Amygdala and hippocampus fail to habituate to faces in individuals with an inhibited temperament

Social Cognitive and Affective Neuroscience

Volumn 8, Issue 2, 2013, Pages 143-150

  Blackford, Jennifer Urbano ^a,b   Allen, Amil H ^a   Cowan, Ronald L ^a,b   Avery, Suzanne N ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

Amygdala; Habituation; Hippocampus; Inhibited temperament; Neuroimaging; Social anxiety

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; CLASSIFICATION; COMPARATIVE STUDY; EQUIPMENT; FACE; FEMALE; HABITUATION; HIPPOCAMPUS; HUMAN; INHIBITION (PSYCHOLOGY); MALE; METHODOLOGY; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PERCEPTION; PHYSIOLOGY; TEMPERAMENT;

ADULT; AMYGDALA; FACE; FEMALE; HABITUATION, PSYCHOPHYSIOLOGIC; HIPPOCAMPUS; HUMANS; INHIBITION (PSYCHOLOGY); MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; SOCIAL PERCEPTION; TEMPERAMENT; YOUNG ADULT;

EID: 84876859195     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nsr078     Document Type: Article

References (46)

1. Beaton, E.A., Schmidt, L.A., Schulkin, J., Antony, M.M., Swinson, R.P., Hall, G.B. (2008). Different neural responses to stranger and personally familiar faces in shy and bold adults. Behavioral Neuroscience, 122, 704-9.
2. Birn, R.M., Cox, R.W., Bandettini, P.A. (2002). Detection versus estimation in event-related fMRI: Choosing the optimal stimulus timing. Neuroimage, 15, 252-64.
3. Blackford, J.U., Avery, S.N., Cowan, R.L., Shelton, R.C., Zald, D.H. (2011). Sustained amygdala response to both novel and newly familiar faces characterizes inhibited temperament. Social Cognitive and Affective Neuroscience, 6(5), 621-29.
4. Blackford, J.U., Avery, S.N., Shelton, R.C., Zald, D.H. (2009). Amygdala temporal dynamics: temperamental differences in the timing of amygdala response to familiar and novel faces. BMC Neuroscience, 10, 145.
5. Blackford, J.U., Buckholtz, J.W., Avery, S.N., Zald, D.H. (2010). A unique role for the amygdala in novelty detection. Neuroimage, 50, 1188-93.
6. Breiter, H.C., Etcoff, N.L., Whalen, P.J., et al. (1996). Response and habituation of the human amygdala during visual processing of facial expression. Neuron, 17, 875-887.
7. Brett, M., Anton, J.-L., Valabregue, R., Poline, J.B. (2002). Region of interest analysis using an SPM toolbox [abstract]. Neuroimage, 16, s497.
8. Britton, J., Shin, L., Barrett, L., Rauch, S., Wright, C. (2008). Amygdala and fusiform gyrus temporal dynamics: Responses to negative facial expressions. BMC Neuroscience, 9, 44.
9. Brozinsky, C.J., Yonelinas, A.P., Kroll, N.E.A., Ranganath, C. (2005). Lag-sensitive repetition suppression effects in the anterior parahippocampal gyrus. Hippocampus, 15, 557-61.
10. Bushnell, I.W.R. (1982). Discrimination of faces by young infants. Journal of Experimental Child Psychology, 33, 298-308.
11. Chronis-Tuscano, A., Degnan, K.A., Pine, D.S., et al. (2009). Stable early maternal report of behavioral inhibition predicts lifetime social anxiety disorder in adolescence. Journal of the American Academy of Child and Adolescent Psychiatry, 48, 928-35.
12. Clauss, J.A., Cowan, R.L., Blackford, J.U. (2011). Expectancy and temperament modulate amygdala and dorsal anterior cingulate responses to fear faces. Cognitive Affective & Behavioral Neuroscience, 11, 13-21.
13. Costafreda, S.G., Brammer, M.J., David, A.S., Fu, C.H.Y. (2008). Predictors of amygdala activation during the processing of emotional stimuli: a meta-analysis of 385 PET and fMRI studies. Brain Research Reviews, 58, 57-70.
14. Davidson, R.J., Irwin, W. (1999). The functional neuroanatomy of emotion and affective style. Trends in Cognitive Science, 3, 11-21.
15. Essex, M.J., Klein, M.H., Slattery, M.J., Goldsmith, H.H., Kalin, N.H. (2010). Early risk factors and developmental pathways to chronic high inhibition and social anxiety disorder in adolescence. American Journal of Psychiatry, 167, 40-6.
16. Fischer, H., Wright, C.I., Whalen, P.J., McInerney, S.C., Shin, L.M., Rauch, S.L. (2003). Brain habituation during repeated exposure to fearful and neutral faces: a functional MRI study. Brain Research Bulletin, 59, 387-92.
17. Fried, I., MacDonald, K.A., Wilson, C.L. (1997). Single neuron activity in human hippocampus and amygdala during recognition of faces and objects. Neuron, 18, 753-765.
18. Friston, K., Holmes, A., Worsley, K., Poline, J., Frith, C., Frackowiak, R. (1994). Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapping, 2, 189-210.
19. Friston, K., Worsley, K., Frackowiak, R., Mazziotta, J., Evans, A. (1993). Assessing the significance of focal activations using their spatial extent. Human Brain Mapping, 1, 210-20.
20. Gonsalves, B.D., Kahn, I., Curran, T., Norman, K.A., Wagner, A.D. (2005). Memory strength and repetition suppression: multimodal imaging of medial temporal cortical contributions to recognition. Neuron, 47, 751-61.
21. Gur, R.C., Ragland, J.D., Moberg, P.J., et al. (2001). Computerized neurocognitive scanning: I. Methodology and validation in healthy people. Neuropsychopharmacology, 25, 766-76.
22. Holt, D.J., Weiss, A.P., Rauch, S.L., et al. (2005). Sustained activation of the hippocampus in response to fearful faces in schizophrenia. Biological Psychiatry, 57, 1011-19.
23. Kagan, J., Reznick, J.S., Snidman, N. (1987). The physiology and psychology of behavioral inhibition in children. Child Development, 58, 1459-73.
24. Kleinhans, N.M., Johnson, L.C., Richards, T., et al. (2009). Reduced neural habituation in the amygdala and social impairments in autism spectrum disorders. American Journal of Psychiatry, 166, 467-75.
25. Lieberman, M., Inagaki, T., Tabibnia, G., Crockett, M. (2011). Subjective responses to emotional stimuli during labeling, reappraisal and distraction. Emotion, 11, 468-80.
26. Lundqvist, D., Flykt, A., Öhman, A. (1998). The Karolinska Directed Emotional Faces - KDEF. Department of Clinical Neuroscience, Psychology section, Karolinska Institute.
27. Maldjian, J.A., Laurienti, P.J., Burdette, J.B., Kraft, R.A. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage, 19, 1233-9.
28. Oler, J.A., Fox, A.S., Shelton, S.E., et al. (2010). Amygdalar and hippocampal substrates of anxious temperament differ in their heritability. Nature, 466, 864-8.
29. Perez-Edgar, K., Roberson-Nay, R., Hardin, M.G., et al. (2007). Attention alters neural responses to evocative faces in behaviorally inhibited adolescents. Neuroimage, 35, 1538-46.
30. Pessoa, L. (2008). On the relationship between emotion and cognition. Nature Reviews Neuroscience, 9, 148-58.
31. Phan, K.L., Liberzon, I., Welsh, R.C., Britton, J.C., Taylor, S.F. (2003). Habituation of rostral anterior cingulate cortex to repeated emotionally salient pictures. Neuropsychopharmacology, 28, 1344-50.
32. Poline, J.B., Mazoyer, B.M. (1993). Analysis of individual positron emission tomography activation maps by detection of high signal-to-noise-ratio pixel clusters. Journal of Cerebral Blood Flow and Metabolism, 13, 425-37.
33. Ranganath, C., Rainer, G. (2003). Neural mechanisms for detecting and remembering novel events. Nature Reviews Neuroscience, 4, 193-202.
34. Rankin, C.H., Abrams, T., Barry, R.J., et al. (2009). Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiology of Learning and Memory, 92, 135-8.
35. Reznick, J.S., Hegeman, I.M., Kaufman, E.R., Woods, S.W., Jacobs, M. (1992). Retrospective and concurrent self-report of behavioral-inhibition and their relation to adult mental-health. Development and Psychopathology, 4, 301-21.
36. Rutishauser, U., Mamelak, A.N., Schuman, E.M. (2006). Single-trial learning of novel stimuli by individual neurons of the human hippocampus-amygdala complex. Neuron, 49, 805-13.
37. Schwartz, C.E., Snidman, N., Kagan, J. (1999). Adolescent social anxiety as an outcome of inhibited temperament in childhood. Journal of the American Academy of Child and Adolescent Psychiatry, 38, 1008-15.
38. Schwartz, C.E., Wright, C.I., Shin, L.M., Kagan, J., Rauch, S.L. (2003a). Inhibited and uninhibited infants "grown up": adult amygdalar response to novelty. Science, 300, 1952-3.
39. Schwartz, C.E., Wright, C.I., Shin, L.M., et al. (2003b). Differential amygdalar response to novel versus newly familiar neutral faces: a functional MRI probe developed for studying inhibited temperament. Biological Psychiatry, 53, 854-62.
40. Strange, B.A., Fletcher, P.C., Henson, R.N.A., Friston, K.J., Dolan, R.J. (1999). Segregating the functions of human hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 96, 4034-9.
41. Taylor, S.F., Phan, K.L., Decker, L.R., Liberzon, I. (2003). Subjective rating of emotionally salient stimuli modulates neural activity. Neuroimage, 18, 650-9.
42. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage, 15, 273-89.
43. Ugurbil, K., Hu, X.P., Chen, W., Zhu, X.H., Kim, S.G., Georgopoulos, A. (1999). Functional mapping in the human brain using high magnetic fields. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 354, 1195-213.
44. Wright, C.I., Fischer, H., Whalen, P.J., McInerney, S., Shin, L.M., Rauch, S.L. (2001). Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli. Neuroreport, 12, 379-83.
45. Wright, C.I., Martis, B., Schwartz, C.E., et al. (2003). Novelty responses and differential effects of order in the amygdala, substantia innominata, and inferior temporal cortex. Neuroimage, 18, 660-9.
46. Yamaguchi, S., Hale, L.A., D'Esposito, M., Knight, R.T. (2004). Rapid prefrontal-hippocampal habituation to novel events. Journal of Neuroscience, 24, 5356-63.