Neural substrates of classically conditioned fear-generalization in humans: A parametric fMRI study

Social Cognitive and Affective Neuroscience

Volumn 9, Issue 8, 2014, Pages 1134-1142

  Lissek, Shmuel ^a,b   Bradford, Daniel E ^c   Alvarez, Ruben P ^d   Burton, Philip ^b   Espensen Sturges, Tori ^b   Reynolds, Richard C ^a   Grillon, Christian ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d LAUREATE INSTITUTE FOR BRAIN RESEARCH   (United States)

Author keywords

Anxiety; Conditioned generalization; Fear conditioning; fMRI; Neurobiology

Indexed keywords

BRAIN; BRAIN MAPPING; CONDITIONED REFLEX; ELECTRIC SHOCK; FEAR; FEMALE; HUMAN; LEARNING; MALE; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PHYSIOLOGY; YOUNG ADULT;

BRAIN; BRAIN MAPPING; CONDITIONING, CLASSICAL; ELECTROSHOCK; FEAR; FEMALE; GENERALIZATION (PSYCHOLOGY); HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; PHOTIC STIMULATION; YOUNG ADULT;

EID: 84905921226     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nst096     Document Type: Article

References (45)

1. Alvarez, R.P., Biggs, A., Chen, G., Pine, D.S., Grillon, C. (2008). Contextual fear conditioning in humans: cortical-hippocampal and amygdala contributions. Journal of Neuroscience, 28, 6211-9.
2. Antunes, R., Moita, M.A. (2010). Discriminative auditory fear learning requires both tuned and nontuned auditory pathways to the amygdala. Journal of Neuroscience, 30, 9782-7.
3. Armony, J.L., Servan-Schreiber, D., Romanski, L.M., Cohen, J.D., LeDoux, J.E. (1997). Stimulus generalization of fear responses: effects of auditory cortex lesions in a computational model and in rats. Cerebral Cortex, 7, 157-65.
4. Bucci, D.J., Saddoris, M.P., Burwell, R.D. (2002). Contextual fear discrimination is impaired by damage to the postrhinal or perirhinal cortex. Behavioral Neuroscience, 116, 479-88.
5. Büchel, C., Morris, J., Dolan, R.J., Friston, K.J. (1998). Brain systems mediating aversive conditioning: an event-related fMRI study. Neuron, 20, 947-57.
6. Cox, R.W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162-73.
7. Dunsmoor, J.E., LaBar, K.S. (2012). Brain activity associated with omission of an aversive event reveals the effects of fear learning and generalization. Neurobiology of Learning and Memory, 97, 301-12.
8. Dunsmoor, J.E., Prince, S.E., Murty, V.P., Kragel, P.A., LaBar, K.S. (2011). Neurobehavioral mechanisms of human fear generalization. NeuroImage, 55, 1878-88.
9. Etkin, A., Egner, T., Kalisch, R. (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences, 15, 85-93.
10. First, M.B., Gibbon, M., Spitzer, R.L., Williams, J.B.W. (2001). Structured Clinical Interview for DSM-IV Axis I Disorders (SCID-I) Research version. New York: New York State Psychiatric Institute.
11. Friston, K.J., Büchel, C., Fink, G.R., Morris, J., Rolls, E., Dolan, R.J. (1997). Psychophysiological and modulatory interactions in neuroimaging. Neuroimage, 6, 218-29.
12. Greenberg, T., Carlson, J.M., Cha, J., Hajcak, G., Mujica-Parodi, L.R. (2013a). Ventromedial prefrontal cortex reactivity is altered in generalized anxiety disorder during fear generalization. Depression and Anxiety, 30, 242-50.
13. Greenberg, T., Carlson, J.M., Cha, J., Hajcak, G., Mujica-Parodi, L.R. (2013b). Neural reactivity tracks fear generalization gradients. Biological Psychology, 92, 2-8.
14. Honig, W.K., Urcuioli, P.J. (1981). The legacy of Guttman and Kalish (1956): twenty-Eve years of research on stimulus generalization. Journal of the Experimental Analysis of Behavior, 36, 405-45.
15. Jarrell, T., Gentile, C., Romanski, L., McCabe, P., Schneiderman, N. (1987). Involvement of cortical and thalamic auditory regions in retention of differential bradycardiac conditioning to acoustic conditioned stimuli in rabbits. Brain Research, 412, 285-94.
16. Kalish, H.I. (1969). Stimulus generalization. In: Marx, M.H., editor. Learning: Processes. Oxford, England: Macmillan.
17. Klumpp, H., Angstadt, M., Phan, K.L. (2012). Insula reactivity and connectivity to anterior cingulate cortex when processing threat in generalized social anxiety disorder. Biological Psychology, 89, 273-6.
18. Knight, D.C., Cheng, D.T., Smith, C.N., Stein, E.A., Helmstetter, F.J. (2004). Neural substrates mediating human delay and trace fear conditioning. Journal of Neuroscience, 24, 218-28.
19. Lissek, S. (2012). Toward an account of clinical anxiety predicated on basic, neurally mapped mechanisms of Pavlovian fear-learning: the case for conditioned overgeneralization. Depression and Anxiety, 29, 257-63.
20. Lissek, S., Biggs, A.L., Rabin, S., et al. (2008). Generalization of conditioned fear-potentiated startle in humans: experimental validation and clinical relevance. Behaviour Research and Therapy, 46, 678-87.
21. Lissek, S., Grillon, C. (2012). Learning models of PTSD. In: Beck, J.G., Sloan, D.M., editors. The Oxford Handbook of Traumatic Stress Disorders. New York, NY: Oxford University Press.
22. Lissek, S., Powers, A.S., McClure, E.B., et al. (2005). Classical fear-conditioning in the anxiety disorders: a meta-analysis. Behaviour Research and Therapy, 43, 1391-424.
23. Lissek, S., Rabin, S.J., Heller, R.E., et al. (2010). Overgeneralization of conditioned fear as a pathogenic marker of panic disorder. American Journal of Psychiatry, 167, 47-55.
24. Mackintosh, N.J. (1974). The Psychology of Animal Learning. New York, NY: Academic Press.
25. McHugh, T.J., Jones, M.W., Quinn, J.J., et al. (2007). Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science, 317, 94-9.
26. Milad, M.R., Wright, C.I., Orr, S.P., Pitman, R.K., Quirk, G.J., Rauch, S.L. (2007). Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biological Psychiatry, 62, 446-54.
27. Mineka, S., Zinbarg, R. (1996). Conditioning and ethological models of anxiety disorders: stress-in-dynamic-context anxiety models. In: Hope, D.A., editor. Perspective on Anxiety, Panic,&Fear, Vol. 43, Lincoln and London: University of Nebraska Press, pp. 135-210.
28. Murray, S.O., Boyaci, H., Kersten, D. (2006). The representation of perceived angular size in human primary visual cortex. Nature Neuroscience, 9, 429-34.
29. Nakazawa, K., McHugh, T.J., Wilson, M.A., Tonegawa, S. (2004). NMDA receptors, place cells and hippocampal spatial memory. Nature Reviews Neuroscience, 5, 361-72.
30. Nitschke, J.B., Sarinopoulos, I., Mackiewica, K.L., Schaefer, H.S., Davidson, R.J. (2006). Functional neuroanatomy of aversion and its anticipation. Neuroimage, 29, 106-16.
31. O'Reilly, R.C., Rudy, J.W. (2001). Conjunctive representations in learning and memory: principles of cortical and hippocampal function. Psychological Review, 108, 311-45.
32. Otto, T., Eichenbaum, H. (1992). Neuronal activity in the hippocampus during delayed non-match to sample performance in rats: evidence for hippocampal processing in recognition memory. Hippocampus, 2, 323-34.
33. Passamonti, L., Rowe, J.B., Schwarzbauer, C., Ewbank, M.P., von dem Hagen, E., Calder, A.J. (2009). Personality predicts the brain's response to viewing appetizing foods: the neural basis of a risk factor for overeating. Journal of Neurosciences, 29, 43-51.
34. Phelps, E.A., Delgado, M.R., Nearing, K.I., Ledoux, J.E. (2004). Extinction learning in humans: role of the amygdala and vmPFC. Neuron, 43, 897-905.
35. Radua, J., Phillips, M.L., Russell, T., et al. (2010). Neural response to specific components of fearful faces in healthy and schizophrenic adults. Neuroimage, 49, 939-46.
36. Sander, D., Grandjean, D., Scherer, K.R. (2005). A systems approach to appraisal mechanisms in emotion. Neural Networks, 18, 317-52.
37. Schiller, D., Levy, I., Niv, Y., LeDoux, J.E., Phelps, E.A. (2008). From fear to safety and back: reversal of fear in the human brain. Journal of Neurosciences, 28, 11517-25.
38. Schwartz, S., Vuilleumier, P., Hutton, C., Maravita, A., Dolan, R.J., Driver, J. (2005). Attentional load and sensory competition in human vision: modulation of fMRI responses by load at fixation during task-irrelevant stimulation in the peripheral visual field. Cerebral Cortex, 15, 770-86.
39. Sehlmeyer, C., Schöning, S., Zwitserlood, P., et al. (2009). Human fear conditioning and extinction in neuroimaging: a systematic review. PLoS One, 4, e5865.
40. Solomon, P.R., Moore, J.W. (1975). Latent inhibition and stimulus generalization of the classically conditioned nictitating membrane response in rabbits (Orcytolagus cuniculus) following dorsal hippocampal ablation. Journal of Comparative and Physiological Psychology, 89, 1192-203.
41. Spielberger, C.D., Gorsuch, R.L., Lushene, R., Vagg, P., Jacobs, G.A. (1983). Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologist Press.
42. Teich, A.H., McCabe, P.M., Gentile, C.G., et al. (1988). Role of auditory cortex in the acquisition of differential heart rate conditioning. Physiology and Behavior, 44, 405-12.
43. Treves, A., Rolls, E. (1994). Computational analysis of the role of the hippocampus in memory. Hippocampus, 4, 374-91.
44. Wild, J.M., Blampied, N.M. (1972). Hippocampal lesions and stimulus generalization in rats. Physiology of Behavior, 9, 505-11.
45. Zelinski, E.L., Hong, N.S., Tyndall, A.V., Halsall, B., McDonald, R.J. (2010). Prefrontal cortical contributions during discriminative fear conditioning, extinction, and spontaneous recovery in rats. Experimental Brain Research, 203, 285-97.