.07.008 · Cited by 209 · see citing works
Autonomic and somatomotor effects of amygdala central N. stimulation in awake rabbits☆
Applegate, C. D., Kapp, B. S., Underwood, M. D., & McNall, C. L. (1983) · Physiology & Behavior · doi:10.1016/0031-9384(83)90201-9 · Cited by 208 · see citing works
Intrinsic functional connectivity of the periaqueductal gray, a resting fMRI study
Kong, J., Tu, P., Zyloney, C. E., & Su, T. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.03.042 · Cited by 198 · see citing works
Postural modulation induced by pictures depicting prosocial or dangerous contexts
Facchinetti, L. D., Imbiriba, L. A., Azevedo, T. M., Vargas, C. D., & Volchan, E. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.09.063 · Cited by 183 · see citing works
Fears, Phobias, and Rituals: Panic, Anxiety and Their Disorders
Beitman, B. D. (1988) · American Journal of Psychiatry · doi:10.1176/ajp.145.5.646 · Cited by 180 · see citing works
Exogenous testosterone attenuates the integrated central stress response in healthy young women
Hermans, E. J., Putman, P., Baas, J. M. P., Gecks, N. M., Kenemans, J. L., & van Honk, J. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.08.006 · Cited by 156 · see citing works
Self-citation
Aversive life events enhance human freezing responses.
Hagenaars, M. A., Stins, J. F., & Roelofs, K. (2012) · Journal of Experimental Psychology General · doi:10.1037/a0024211 · Cited by 128 · see citing works
To freeze or not to freeze? Affective and cognitive perturbations have markedly different effects on postural control
Stins, J. F., Roerdink, M., & Beek, P. J. (2010) · Human Movement Science · doi:10.1016/j.humov.2010.05.013 · Cited by 120 · see citing works
Effects of affective picture viewing on postural control.
Stins, J. F., & Beek, P. J. (2007) · BMC Neuroscience · doi:10.1186/1471-2202-8-83 · Cited by 114 · see citing works
AUTONOMIC RESPONSES TO AFFECTIVE VISUAL STIMULATION
Hare, R. D., Wood, K., Britain, S., & Shadman, J. (1970) · Psychophysiology · doi:10.1111/j.1469-8986.1970.tb01766.x · Cited by 114 · see citing works
Common representation of pain and negative emotion in the midbrain periaqueductal gray
Buhle, J. T., Kober, H., Ochsner, K. N., Mende-Siedlecki, P., Weber, J., Hughes, B. L., Kross, E., Atlas, L. Y., McRae, K., & Wager, T. D. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss038 · Cited by 100 · see citing works
On The Automaticity of Autonomic Responses in Emotion: An Evolutionary Perspective
�hman, A., & Wiens, S. (2002) · doi:10.1093/oso/9780195126013.003.0013 · Cited by 72 · see citing works
The role of central midbrain structures in conditioned responding to aversive noise in the rat
Lyon, M. (1964) · Journal of Comparative Neurology · doi:10.1002/cne.901220310 · Cited by 71 · see citing works
Freezing reaction in panic disorder patients associated with anticipatory anxiety.
Lopes, F. L., Azevedo, T. M., Imbiriba, L. A., Freire, R. C., Valença, A. M., Caldirola, D., Perna, G., Volchan, E., & Nardi, A. E. (2009) · Depression and Anxiety · doi:10.1002/da.20593 · Cited by 54 · see citing works
Preparing hearts and minds: Cardiac slowing and a cortical inhibitory network
Jennings, J. R., van der Molen, M. W., & Tanase, C. (2009) · Psychophysiology · doi:10.1111/j.1469-8986.2009.00866.x · Cited by 39 · see citing works
The Threatened Brain
Maren, S. (2007) · Science · doi:10.1126/science.1147797 · Cited by 38 · see citing works
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Terburg, D., Scheggia, D., Rio, R. T. D., Klumpers, F., Ciobanu, A. C., Morgan, B. E., Montoya, E. R., Bos, P. A., Giobellina, G., van den Burg, E. H., et al. (2018) · Cell · doi:10.1016/j.cell.2018.09.028 · Cited by 156 · see citing works
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MacDonald, K., & Feifel, D. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.025 · Cited by 139 · see citing works
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Gladwin, T. E., Hashemi, M. M., van Ast, V., & Roelofs, K. (2016) · Neuroscience Letters · doi:10.1016/j.neulet.2016.03.027 · Cited by 133 · see citing works
The periaqueductal gray controls brainstem emotional motor systems including respiration
Holstege, G. (2014) · Progress in brain research · doi:10.1016/b978-0-444-63274-6.00020-5 · Cited by 102 · see citing works
Neural Dynamics of Shooting Decisions and the Switch from Freeze to Fight
Hashemi, M. M., Gladwin, T. E., de Valk, N. M., Zhang, W., Kaldewaij, R., van Ast, V. A., Koch, S. B. J., Klumpers, F., & Roelofs, K. (2019) · Scientific Reports · doi:10.1038/s41598-019-40917-8 · Cited by 105 · see citing works
Approach-Avoidance Decisions Under Threat: The Role of Autonomic Psychophysiological States
Livermore, J. J. A., Klaassen, F. H., Bramson, B., Hulsman, A. M., Meijer, S. W., Held, L. K., Klumpers, F., de Voogd, L. D., & Karin Roelofs, A. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.621517 · Cited by 100 · see citing works
How Human Amygdala and Bed Nucleus of the Stria Terminalis May Drive Distinct Defensive Responses
Klumpers, F., Kroes, M. C. W., Baas, J. M. P., & Fernández, G. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3830-16.2017 · Cited by 95 · see citing works
Self-citation
Persistence of Amygdala‐Hippocampal Connectivity and Multi‐Voxel Correlation Structures During Awake Rest After Fear Learning Predicts Long‐Term Expression of Fear
Hermans, E., Kanen, J. W., Tambini, A., Fernández, G., Davachi, L., & Phelps, E. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw145 · Cited by 103 · see citing works
Self-citation
Freezing promotes perception of coarse visual features.
Lojowska, M., Gladwin, T. E., Hermans, E. J., & Roelofs, K. (2015) · Journal of Experimental Psychology: General · doi:10.1037/xge0000117 · Cited by 95 · see citing works
Self-citation
Down-regulation of amygdala activation with real-time fMRI neurofeedback in a healthy female sample
Paret, C., Kluetsch, R., Ruf, M., Demirakca, T., Hoesterey, S., Ende, G., & Schmahl, C. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00299 · Cited by 95 · see citing works
Modulation of the initial light reflex during affective picture viewing
Henderson, R. R., Bradley, M. M., & Lang, P. J. (2014) · Psychophysiology · doi:10.1111/psyp.12236 · Cited by 95 · see citing works
Translating dynamic defense patterns from rodents to people
Blanchard, D. C. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.11.001 · Cited by 94 · see citing works
Awake reactivation of emotional memory traces through hippocampal-neocortical interactions
de Voogd, L. D., Fernández, G., & Hermans, E. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.04.026 · Cited by 83 · see citing works
Self-citation
A pupil size response model to assess fear learning
Korn, C. W., Staib, M., Tzovara, A., Castegnetti, G., & Bach, D. R. (2016) · Psychophysiology · doi:10.1111/psyp.12801 · Cited by 84 · see citing works
Eye-Movement Intervention Enhances Extinction via Amygdala Deactivation
de Voogd, L. D., Kanen, J. W., Neville, D. A., Roelofs, K., Fernández, G., & Hermans, E. J. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0703-18.2018 · Cited by 85 · see citing works
Self-citation
The effects of trauma on brain and body: A unifying role for the midbrain periaqueductal gray
Terpou, B. A., Harricharan, S., McKinnon, M. C., Frewen, P., Jetly, R., & Lanius, R. A. (2019) · Journal of Neuroscience Research · doi:10.1002/jnr.24447 · Cited by 82 · see citing works
Specific proactive and generic reactive inhibition
Kenemans, J. L. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.06.011 · Cited by 82 · see citing works
Prepronociceptin-Expressing Neurons in the Extended Amygdala Encode and Promote Rapid Arousal Responses to Motivationally Salient Stimuli
Rodriguez-Romaguera, J., Ung, R. L., Nomura, H., Otis, J. M., Basiri, M. L., Namboodiri, V. M. K., Zhu, X., Robinson, J. E., van den Munkhof, H. E., McHenry, J. A., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108362 · Cited by 75 · see citing works
Orchestration of innate and conditioned defensive actions by the periaqueductal gray
Reis, F. M., Mobbs, D., Canteras, N. S., & Adhikari, A. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2023.109458 · Cited by 73 · see citing works
Aversive stimuli exacerbate defensive motor behaviour in motor conversion disorder
Blakemore, R. L., Sinanaj, I., Galli, S., Aybek, S., & Vuilleumier, P. O. (2016) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2016.11.005 · Cited by 69 · see citing works
Role played by periaqueductal gray neurons in parasympathetically mediated fear bradycardia in conscious rats
Koba, S., Inoue, R., & Watanabe, T. (2016) · Physiological Reports · doi:10.14814/phy2.12831 · Cited by 65 · see citing works
Functional Involvement of Human Periaqueductal Gray and Other Midbrain Nuclei in Cognitive Control
Kragel, P. A., Bianciardi, M., Hartley, L., Matthewson, G., Choi, J., Quigley, K. S., Wald, L. L., Wager, T. D., Barrett, L. F., & Satpute, A. B. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2043-18.2019 · Cited by 60 · see citing works
Integrated cardio-behavioral responses to threat define defensive states
Signoret-Genest, J., Schukraft, N., Reis, S. L., Segebarth, D., Deisseroth, K. A., & Tovote, P. (2023) · Nature Neuroscience · doi:10.1038/s41593-022-01252-w · Cited by 68 · see citing works
"Hot" cognition and dual systems: Introduction, criticisms, and ways forward
Gladwin, T. E., & Figner, B. (2014) · UvA-DARE (University of Amsterdam) · Cited by 57 · see citing works
Task modulated brain connectivity of the amygdala: a meta-analysis of psychophysiological interactions
Di, X., Huang, J., & Biswal, B. B. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1239-4 · Cited by 57 · see citing works
Imaging studies of functional neurologic disorders
Aybek, S., & Vuilleumier, P. O. (2016) · Handbook of clinical neurology · doi:10.1016/b978-0-12-801772-2.00007-2 · Cited by 57 · see citing works
Help or flight? Increased threat imminence promotes defensive helping in humans
Vieira, J. B., Schellhaas, S., Enström, E., & Olsson, A. (2020) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2020.1473 · Cited by 58 · see citing works
Neural correlates of social and non-social personal space intrusions: Role of defensive and peripersonal space systems in interpersonal distance regulation
Vieira, J. B., Pierzchajlo, S. R., & Mitchell, D. G. V. (2020) · Social Neuroscience · doi:10.1080/17470919.2019.1626763 · Cited by 54 · see citing works
Emotion’s Response Patterns: The Brain and the Autonomic Nervous System
Lang, P. J. (2014) · Emotion Review · doi:10.1177/1754073913512004 · Cited by 54 · see citing works
What Does Neuroscience Tell Us About the Conversion Model of Functional Neurological Disorders?
Cretton, A., Brown, R. J., LaFrance, W. C., Jr., & Aybek, S. (2019) · Journal of Neuropsychiatry · doi:10.1176/appi.neuropsych.19040089 · Cited by 53 · see citing works
Globally conditioned Granger causality in brain–brain and brain–heart interactions: a combined heart rate variability/ultra-high-field (7 T) functional magnetic resonance imaging study
Duggento, A., Bianciardi, M., Passamonti, L., Wald, L. L., Guerrisi, M., Barbieri, R., & Toschi, N. (2016) · Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rsta.2015.0185 · Cited by 52 · see citing works
Modeling fear‐conditioned bradycardia in humans
Castegnetti, G., Tzovara, A., Staib, M., Paulus, P. C., Hofer, N., & Bach, D. R. (2016) · Psychophysiology · doi:10.1111/psyp.12637 · Cited by 47 · see citing works
Behavioral inhibition system sensitivity enhances motor cortex suppression when watching fearful body expressions
Borgomaneri, S., Vitale, F., & Avenanti, A. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1403-5 · Cited by 48 · see citing works
Non-expert listeners show decreased heart rate and increased blood pressure (fear bradycardia) in response to atonal music
Proverbio, A. M., Manfrin, L., Arcari, L. A., Benedetto, F. D., Gazzola, M., Guardamagna, M., Nasi, V. L., & Zani, A. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01646 · Cited by 46 · see citing works
Emotional enhancement of error detection—The role of perceptual processing and inhibition monitoring in failed auditory stop trials
Senderecka, M. (2017) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-017-0546-4 · Cited by 43 · see citing works
The association between serotonin transporter availability and the neural correlates of fear bradycardia
Schipper, P., Hiemstra, M., Bosch, K., Nieuwenhuis, D., Adinolfi, A., Glotzbach, S., Borghans, B., Lopresto, D., Fernández, G., Klumpers, F., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1904843116 · Cited by 44 · see citing works
Self-citation
Approaching threats elicit a freeze-like response in humans
Sagliano, L., Cappuccio, A., Trojano, L., & Conson, M. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.12.038 · Cited by 43 · see citing works
Infant attachment predicts bodily freezing in adolescence: evidence from a prospective longitudinal study
Niermann, H. C. M., Ly, V., Smeekens, S., Figner, B., Riksen-Walraven, J. M., & Roelofs, K. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00263 · Cited by 42 · see citing works
Individual differences in bodily freezing predict emotional biases in decision making
Ly, V., Huys, Q. J. M., Stins, J. F., Roelofs, K., & Cools, R. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00237 · Cited by 43 · see citing works
Mapping the structural connectivity between the periaqueductal gray and the cerebellum in humans
Cacciola, A., Bertino, S., Basile, G. A., Mauro, D. D., Calamuneri, A., Chillemi, G., Duca, A., Bruschetta, D., Flace, P., Favaloro, A., et al. (2019) · Brain Structure and Function · doi:10.1007/s00429-019-01893-x · Cited by 42 · see citing works
Individual differences in defensive stress-responses: the potential relevance for psychopathology
Niermann, H. C., Figner, B., & Karin Roelofs, A. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.01.002 · Cited by 40 · see citing works
Anti-annexin V antibodies and digital ischemia in patients with scleroderma.
Sugiura, K., & Muro, Y. (1999) · PubMed · Cited by 38 · see citing works
Disentangling the roles of arousal and amygdala activation in emotional declarative memory.
de Voogd, L. D., Fernández, G., & Hermans, E. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw055 · Cited by 32 · see citing works
Self-citation
Visuocortical changes during a freezing-like state in humans
Lojowska, M., Ling, S., Roelofs, K., & Hermans, E. J. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.06.013 · Cited by 33 · see citing works
Self-citation
Subcortical contributions to salience network functioning during negative emotional processing
Ince, S., Steward, T., Harrison, B. J., Jamieson, A. J., Davey, C. G., Agathos, J. A., Moffat, B. A., Glarin, R. K., & Felmingham, K. L. (2023) · NeuroImage · doi:10.1016/j.neuroimage.2023.119964 · Cited by 33 · see citing works
Temporal dynamics of conditioned skin conductance and pupillary responses during fear acquisition and extinction
Jentsch, V. L., Wolf, O. T., & Merz, C. J. (2019) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2019.11.006 · Cited by 35 · see citing works
Reframing the Past: Role of Memory Processes in Emotion Regulation
Samide, R., & Ritchey, M. (2020) · Cognitive Therapy and Research · doi:10.1007/s10608-020-10166-5 · Cited by 34 · see citing works
Functional movement disorders
Barbey, A., & Aybek, S. (2017) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000464 · Cited by 32 · see citing works
Uncovering the etiology of conversion disorder: insights from functional neuroimaging
Kanaan, R., & dar, M. E. (2016) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s65880 · Cited by 30 · see citing works
Negative emotions facilitate isometric force through activation of prefrontal cortex and periaqueductal gray
Blakemore, R. L., Rieger, S. W., & Vuilleumier, P. O. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.09.029 · Cited by 30 · see citing works
Interoception and stress in patients with functional neurological symptom disorder
Williams, I. A., Reuber, M., & Levita, L. (2021) · Cognitive Neuropsychiatry · doi:10.1080/13546805.2020.1865895 · Cited by 29 · see citing works
Proven cardiac changes during death-feigning (tonic immobility) in rabbits (Oryctolagus cuniculus)
Giannico, A. T., Lima, L., Lange, R. R., Fróes, T. R., & Montiani‐Ferreira, F. (2014) · Journal of Comparative Physiology A · doi:10.1007/s00359-014-0884-4 · Cited by 27 · see citing works
Defensive freezing links Hypothalamic-Pituitary-Adrenal-axis activity and internalizing symptoms in humans
Niermann, H. C. M., Figner, B., Tyborowska, A., van Peer, J. M., Cillessen, A. H. N., & Karin Roelofs, A. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.05.001 · Cited by 27 · see citing works
Roles of the bed nucleus of the stria terminalis and amygdala in fear reactions
Hulsman, A. M., Terburg, D., Karin Roelofs, A., & Klumpers, F. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-819975-6.00027-3 · Cited by 25 · see citing works
Human defensive freezing: Associations with hair cortisol and trait anxiety
Hashemi, M. M., Zhang, W., Kaldewaij, R., Koch, S. B. J., Smit, A. S., Figner, B., Jonker, R., Klumpers, F., & Karin Roelofs, A. (2021) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2021.105417 · Cited by 32 · see citing works
The role of automatic defensive responses in the development of posttraumatic stress symptoms in police recruits: protocol of a prospective study
Koch, S. B. J., Klumpers, F., Zhang, W., Hashemi, M. M., Kaldewaij, R., van Ast, V. A., Smit, A. S., & Karin Roelofs, A. (2017) · European Journal of Psychotraumatology · doi:10.1080/20008198.2017.1412226 · Cited by 25 · see citing works
Emotional orienting during interoceptive threat in orthostatic intolerance: Dysautonomic contributions to psychological symptomatology in the postural tachycardia syndrome and vasovagal syncope
Owens, A. P., Low, D. A., Critchley, H., & Mathias, C. J. (2018) · Autonomic Neuroscience · doi:10.1016/j.autneu.2018.01.004 · Cited by 25 · see citing works
Bidirectional cardiovascular responses evoked by microstimulation of the amygdala in rats
Yamanaka, K., Takagishi, M., Kim, J., Gouraud, S. S., & Waki, H. (2017) · The Journal of Physiological Sciences · doi:10.1007/s12576-017-0523-2 · Cited by 25 · see citing works
Stimulation of the ventromedial prefrontal cortex blocks the return of subcortically mediated fear responses
Szeska, C., Pünjer, H., Riemann, S., Meinzer, M., & Hamm, A. O. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02174-8 · Cited by 23 · see citing works
Dissociated neural effects of cortisol depending on threat escapability
Montoya, E. R., van Honk, J., Bos, P. A., & Terburg, D. (2015) · Human Brain Mapping · doi:10.1002/hbm.22918 · Cited by 23 · see citing works
Neural activity during the viewing of emotional pictures in veterans with pathological anger and aggression
Heesink, L., Gladwin, T. E., Vink, M., van Honk, J., Kleber, R. J., & Geuze, E. (2017) · European Psychiatry · doi:10.1016/j.eurpsy.2017.09.002 · Cited by 22 · see citing works
Effects of testosterone administration on threat and escape anticipation in the orbitofrontal cortex
Heany, S. J., Bethlehem, R. A. I., van Honk, J., Bos, P. A., Stein, D. J., & Terburg, D. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.05.038 · Cited by 23 · see citing works
Neural correlates of anticipatory cardiac deceleration and its association with the speed of perceptual decision-making, in young and older adults
Ribeiro, M. J., & Castelo-Branco, M. S. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.06.004 · Cited by 23 · see citing works
Stress, Panic, and Central Serotonergic Inhibition
Hassell, J. E., Yamashita, P., Johnson, P. L., Zangrossi, H., Shekhar, A., & Lowry, C. A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-802175-0.00015-2 · Cited by 22 · see citing works
Behavioral and neuroimaging responses induced by mental imagery of threatening scenarios
Shuhama, R., Rondinoni, C., de Araújo, D. B., Caetano, G. D. F., dos Santos, A. C., Graeff, F. G., & Del‐Ben, C. M. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.06.059 · Cited by 20 · see citing works
Recent Advancements Surrounding the Role of the Periaqueductal Gray in Predators and Prey
Franklin, T. B. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00060 · Cited by 20 · see citing works
Detecting driver stress and hazard anticipation using real‐time cardiac measurement: A simulator study
Kerautret, L., Dabic, S., & Navarro, J. (2022) · Brain and Behavior · doi:10.1002/brb3.2424 · Cited by 19 · see citing works
Why Stuttering Occurs
Usler, E. R. (2022) · Topics in Language Disorders · doi:10.1097/tld.0000000000000275 · Cited by 19 · see citing works
Pupillary reactivity to negative stimuli prospectively predicts recurrence of major depressive disorder in women
Kudinova, A. Y., Burkhouse, K. L., Siegle, G. J., Owens, M., Woody, M. L., & Gibb, B. E. (2016) · Psychophysiology · doi:10.1111/psyp.12764 · Cited by 18 · see citing works
Proximity alert! Distance related cuneus activation in military veterans with anger and aggression problems
Heesink, L., Gladwin, T. E., Terburg, D., van Honk, J., Kleber, R. J., & Geuze, E. (2017) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2017.06.012 · Cited by 19 · see citing works
Disentangling brain activity related to the processing of emotional visual information and emotional arousal
Kuniecki, M., Wołoszyn, K., Domagalik, A., & Pilarczyk, J. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1576-y · Cited by 20 · see citing works
Threat imminence reveals links among unfolding of anticipatory physiological response, cortical-subcortical intrinsic functional connectivity, and anxiety
Abend, R., Ruiz, S. G., Bajaj, M. A., Harrewijn, A., Linke, J. O., Atlas, L. Y., Winkler, A. M., & Pine, D. S. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100428 · Cited by 17 · see citing works
Investigation of the Stability of Human Freezing-Like Responses to Social Threat From Mid to Late Adolescence
Niermann, H. C. M., Figner, B., Tyborowska, A., Cillessen, A. H. N., & Karin Roelofs, A. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00097 · Cited by 18 · see citing works
Paradoxical olfactory function in combat Veterans: The role of PTSD and odor factors
Wilkerson, A. K., Uhde, T. W., Leslie, K., Freeman, W. C., LaRowe, S. D., Schumann, A. Y., & Cortese, B. M. (2018) · Military Psychology · doi:10.1080/08995605.2018.1425063 · Cited by 17 · see citing works
Management of Functional Neurological Disorders (FND): Experience from a Swiss FND Clinic
Barbey, A., Pjanic, I., Studer, H., Bischoff, N., Bassetti, C. L., & Aybek, S. (2022) · Clinical and Translational Neuroscience · doi:10.3390/ctn6010002 · Cited by 17 · see citing works
Neural mediators of subjective and autonomic responding during threat learning and regulation
Savage, H. S., Davey, C. G., Wager, T. D., Garfinkel, S. N., Moffat, B. A., Glarin, R. K., & Harrison, B. J. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118643 · Cited by 14 · see citing works
Abnormal postural behavior in patients with functional movement disorders during exposure to stress
Zito, G. A., Apazoglou, K., Paraschiv-Ionescu, A., Aminian, K., & Aybek, S. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.11.020 · Cited by 14 · see citing works
Exploring hazard anticipation and stress while driving in light of defensive behavior theory
Kerautret, L., Dabic, S., & Navarro, J. (2023) · Scientific Reports · doi:10.1038/s41598-023-34714-7 · Cited by 14 · see citing works
Threat imminence modulates neural gain in attention and motor relevant brain circuits in humans
de Echegaray, J., & Moratti, S. (2021) · Psychophysiology · doi:10.1111/psyp.13849 · Cited by 14 · see citing works
Physiological arousal and visuocortical connectivity predict subsequent vividness of negative memories
Kark, S. M., & Kensinger, E. A. (2019) · Neuroreport · doi:10.1097/wnr.0000000000001274 · Cited by 14 · see citing works
Emotion regulation from an action-control perspective
Bramson, B., Toni, I., & Karin Roelofs, A. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105397 · Cited by 14 · see citing works
When the approaching threat is uncertain: Dynamics of defensive motivation and attention in trait anxiety
Qiao, Z., Pan, D., Hoid, D., van Winkel, R., & Li, X. (2022) · Psychophysiology · doi:10.1111/psyp.14049 · Cited by 11 · see citing works
Unraveling the cognitive correlates of heart rate variability with the drift diffusion model
Spangler, D. P., Yang, X., Weidler, B. J., Thayer, J. F., & McGinley, J. J. (2022) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2022.08.003 · Cited by 10 · see citing works
Transcranial magnetic stimulation induces heart rate decelerations independent of treatment outcome
Alario, A. A., Pace, B., Niciu, M. J., & Trapp, N. T. (2023) · Brain stimulation · doi:10.1016/j.brs.2023.06.005 · Cited by 10 · see citing works
The Impact Of The Left Inferior Frontal Gyrus On Fear Extinction: A Transcranial Direct Current Stimulation Study.
Ma, Y., Jiao, F., Batsikadze, G., Yavari, F., & Nitsche, M. A. (2024) · Brain Stimulation · doi:10.1016/j.brs.2024.07.004 · Cited by 9 · see citing works
Physiological reactions at encoding selectively predict recognition of emotional images.
Pilarczyk, J., Sterna, R., Schwertner, E., Pacula, B., Bartoszek, M., & Kuniecki, M. (2022) · Biological Psychology · doi:10.1016/j.biopsycho.2022.108429 · Cited by 9 · see citing works
Seven Tesla Evidence for Columnar and Rostral–Caudal Organization of the Human Periaqueductal Gray Response in the Absence of Threat: A Working Memory Study
Fischbach, A. K., Satpute, A. B., Quigley, K. S., Kragel, P. A., Chen, D., Bianciardi, M., Wald, L. L., Wager, T. D., Choi, J., Zhang, J., et al. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1757-23.2024 · Cited by 9 · see citing works
The neurocomputational link between defensive cardiac states and approach-avoidance arbitration under threat
Klaassen, F. H., de Voogd, L. D., Hulsman, A. M., O’Reilly, J. X., Klumpers, F., Figner, B., & Karin Roelofs, A. (2024) · Communications Biology · doi:10.1038/s42003-024-06267-6 · Cited by 9 · see citing works
Direct projection from the lateral habenula to the trigeminal mesencephalic nucleus in rats
Ohara, H., Tachibana, Y., Fujio, T., Takeda, R., Sato, F., Oka, A., Kato, T., Ikenoue, E., Yamashiro, T., & Yoshida, A. (2015) · Brain Research · doi:10.1016/j.brainres.2015.11.012 · Cited by 9 · see citing works
Incident experience predicts freezing-like responses in firefighters
Ly, V., Roijendijk, L., Hazebroek, H., Tonnaer, C., & Hagenaars, M. A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0186648 · Cited by 9 · see citing works
Facilitated extinction but impaired extinction recall by eye movement manipulation in humans – Indications for action mechanisms and the applicability of eye movement desensitization
Szeska, C., Mohrmann, H., & Hamm, A. O. (2022) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2022.12.009 · Cited by 8 · see citing works
Affective science and avoidant end-of-life communication: Can the science of emotion help physicians talk with their patients about the end of life?
Soodalter, J. A., Siegle, G. J., Klein‐Fedyshin, M., Arnold, R., & Schenker, Y. (2017) · Patient Education and Counseling · doi:10.1016/j.pec.2017.12.008 · Cited by 9 · see citing works
Subcortical modulation of the salience network during negative emotional processing in mood and anxiety disorders
Ince, S., Harrison, B. J., Felmingham, K. L., Jamieson, A. J., Davey, C. G., Agathos, J. A., Moffat, B. A., Glarin, R. K., & Steward, T. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03135-5 · Cited by 7 · see citing works
Investigation into the characteristics, triggers and mechanism of apnoea and bradycardia in the anaesthetized platypus (Ornithorhynchus anatinus)
Macgregor, J. W., Holyoake, C. S., Fleming, P. A., Robertson, I., Connolly, J. H., & Warren, K. S. (2014) · Conservation Physiology · doi:10.1093/conphys/cou053 · Cited by 7 · see citing works
The relevance of accounting for parasympathetic as well as sympathetic arousal in threat conditioning: Methodological and clinical considerations
Jaswetz, L., de Voogd, L. D., Becker, E. S., & Karin Roelofs, A. (2025) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2025.112561 · Cited by 7 · see citing works

Neural changes in control implementation of a continuous task
Lungu, O., Binenstock, M. M., Pline, M. A., Yeaton, J. R., & Carey, J. R. (2008) · Brain and Cognition · doi:10.1016/j.bandc.2008.02.057
Role played by periaqueductal gray neurons in parasympathetically mediated fear bradycardia in conscious rats
Koba, S., Inoue, R., & Watanabe, T. (2016) · Physiological Reports · doi:10.14814/phy2.12831 · Cited by 65 · see citing works
Freeze for action: neurobiological mechanisms in animal and human freezing
Roelofs, K. (2017) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2016.0206 · Cited by 616 · see citing works
Stimulation of the human periaqueductal gray induces threat bradycardia: a case report
Klaassen, F. H., de Voogd, L. D., Hulsman, A. M., Klumpers, F., Farrell, S., Green, A. L., van den Munckhof, P., & Karin Roelofs, A. (2026) · Figshare · doi:10.6084/m9.figshare.31932021
Serotonin and the heart of fear
Horder, J. (2020) · Nature Human Behaviour · doi:10.1038/s41562-020-0831-z

Authors: Hermans, E. J., Henckens, M. J. A. G., Roelofs, K., & Fernández, G.
Affiliations: Radboud University Nijmegen (NL)
Corresponding author: Hermans, Erno J.
ORCID: Hermans, Erno J.
Henckens, Marloes J.A.G.
Fernández, Guillén
Venue: NeuroImage
Publisher: Elsevier BV
Published: 2013-02
Volume: 66
Pages: 278-287
ISSN: 1053-8119 (ISSN-L)
DOI: 10.1016/j.neuroimage.2012.10.063
OpenAlex: W2151757477
Cited by: 151
References: 75
Citations by year: 2026: 13 · 2025: 10 · 2024: 9 · 2023: 7 · 2022: 12 · 2021: 8 · 2020: 9 · 2019: 14 · 2018: 10 · 2017: 18 · 2016: 15 · 2015: 13 · 2014: 10 · 2013: 2
FWCI: 4.10
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: NeuroImage (publishedVersion)
PubMed (publishedVersion)
Radboud Repository (Radboud University) (submittedVersion)
Funders: Netherlands Organisation for Scientific Research (NWO) (451.07.019, 918.66.613, 452.07.008)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: periaqueductal gray, freezing behavior, predator defense, parasympathetic activation, sympathetic activation, pupil dilation, autonomic responses, effective connectivity, anxiety disorders, motor inhibition
MeSH terms: Adult, Amygdala, Bradycardia, Brain Mapping, Fear, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Periaqueductal Gray, Freezing Reaction, Cataleptic, Young Adult

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Fear bradycardia and activation of the human periaqueductal grey

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