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Anticipation and the Neural Response to Threat

  • Nathaniel G. Harnett
  • Kimberly H. Wood
  • Muriah D. Wheelock
  • Amy J. Knight
  • David C. KnightEmail author
Chapter
  • 559 Downloads

Abstract

An important function of emotion is that it allows one to respond more effectively to threats in our environment. The response to threat is an important aspect of emotional behavior given the direct biological impact it has on survival. More specifically, survival is dependent upon the ability to avoid, escape, or defend against a threat once it is encountered. Anticipatory processes supported by neural circuitry that includes the prefrontal cortex and amygdala are critical for the expression and regulation of the emotional response. Further, these anticipatory processes appear to regulate the response to the threat itself. Healthy emotional function is characterized by anticipatory processes that diminish the emotional response to threat. In contrast, emotional dysfunction is characterized by anticipatory processes that lead to an exaggerated threat response. Thus, anticipatory mechanisms play an important role in both healthy and dysfunctional emotional behavior.

Keywords

Anticipation Conditioning Fear Emotion Threat Regulation 

References

  1. 1.
    Delgado, M.R., Nearing, K.I., LeDoux, J.E., Phelps, E.A.: Neural circuitry underlying the regulation of conditioned fear and its relation to extinction. Neuron 59, 829–838 (2008)CrossRefGoogle Scholar
  2. 2.
    Knight, D.C., Cheng, D.T., Smith, C.N., Stein, E.A., Helmstetter, F.J.: Neural substrates mediating human delay and trace fear conditioning. J. Neurosci. 24, 218–228 (2004)CrossRefGoogle Scholar
  3. 3.
    Knight, D.C., Smith, C.N., Stein, E.A., Helmstetter, F.J.: Functional MRI of human Pavlovian fear conditioning: patterns of activation as a function of learning. NeuroReport 10, 3665–3670 (1999)CrossRefGoogle Scholar
  4. 4.
    LeDoux, J.E.: Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155–184 (2000)CrossRefGoogle Scholar
  5. 5.
    Wagner, A. R., Brandon, S. E., Klein, S., Mowrer, R.: Evolution of a structured connectionist model of Pavlovian conditioning (AESOP). Contemporary learning theories: Pavlovian conditioning and the status of traditional learning theory 149–189 (1989)Google Scholar
  6. 6.
    Critchley, H.D., Elliott, R., Mathias, C.J., Dolan, R.J.: Neural activity relating to generation and representation of galvanic skin conductance responses: a functional magnetic resonance imaging study. J. Neurosci. 20, 3033–3040 (2000)Google Scholar
  7. 7.
    Knight, D.C., Nguyen, H.T., Bandettini, P.A.: The role of the human amygdala in the production of conditioned fear responses. Neuroimage 26, 1193–1200 (2005)CrossRefGoogle Scholar
  8. 8.
    Lykken, D.T., Venables, P.H.: Direct measurement of skin conductance: a proposal for standardization. Psychophysiology 8, 656–672 (1971)CrossRefGoogle Scholar
  9. 9.
    Mangina, C.A., Beuzeron-Mangina, J.H.: Direct electrical stimulation of specific human brain structures and bilateral electrodermal activity. Int. J. Psychophysiol. 22, 1–8 (1996)CrossRefGoogle Scholar
  10. 10.
    Domjan, M.: Pavlovian conditioning: a functional perspective. Annu. Rev. Psychol. 56, 179–206 (2005)CrossRefGoogle Scholar
  11. 11.
    Franchina, J.J.: Escape behavior and shock intensity: within-subject versus between-groups comparisons. J. Comp. Physiol. Psychol. 69, 241–245 (1969)CrossRefGoogle Scholar
  12. 12.
    Helmstetter, F.J., Bellgowan, P.S.: Lesions of the amygdala block conditional hypoalgesia on the tail flick test. Brain Res. 612, 253–257 (1993)CrossRefGoogle Scholar
  13. 13.
    Kamin, L.J.: Traumatic avoidance learning: the effects of CS-US interval with a trace-conditioning procedure. J. Comp. Physiol. Psychol. 47, 65–72 (1954)CrossRefGoogle Scholar
  14. 14.
    Kim, J.J., Jung, M.W.: Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review. Neurosci. Biobehav. Rev. 30, 188–202 (2006)CrossRefGoogle Scholar
  15. 15.
    Helmstetter, F.J.: The amygdala is essential for the expression of conditional hypoalgesia. Behav. Neurosci. 106, 518–528 (1992)CrossRefGoogle Scholar
  16. 16.
    Baxter, R.: Diminution and recovery of the UCR in delayed and trace classical GSR conditioning. J. Exp. Psychol. 71, 447–451 (1966)CrossRefGoogle Scholar
  17. 17.
    Dunsmoor, J.E., Bandettini, P.A., Knight, D.C.: Neural correlates of unconditioned response diminution during Pavlovian conditioning. Neuroimage 40, 811–817 (2008)CrossRefGoogle Scholar
  18. 18.
    Marcos, J.L., Redondo, J.: Effects of conditioned stimulus presentation on diminution of the unconditioned response in aversive classical conditioning. Biol. Psychol. 50, 89–102 (1999)CrossRefGoogle Scholar
  19. 19.
    Rust, J.: Unconditioned response diminution in the skin resistance response. J. Gen. Psychol. 95, 77–84 (1976)CrossRefGoogle Scholar
  20. 20.
    Knight, D.C., Waters, N.S., King, M.K., Bandettini, P.A.: Learning-related diminution of unconditioned SCR and fMRI signal responses. NeuroImage 49, 843–848 (2010)CrossRefGoogle Scholar
  21. 21.
    Canli, T., Detmer, W.M., Donegan, N.H.: Potentiation or diminution of discrete motor unconditioned responses (rabbit eyeblink) to an aversive pavlovian unconditioned stimulus by two associative processes: conditioned fear and a conditioned diminution of unconditioned stimulus processing. Behav. Neurosci. 106, 498–508 (1992)CrossRefGoogle Scholar
  22. 22.
    Canli, T., Donegan, N.H.: Conditioned diminution of the unconditioned response in rabbit eyeblink conditioning: Identifying neural substrates in the cerebellum and brainstem. Behav. Neurosci. 109, 874–892 (1995)CrossRefGoogle Scholar
  23. 23.
    Knight, D.C., Lewis, E.P., Wood, K.H.: Conditioned diminution of the unconditioned skin conductance response. Behav. Neurosci. 125, 626–631 (2011)Google Scholar
  24. 24.
    Wood, K. H., Kuykendall, D., Ver Hoef, L. W., Knight, D. C.: Neural substrates underlying learning-related changes of the unconditioned fear response. Open Neuroimaging J. 7, 41–52 (2013)Google Scholar
  25. 25.
    Wood, K. H., Ver Hoef, L. W., Knight, D. C.: Neural mechanisms underlying the conditioned diminution of the unconditioned fear response. Neuroimage 60, 787–799 (2012)Google Scholar
  26. 26.
    Kimmel, E.: Judgments of UCS intensity and diminution of the UCR in classical GSR conditioning. J. Exp. Psychol. 73, 532–543 (1967)CrossRefGoogle Scholar
  27. 27.
    Rescorla, R.A.: Pavlovian conditioning: It’s not what you think it is. Am. Psychol. 43, 151–160 (1988)CrossRefGoogle Scholar
  28. 28.
    Rescorla, R. A., Wagner, A. R.: A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. Class. Conditioning: Current Res. Theory (1972)Google Scholar
  29. 29.
    Amaral, D. G., Price, J. L., Pitkanen, A., Carmichael, S. T.: Anatomical organization of the primate amygdaloid complex. In: The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction 1–66 (1992)Google Scholar
  30. 30.
    Cheng, D.T., Knight, D.C., Smith, C.N., Helmstetter, F.J.: Human amygdala activity during the expression of fear responses. Behav. Neurosci. 120, 1187–1195 (2006)CrossRefGoogle Scholar
  31. 31.
    Cheng, D.T., Knight, D.C., Smith, C.N., Stein, E.A., Helmstetter, F.J.: Functional MRI of human amygdala activity during Pavlovian fear conditioning: stimulus processing versus response expression. Behav. Neurosci. 117, 3–10 (2003)CrossRefGoogle Scholar
  32. 32.
    Davis, M., Walker, D.L., Miles, L., Grillon, C.: Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 35, 105–135 (2010)CrossRefGoogle Scholar
  33. 33.
    Knight, D.C., Nguyen, H.T., Bandettini, P.A.: The role of awareness in delay and trace fear conditioning in humans. Cogn. Affect. Behav. Neurosci. 6, 157–162 (2006)CrossRefGoogle Scholar
  34. 34.
    LeDoux, J.E., Cicchetti, P., Xagoraris, A., Romanski, L.M.: The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J. Neurosci. 10, 1062–1069 (1990)Google Scholar
  35. 35.
    Fendt, M., Fanselow, M.: The neuroanatomical and neurochemical basis of conditioned fear. Neurosci. Biobehav. Rev. 23, 743–760 (1999)CrossRefGoogle Scholar
  36. 36.
    Urry, H.L., Van Reekum, C.M., Johnstone, T., Kalin, N.H., Thurow, M.E., Schaefer, H.S., Jackson, C.A., Frye, C.J., Greischar, L.L., Alexander, A.L.: Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. J. Neurosci. 26, 4415–4425 (2006)CrossRefGoogle Scholar
  37. 37.
    Büchel, C., Morris, J., Dolan, R.J., Friston, K.J.: Brain systems mediating aversive conditioning: an event-related fMRI study. Neuron 20, 947–957 (1998)CrossRefGoogle Scholar
  38. 38.
    Dunsmoor, J.E., Bandettini, P.A., Knight, D.C.: Impact of continuous versus intermittent CS-UCS pairing on human brain activation during Pavlovian fear conditioning. Behav. Neurosci. 121, 635–642 (2007)CrossRefGoogle Scholar
  39. 39.
    Hugdahl, K., Berardi, A., Thompson, W.L., Kosslyn, S.M., Macy, R., Baker, D.P., Alpert, N.M., LeDoux, J.E.: Brain mechanisms in human classical conditioning: a PET blood flow study. NeuroReport 6, 1723–1728 (1995)CrossRefGoogle Scholar
  40. 40.
    Knight, D.C., Smith, C.N., Cheng, D.T., Stein, E.A., Helmstetter, F.J.: Amygdala and hippocampal activity during acquisition and extinction of human fear conditioning. Cogn. Affect. Behav. Neurosci. 4, 317–325 (2004)CrossRefGoogle Scholar
  41. 41.
    Knight, D.C., Waters, N.S., Bandettini, P.A.: Neural substrates of explicit and implicit fear memory. Neuroimage 45, 208–214 (2009)CrossRefGoogle Scholar
  42. 42.
    Wheelock, M., Sreenivasan, K., Wood, K., Ver Hoef, L., Deshpande, G., Knight, D.: Threat-related learning relies on distinct dorsal prefrontal cortex network connectivity. NeuroImage 102, 904–912 (2014)Google Scholar
  43. 43.
    Wood, K. H., Wheelock, M. D., Shumen, J. R., Bowen, K. H., VerHoef, L. W., Knight, D. C.: Controllability modulates the neural response to predictable but not unpredictable threat in humans. NeuroImage 119, 371–381 (2015)Google Scholar
  44. 44.
    Baratta, M.V., Zarza, C.M., Gomez, D.M., Campeau, S., Watkins, L.R., Maier, S.F.: Selective activation of dorsal raphe nucleus-projecting neurons in the ventral medial prefrontal cortex by controllable stress. Eur. J. Neurosci. 30, 1111–1116 (2009)CrossRefGoogle Scholar
  45. 45.
    Amat, J., Matus-Amat, P., Watkins, L.R., Maier, S.F.: Escapable and inescapable stress differentially and selectively alter extracellular levels of 5-HT in the ventral hippocampus and dorsal periaqueductal gray of the rat. Brain Res. 797, 12–22 (1998)CrossRefGoogle Scholar
  46. 46.
    Baratta, M.V., Christianson, J.P., Gomez, D.M., Zarza, C.M., Amat, J., Masini, C.V., Watkins, L.R., Maier, S.F.: Controllable versus uncontrollable stressors bi-directionally modulate conditioned but not innate fear. Neuroscience 146, 1495–1503 (2007)CrossRefGoogle Scholar
  47. 47.
    Baratta, M.V., Lucero, T.R., Amat, J., Watkins, L.R., Maier, S.F.: Role of the ventral medial prefrontal cortex in mediating behavioral control-induced reduction of later conditioned fear. Learn. Mem. 15, 84–87 (2008)CrossRefGoogle Scholar
  48. 48.
    Amat, J., Paul, E., Watkins, L.R., Maier, S.F.: Activation of the ventral medial prefrontal cortex during an uncontrollable stressor reproduces both the immediate and long-term protective effects of behavioral control. Neuroscience 154, 1178–1186 (2008)CrossRefGoogle Scholar
  49. 49.
    Maier, S.F., Amat, J., Baratta, M.V., Paul, E., Watkins, L.R.: Behavioral control, the medial prefrontal cortex, and resilience. Dialogues Clin. Neurosci. 8, 397–407 (2006)Google Scholar
  50. 50.
    Rauch, S.L., Shin, L.M., Phelps, E.A.: Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research–past, present, and future. Biol. Psychiatry 60, 376–382 (2006)CrossRefGoogle Scholar
  51. 51.
    Milad, M.R., Wright, C.I., Orr, S.P., Pitman, R.K., Quirk, G.J., Rauch, S.L.: Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol. Psychiatry 62, 446–454 (2007)CrossRefGoogle Scholar
  52. 52.
    Hartley, C.A., Phelps, E.A.: Changing fear: the neurocircuitry of emotion regulation. Neuropsychopharmacology 35, 136–146 (2010)CrossRefGoogle Scholar
  53. 53.
    Schiller, D., Kanen, J.W., LeDoux, J.E., Monfils, M.-H., Phelps, E.A.: Extinction during reconsolidation of threat memory diminishes prefrontal cortex involvement. Proc. Natl. Acad. Sci. USA 110, 20040–20045 (2013)CrossRefGoogle Scholar
  54. 54.
    Milad, M.R., Pitman, R.K., Ellis, C.B., Gold, A.L., Shin, L.M., Lasko, N.B., Zeidan, M.A., Handwerger, K., Orr, S.P., Rauch, S.L.: Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol. Psychiatry 66, 1075–1082 (2009)CrossRefGoogle Scholar
  55. 55.
    Etkin, A., Wager, T. D.: Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am. J. Psychiatry 164, 1476–1488 (2007)Google Scholar
  56. 56.
    Indovina, I., Robbins, T.W., Núñez-Elizalde, A.O., Dunn, B.D., Bishop, S.J.: Fear-conditioning mechanisms associated with trait vulnerability to anxiety in humans. Neuron 69, 563–571 (2011)CrossRefGoogle Scholar
  57. 57.
    Phan, K.L., Fitzgerald, D.A., Nathan, P.J., Tancer, M.E.: Association between amygdala hyperactivity to harsh faces and severity of social anxiety in generalized social phobia. Biol. Psychiatry 59, 424–429 (2006)CrossRefGoogle Scholar
  58. 58.
    Lissek, S., Powers, A.S., McClure, E.B., Phelps, E.A., Woldehawariat, G., Grillon, C., Pine, D.S.: Classical fear conditioning in the anxiety disorders: a meta-analysis. Behav. Res. Ther. 43, 1391–1424 (2005)CrossRefGoogle Scholar
  59. 59.
    Milad, M.R., Orr, S.P., Lasko, N.B., Chang, Y., Rauch, S.L., Pitman, R.K.: Presence and acquired origin of reduced recall for fear extinction in PTSD: results of a twin study. J. Psychiatr. Res. 42, 515–520 (2008)CrossRefGoogle Scholar
  60. 60.
    Milad, M.R., Rauch, S.L., Pitman, R.K., Quirk, G.J.: Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol. Psychol. 73, 61–71 (2006)CrossRefGoogle Scholar
  61. 61.
    Bremner, J.D., Vermetten, E., Vythilingam, M., Afzal, N., Schmahl, C., Elzinga, B., Charney, D.S.: Neural correlates of the classic color and emotional stroop in women with abuse-related posttraumatic stress disorder. Biol. Psychiatry 55, 612–620 (2004)CrossRefGoogle Scholar
  62. 62.
    Haas, B.W., Garrett, A., Song, S., Reiss, A.L., Carrio, V.G.: Reduced hippocampal activity in youth with posttraumatic stress symptoms: an fMRI study. J. Pediatr. Psychol. 35, 559–569 (2010)CrossRefGoogle Scholar
  63. 63.
    Jovanovic, T., Ressler, K.J.: How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD. Am. J. Psychiatry 167, 648–662 (2010)CrossRefGoogle Scholar
  64. 64.
    Briscione, M.A., Jovanovic, T., Norrholm, S.D.: Conditioned fear associated phenotypes as robust, translational indices of trauma-, stressor-, and anxiety-related behaviors. Front. Psychiatry 5, 1–9 (2014)CrossRefGoogle Scholar
  65. 65.
    Robison-Andrew, E.J., Duval, E.R., Nelson, C.B., Echiverri-Cohen, A., Giardino, N., Defever, A., Norrholm, S.D., Jovanovic, T., Rothbaum, B.O., Liberzon, I., Rauch, S.A.M.: Changes in trauma-potentiated startle with treatment of posttraumatic stress disorder in combat Veterans. J. Anxiety Disord. 28, 358–362 (2014)CrossRefGoogle Scholar
  66. 66.
    Sripada, R.K., King, A.P., Welsh, R.C., Garfinkel, S.N., Wang, X., Sripada, C.S., Liberzon, I.: Neural dysregulation in posttraumatic stress disorder: evidence for disrupted equilibrium between salience and default mode brain networks. Psychosom. Med. 74, 904–911 (2012)CrossRefGoogle Scholar
  67. 67.
    Birn, R.M., Patriat, R., Phillips, M.L., Germain, A., Herringa, R.J.: Childhood maltreatment and combat posttraumatic stress differentially predict fear-related fronto-subcortical connectivity. Depress. Anxiety 31, 880–892 (2014)CrossRefGoogle Scholar
  68. 68.
    Gilmartin, M. R., Balderston, N. L., Helmstetter, F. J.: Prefrontal cortical regulation of fear learning. Trends Neurosci. 37, 1–10 (2014)Google Scholar
  69. 69.
    Maier, S.F., Seligman, M.E.: Learned helplessness: theory and evidence. J. Exp. Psychol. Gen. 105, 3–46 (1976)CrossRefGoogle Scholar
  70. 70.
    Foa, E.B., Zinbarg, R., Rothbaum, B.O.: Uncontrollability and unpredictability in post-traumatic stress disorder: an animal model. Psychol. Bull. 112, 218–238 (1992)CrossRefGoogle Scholar
  71. 71.
    Chorpita, B.F., Barlow, D.H.: The development of anxiety: the role of control in the early environment. Psychol. Bull. 124, 3–21 (1998)CrossRefGoogle Scholar
  72. 72.
    McNally, G.P., Johansen, J.P., Blair, H.T.: Placing prediction into the fear circuit. Trends Neurosci. 34, 283–292 (2011)CrossRefGoogle Scholar
  73. 73.
    Kerr, D.L., McLaren, D.G., Mathy, R.M., Nitschke, J.B.: Controllability modulates the anticipatory response in the human ventromedial prefrontal cortex. Front. Psychol. 3, 1–11 (2012)CrossRefGoogle Scholar
  74. 74.
    Franklin, T.B., Saab, B.J., Mansuy, I.M.: Neural mechanisms of stress resilience and vulnerability. Neuron 75, 747–761 (2012)CrossRefGoogle Scholar
  75. 75.
    Russo, S.J., Murrough, J.W., Han, M.-H., Charney, D.S., Nestler, E.J.: Neurobiology of resilience. Nat. Neurosci. 15, 1475–1484 (2012)CrossRefGoogle Scholar
  76. 76.
    Maren, S.: Fear of the unexpected: hippocampus mediates novelty-induced return of extinguished fear in rats. Neurobiol. Learn. Mem. 108, 88–95 (2014)CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Nathaniel G. Harnett
    • 1
  • Kimberly H. Wood
    • 1
  • Muriah D. Wheelock
    • 1
  • Amy J. Knight
    • 2
  • David C. Knight
    • 1
    Email author
  1. 1.Department of PsychologyUniversity of Alabama at BirminghamBirminghamUSA
  2. 2.Department of Physical Medicine and RehabilitationUniversity of Alabama at BirminghamBirminghamUSA

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