Daniel E.

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Polyvagal theory (poly- "many" + vagal "wandering") is a collection of unproven, evolutionary, neuroscientific, and psychological constructs pertaining to the role of the vagus nerve in emotion regulation, social connection and fear response, introduced in 1994 by Stephen Porges.

It is popular among some clinical practitioners and patients,[1] but is not endorsed by current social neuroscience.[2][3][4][5][6][7]

Polyvagal theory takes its name from the vagus, a cranial nerve that forms the primary component of the parasympathetic nervous system.[8][9][10] The traditional view of the autonomic nervous system presents a two-part system: the sympathetic nervous system, which is more activating (“fight or flight”), and the parasympathetic nervous system, which supports health, growth, and restoration (“rest and digest”). Polyvagal theory identifies a third type of nervous system response – the ‘social engagement system,’ a hybrid state of activation and calming that plays a role in our ability to socially engage (or not).

Polyvagal theory views the parasympathetic nervous system as being split into two distinct branches: a "ventral vagal system" which supports social engagement, and a "dorsal vagal system" which supports immobilisation behaviours, both “rest and digest” and defensive immobilisation or “shutdown”. Polyvagal theory was introduced by behavioral neuroscientist, Stephen W. Porges, in his presidential address to the Society of Psychophysiological Research in Atlanta, Georgia on October 8, 1994.

The talk was later published in Psychophysiology, 32 (1995) with the title Orienting in a defensive world: Mammalian modifications of our evolutionary heritage. A Polyvagal theory (Porges, 1995).[11]

Theory​

According to the theory, three organizational principles can be distinguished:

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  1. Hierarchy: The autonomic nervous system reacts in three reaction patterns, which are activated in a specific order.
  2. Neuroception: In contrast to perception, it is here a cognition without awareness, triggered by a stimulus such as danger.[12][13]
  3. Co-regulation: The need to feel safe enough to allow yourself to be in relationships, which is difficult for traumatized people.[14]
When it comes to immobilization, the decisive factor for Porges is whether immobile in safety or frozen because of the feedback of danger.

Porges describes the three neural circuits as regulators for reactive behavior. His findings about the ANS were taken into account e.g. in the modern therapy of childhood trauma and are used by trauma therapists such as Peter A. Levine and Marianne Bentzen. The "autonomy" of the vegetative self-regulation refers to the fact that biologically fixed, automatically running internal processes are adapted and regulated via the VNS, which can therefore not be consciously influenced directly by humans, but at most indirectly. This forms in the course of childhood and according to the suggestions of the parents or the caregivers. If the caregivers have a grown-up, developed system, then the child can also develop its resilience. However, if the caregiver is traumatized or has other impairments, the child cannot develop a stress-resistant adult nervous system.

The polyvagal theory is not simply a "theory of relaxation techniques" like autogenic training and others. According to the polyvagal theory, it is possible to strengthen a nervous system that has not yet grown up or has been dysregulated by trauma. You can use "pendulum exercises" for this: The principle is to intentionally bring yourself out of relaxation into light stress and then back into a safe state. By oscillating between these activation states, the nervous system will be trained and will find its way back to relaxation more quickly.[tone][citation needed]

Hypothesized phylogenetic subsystems/stages​

The vagus nerve is a primary component of the autonomic nervous system. The polyvagal theory focuses on the structure and function of the two efferent branches of the vagus cranial nerve, both of which originate from the medulla.[15] More specifically, each branch is claimed to be associated with a different adaptive behavioral strategy; the ventral branches are more restful in nature and the dorsal ones are more active in nature. The vagal system is claimed to be inhibitory of primal instincts by being part of the parasympathetic nervous system, and in opposition, the sympathetic-adrenal system is involved in mobilization behaviors. According to polyvagal theory, these opposing systems are phylogenetically ordered and activated for responses.[15]

Anatomical hypothesis​

The vagus, or tenth cranial nerve transmits parasympathetic signals to and from the heart, lungs, and digestive tract, a fact established before the middle of the 20th century.[16] "Polyvagal theory" was introduced in 1994 by Stephen Porges, director of the Brain-Body Center at the University of Illinois at Chicago. As has been established since the early days of neuroanatomy, the autonomic nervous system encompasses nerve fibers transmitting information from the body toward the brain, called afferent influences. According to polyvagal theory, this effect has been observed and demonstrated by adaptive reactivity dependent on the neural circuits' phylogenetical development.[citation needed] Polyvagal theory claims that human facial expressions are associated with, or reflect, physical reactions, such as cardiac and digestive changes.[17]

Porges argues this theory with observations from both evolutionary biology and neurology.[citation needed]

The branches of the vagal nerve are claimed to serve different evolutionary stress responses in mammals: the more primitive branch is said to elicit immobilization behaviors (e.g., feigning death), whereas the more evolved branch is said to be linked to social communication and self-soothing behaviors. These functions are claimed to follow a phylogenetichierarchy, where the most primitive systems are activated only when the more evolved functions fail. These neural pathways regulate autonomic states and the expression of emotional and social behaviour. Thus, according to this theory, physiological state dictates the range of behaviour and psychological experience.

Polyvagal theory makes broad claims on the nature of stress, emotion, and social behaviour, for the study of which peripheral indices of arousal such as heart rate, cortisol level and skin conductance have traditionally been used. Polyvagal theory champions the measurement of vagal tone in humans as a novel index of stress vulnerability and reactivity in populations with affective disorders.[18]

The proposed dorsal vagal complex (DVC)​

The dorsal branch of the vagus nerve originates in the dorsal motor nucleus and is postulated by polyvagal theory to be the phylogenetically older branch.[19][dubiousdiscuss] This branch is unmyelinated and exists in most vertebrates. Polyvagal theory calls this the "vegetative vagus" because it sees it as being associated with primal survival strategies of primitive vertebrates, reptiles, and amphibians.[19] Under certain conditions, these animals "freeze" when threatened, conserving their metabolic resources. This draws on the simplifying claims of the triune brain theory which are no longer considered accurate due to the many exceptions to this rule (See Triune brain – Status of the model for more).

The DVC provides primary control of subdiaphragmatic visceral organs, such as the digestive tract. Under normal conditions, the DVC maintains regulation of these digestive processes. However, prolonged disinhibition can be lethal for mammals, as it results in apnea and bradycardia.[15][dubiousdiscuss]

The proposed ventral vagal complex (VVC)​

With increased neural complexity as seen in mammals (due to phylogenetic development) there is said to have evolved a more sophisticated system to enrich behavioral and affective responses to an increasingly complex environment.[15][dubiousdiscuss] The ventral branch of the vagus originates in the nucleus ambiguus and is myelinated to provide more speed in responding.[15] Polyvagal theory calls this the "smart vagus" because it associates it with the regulation of sympathetic "fight or flight" behaviors by way of social affiliative behaviors.[19] These behaviors are said to include social communication and self-soothing and calming.[15] In other words, this branch of the vagus is said to inhibit or disinhibit defensive limbic circuits, depending on the situation. Note: Attributing defensive behaviours purely to the limbic system is an oversimplification, as these are triggered by perceived threats, thus requiring an interplay of brain areas performing sensory integration, memory, and semantic knowledge with the limbic system to be elicited. Similarly, the regulation of emotionsrequires a complex interplay of higher cognitive areas with limbic ones. The vagus nerve mediates the control of supradiaphragmatic visceral organs, such as the esophagus, bronchi, pharynx, and larynx. It also exerts an important influence on the heart. When vagal tone to the heart’s pacemaker is high, a baseline or resting heart rate is produced. In other words, the vagus acts as a restraint, or brake, limiting heart rate. However, when vagal tone is removed, there is little inhibition to the pacemaker, and according to polyvagal theory, rapid mobilization ("fight/flight") can be activated in times of stress, but without having to engage the sympathetic-adrenal system, as activation comes at a severe biological cost.[15]Note: While the vagus nerve's role in downregulating the heart rate is well-established, the notion that a Fight-or-flight response can be triggered without engaging the sympathetic nervous system is not substantiated by any evidence.

Vagal tone as a physiological marker of stress​

In order to maintain homeostasis, the central nervous system responds constantly, via neural feedback, to environmental cues. Stressful events disrupt the rhythmic structure of autonomic states, and subsequently, behaviors. Since the vagus plays such an integral role in the peripheral nervous system via regulation of heart rate, Porges suggests that the amplitude of respiratory sinus arrhythmia (RSA) is a good index of parasympathetic nervous system activity via the cardiac vagus.[20]That is, RSA is proposed as a measurable, noninvasive way to see how the vagus modulates heart rate activity in response to stress. If true, this method could be useful to measure individual differences in stress reactivity.

RSA is the widely used measure of the amplitude of heart rate rhythm associated with the rate of spontaneous breathing.[20]Research has shown that amplitude of RSA is an accurate indicator of the efferent influence of the vagus on the heart.[20]Since inhibitory effects of the VVC branch of the vagus allow for a wide range of adaptive, prosocial behaviors, it has been theorized that individuals with greater vagal tone are able to exhibit a greater range of such behaviors. On the other hand, decreased vagal tone is associated with illnesses and medical complications that compromise the CNS.[20] These complications may reduce one's capacity to respond to stress appropriately.

Clinical applications in the human fetus​

Healthy human fetuses have high variability in heart rate, which is mediated by the vagus.[21] On the other hand, heart rate decelerations, which are also mediated by the vagus, are a sign of fetal distress. More specifically, prolonged withdrawal of vagal influence on the heart creates a physiological vulnerability to the influence of the Dorsal Vagal Control, which in turn produces bradycardia (very low heart rate). However, the onset of this deceleration is commonly preceded by transitory tachycardia, which is reflective of the immediate effects of Ventral Vagal Control withdrawal.

Results of Porges' theory​

According to Bessel van der Kolk, professor of psychiatry at the Boston University School of Medicine:[22]

The Polyvagal Theory provided us with a more sophisticated understanding of the biology of safety and danger, one based on the subtle interplay between the visceral experiences of our own bodies and the voices and faces of the people around us. It explains why a kind face or a soothing tone of voice can dramatically alter the way we feel. It clarifies why knowing that we are seen and heard by the important people in our lives can make us feel calm and safe, and why being ignored or dismissed can precipitate rage reactions or mental collapse. It helped us understand why attuning with another person can shift us out of disorganized and fearful states. In short, Porges's theory makes us look beyond the effects of fight or flight and put social relationships front and centre in our understanding of trauma. It also suggested new approaches to healing that focus on strengthening the body’s system for regulating arousal.
Others[who?] disagree with this assessment and would consider the theory an unnecessary and unsubstantiated conflict imposed on the public dialogue.

Criticism​

Polyvagal theory has not, to date, been shown to explain any phenomena or experimental data above and beyond what is explained more precisely by attachment theory, research on emotional self-regulation, psychological stress models, the Neurovisceral Integration Model[23][24] and neuroimaging studies from the field of social neuroscience. Its appeal may lie in the fact that it provides a very simple (if inaccurate) neural/evolutionary backstory to already well-established psychiatric knowledge.

Inconsistencies and lack of evidence​

Critics of the polyvagal theory point out that its premises are not supported by empirical, scientific research. Paul Grossman of University Hospital Basel argues that there is no evidence that the dorsal motor nucleus (DMN) is an evolutionarily more primitive center of the brainstem parasympathetic system than the nucleus ambiguus (NA), and that no evidence supports the claim that sudden decrease in heart rate elicited by extreme emotional circumstances (like trauma-related dissociation) is due to DMN efferent activity to the heart.[25] In fact, there seems to be no evidence that such decrease happens in trauma-related dissociation in the first place.

Grossman also points out that even the results of Porges' own study on two species of lizard was flawed due to inappropriate measurement of heart rate variability.[25]

While Grossman's criticism does not address the clinical speculations of the polyvagal theory directly, it contradicts its premises. In particular, it undermines the suggestion that there is a phylogenetic hierarchy, where one vagal system is more primitive than the other, and therefore is activated only when the more evolved one fails (as in dissociation, or acute trauma). It has been known for roughly a century that "a differentiation of the visceral efferent column of the vagus nerve into a dorsal motor nucleus and a ventrolateral nucleus (nucleus ambiguus) is first seen in reptiles (Ariens Kappers, '12; Ariens Kappers et al., '36; Addens, '33)".[26] This contradicts the polyvagal claim of the nucleus ambiguus being unique to mammals.[27] More recent findings in lungfish of myelinated vagus nerve fibres leading from the nucleus ambiguus to the heart point in the same direction.[28][29] Furthermore, Monteiro et al. (2018) state that "the mechanisms [Porges] identifies as solely mammalian are undeniably present in the lungfish that sits at the evolutionary base of the air-breathing vertebrates."[28]

In polyvagal theory the term vagal tone is equated with respiratory sinus arrhythmia (RSA), which is suggested to be linked to dimensions of psychopathology. A number of research studies have evaluated RSA responses across a range of dimensions of psychopathology, but a comprehensive meta-analysis has shown that no clinically meaningful relation can be found between psychopathology and RSA reactivity.[30] Grossman & Taylor (2005) reviewed findings indicating that RSA is not a reliable marker of vagal tone, being subject to both respiratory variables and sympathetic (beta-adrenergic) influences in addition to vagal influences.[31]

By overemphasizing the role of the vagus nerve in deciding between freezing and other fear responses, the theory disregards decades of neuroscientific findings on the origins of the freeze response[32] and fear responses in general.[33]While the vagus nerve undoubtedly plays a role in transmitting and integrating emotion-related signals between the brain and the rest of the body (a fact established long before the emergence of polyvagal speculations, see Vagusstoff), there is no evidence to suggest that it has any control over whether a freeze response is triggered or not.

From a methodological perspective, many claims do not meet the criteria of a scientific theory because they are formulated in a manner too vague for empirical testing. For example, the precise functioning of the two proposed distinct "vagal systems" or of the "social engagement system" is not explained,[17] nor is that of the "face-heart connection" supposedly embodied in the ventral branch of the vagus nerve. Furthermore, the claims do not explain any findings beyond what is more precisely explained by Thayer's Neurovisceral Integration Model.[23]

While other brain areas known to be involved in fear responses (e. g. the amygdala and periaqueductal gray[32][33]) are mentioned by Porges, he does not integrate them into the description of his own hypothesized systems. The proposed anatomical difference between the vagus nerve origins of mammals vs. other vertebrates, even if it were borne out by more recent studies, would be an insufficient basis for explaining complex social and emotional behaviour differences.

In addition, polyvagal theory introduces the term "neuroception" for "a neural process that enables humans and other mammals to engage in social behaviors by distinguishing safe from dangerous contexts".[17] It thus attempts to encompass several categories of psychological phenomena, each one of which constitutes a broad field of research in its own right: fear, threat perception, social behaviour, and emotion regulation. The neural substrates for many of the included phenomena are known at least tentatively, and comprise a large number of brain structures including, but not limited to, the vagus nerve. Polyvagal theory does not explain the mechanism of any of these phenomena with any precision, resulting in an oversimplification rather than an expansion or refinement of existing knowledge.

Books​

  • Deb Dana: The Polyvagal Theory in Therapy, Engaging the Rhythm of Regulation (Norton Series on Interpersonal Neurobiology, Band 0), WW Norton & Co; Illustrated Edition (2018), ISBN 978-0393712377
  • Ulrich F. Lanius, Sandra L. Paulsen, Frank M. Corrigan: Neurobiology and Treatment of Traumatic Dissociation: Towards an Embodied Self Springer Publishing Company, 2014 www.books.google.de
  • S. W. Porges: The polyvagal perspective. In: Biological psychology. Band 74, Nummer 2, Februar 2007, S. 116–143, doi:10.1016/j.biopsycho.2006.06.009, PMID 17049418, PMC 1868418 (Review).
  • Holly Bridges: Reframe Your Thinking Around Autism: How the Polyvagal Theory and Brain Plasticity Help Us Make Sense of Autism ISBN 978-1849056724 Jessica Kingsley Publishers 2015
  • Robert Bright: The Polyvagal Theory: The Simplified Guide to Understanding the Autonomic Nervous System and the Healing Power of the Vagus Nerve - Learn to Manage Emotional Stress and PTSD Through Neurobiology White Publishing Ltd 2020, ISBN 978-1-80111-968-9

See also​

References​

  1. ^ "Polyvagal theory in practice". Counseling Today. 2016-06-27. Retrieved 2020-10-31.
  2. ^ Todorov, Alexander; Fiske, Susan; Prentice, Deborah (2011). Social Neuroscience: Toward Understanding the Underpinnings of the Social Mind. Oxford University Press. ISBN 978-0-19-972406-2.[page needed]
  3. ^ Ward, Jamie (2016). The Student's Guide to Social Neuroscience. Psychology Press. ISBN 978-1-317-43918-9.[page needed]
  4. ^ Schutt, Russell K.; Seidman, Larry J.; Keshavan, Matcheri S. (2015). Social Neuroscience: Brain, Mind, and Society. Harvard University Press. ISBN 978-0-674-72897-4.[page needed] Litfin, Karen T.; Berntson, Gary G. (2006). Social Neuroscience: People Thinking about Thinking People. MIT Press. ISBN 978-0-262-03335-0.[page needed]
  5. ^ Baron-Cohen, Simon; Tager-Flusberg, Helen; Lombardo, Michael (2013). Understanding Other Minds: Perspectives from Developmental Social Neuroscience. OUP Oxford. ISBN 978-0-19-969297-2.[page needed]
  6. ^ Cacioppo, Stephanie; Cacioppo, John T. (2020). Introduction to Social Neuroscience. Princeton University Press. ISBN 978-0-691-16727-5.[page needed]
  7. ^ Decety, Jean; Cacioppo, John T. (2011). The Oxford Handbook of Social Neuroscience. Oxford University Press. ISBN 978-0-19-534216-1.[page needed]
  8. ^ Anthony, Andrew. "Stephen Porges: 'Survivors are blamed because they don't fight". The Guardian. Retrieved 2021-09-17.
  9. ^ Brookes, David (2019-11-28). "The Wisdom Your Body Knows". The New York Times. ISSN 0362-4331. Retrieved 2021-09-17.
  10. ^ Quinn, Robert E.; Fessell, David P.; Porges, Stephen W. (2021-01-15). "How to Keep Your Cool in High-Stress Situations". Harvard Business Review. ISSN 0017-8012. Retrieved 2021-09-19.
  11. ^ The Polyvagal Theory, Retrieved 2022-03-02
  12. ^ Porges, Stephen W. (2009). "The polyvagal theory: New insights into adaptive reactions of the autonomic nervous system". Cleveland Clinic Journal of Medicine. 76 (Suppl 2): S86–S90. doi:10.3949/ccjm.76.s2.17. ISSN 0891-1150. PMC 3108032. PMID 19376991.
  13. ^ Essex, Tori. "New Episode of Transforming Trauma: The Rhythm of Regulation: Exploring the Polyvagal Theory with Deb Dana". PACEsConnection. Retrieved 2022-01-21.
  14. ^ Den Dana: The Polyvagal Theory in Therapy, p. 20
  15. ^ Jump up to: a b c d e f g Porges, Stephen W. (October 2001). "The polyvagal theory: phylogenetic substrates of a social nervous system". International Journal of Psychophysiology. 42 (2): 123–146. doi:10.1016/S0167-8760(01)00162-3. ISSN 0167-8760. PMID 11587772.
  16. ^ Dale, H. H.; Feldberg, W. (1934). "The chemical transmitter of vagus effects to the stomach". The Journal of Physiology. 81 (3): 320–334. doi:10.1113/jphysiol.1934.sp003138. ISSN 1469-7793. PMC 1394148. PMID 16994546.
  17. ^ Jump up to: a b c Porges, Stephen W. (April 2009). "The polyvagal theory: New insights into adaptive reactions of the autonomic nervous system". Cleveland Clinic Journal of Medicine. 76 (Supplement 2): S86–S90. doi:10.3949/ccjm.76.s2.17. ISSN 1939-2869. PMC 3108032. PMID 19376991.
  18. ^ Connell, Arin M.; Hughes-Scalise, Abigail; Klostermann, Susan; Azem, Talla (2011). "Maternal depression and the heart of parenting: Respiratory sinus arrhythmia and affective dynamics during parent–adolescent interactions". Journal of Family Psychology. 25 (5): 653–662. doi:10.1037/a0025225. PMID 21875198.
  19. ^ Jump up to: a b c Beauchaine, Theodore P; Gatzke-Kopp, Lisa; Mead, Hilary K (February 2007). "Polyvagal Theory and developmental psychopathology: Emotion dysregulation and conduct problems from preschool to adolescence". Biological Psychology. 7 (2): 174–184. doi:10.1016/j.biopsycho.2005.08.008. ISSN 0301-0511. PMC 1801075. PMID 17045726.
  20. ^ Jump up to: a b c d Porges, Stephen W. (2011). The Polyvagal Theory: Neurophysiological Foundations of Emotions, Attachment, Communication, and Self-regulation. W. W. Norton & Company. ISBN 978-0-3937-0700-7.[page needed]
  21. ^ Reed, Shawn F.; Ohel, Gonen; David, Rahav; Porges, Stephen W. (September 1999). "A neural explanation of fetal heart rate patterns: A test of the polyvagal theory". Developmental Psychobiology. 35 (2): 108–118. doi:10.1002/(SICI)1098-2302(199909)35:2<108::AID-DEV4>3.0.CO;2-N. ISSN 1098-2302. PMID 10461125.
  22. ^ Van Der Kolk, Bessel (2014). The body keeps the score: brain, mind, and body in the healing of trauma. New York: Viking Penguin. p. 80. ISBN 9780670785933. Retrieved 3 February 2018.
  23. ^ Jump up to: a b Thayer (2009). "Heart Rate Variability: A Neurovisceral Integration Model". Encyclopedia of Neuroscience: 1041–1047. doi:10.1016/B978-008045046-9.01991-4. ISBN 9780080450469.
  24. ^ Smith (2017). "The hierarchical basis of neurovisceral integration". Neuroscience and Biobehavioral Reviews. 75: 274–296. doi:10.1016/j.neubiorev.2017.02.003. PMID 28188890. S2CID 24169508.
  25. ^ Jump up to: a b Grossman, Paul; Taylor, Edwin W. (2007-02-01). "Toward understanding respiratory sinus arrhythmia: Relations to cardiac vagal tone, evolution and biobehavioral functions". Biological Psychology. 74 (2): 263–285. doi:10.1016/j.biopsycho.2005.11.014. ISSN 0301-0511. PMID 17081672. S2CID 16818862.
  26. ^ Barbas-Henry, Heleen (1984). "The Motor Nuclei and Primary Projections of the IXth, Xth, XIth, and XIIth Cranial Nerves in the Monitor Lizard, Varanus exanthematicus". Journal of Comparative Neurology. 226 (4): 565–579. doi:10.1002/cne.902260409. PMID 6747035. S2CID 31092668.
  27. ^ Taylor, E. W.; Al-Ghamdi, M. S.; Ihmied, I. H.; Wang, T.; Abe, A. S. (November 2001). "Physiological Society Symposium – Vagal Control: From Axolotl to Man: The neuranatomical basis of central control of cardiorespiratory interactions in vertebrates". Experimental Physiology. 86 (6): 771–776. doi:10.1111/j.1469-445x.2001.tb00043.x. PMID 11698972. S2CID 86840074.
  28. ^ Jump up to: a b Monteiro, Diana (2018). "Cardiorespiratory interactions previously identified as mammalian are present in the primitive lungfish". Science Advances. 4 (2): eaaq0800. Bibcode:2018SciA....4..800M. doi:10.1126/sciadv.aaq0800. PMC 5833999. PMID 29507882.
  29. ^ Taylor, E. W. (2010). "Autonomic control of cardiorespiratory interactions in fish, amphibians and reptiles". Brazilian Journal of Medical and Biological Research. 43 (7): 600–610. doi:10.1590/S0100-879X2010007500044. PMID 20464342.
  30. ^ Beauchaine, Theodore P.; Bell, Ziv; Knapton, Erin; McDonough‐Caplan, Heather; Shader, Tiffany; Zisner, Aimee (2019). "Respiratory sinus arrhythmia reactivity across empirically based structural dimensions of psychopathology: A meta-analysis". Psychophysiology. 56 (5): e13329. doi:10.1111/psyp.13329. ISSN 1469-8986. PMC 6453712. PMID 30672603.
  31. ^ Grossman, Paul; Taylor, Edwin W. (February 2007). "Toward understanding respiratory sinus arrhythmia: Relations to cardiac vagal tone, evolution and biobehavioral functions". Biological Psychology. 74 (2): 263–285. doi:10.1016/j.biopsycho.2005.11.014. PMID 17081672. S2CID 16818862.
  32. ^ Jump up to: a b Roelofs, Karin (2017). "Freeze for action: neurobiological mechanisms in animal and human freezing". Philosophical Transactions of the Royal Society B: Biological Sciences. 372 (1718). doi:10.1098/rstb.2016.0206. PMC 5332864. PMID 28242739.
  33. ^ Jump up to: a b Johansen, Joshua (2010). "Neural substrates for expectation-modulated fear learning in the amygdala and periaqueductal gray". Nature Neuroscience. 13 (8): 979–986. doi:10.1038/nn.2594. PMC 2910797. PMID 20601946.

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