Human attachment security is mediated by the amygdala: Evidence from combined fMRI and psychophysiological measures

Human Brain Mapping

Volumn 27, Issue 8, 2006, Pages 623-635

  Lemche, Erwin ^a,b   Giampietro, Vincent P ^a   Surguladze, Simon A ^a   Amaro, Edson J ^a,c   Andrew, Christopher M ^a   Williams, Steven C R ^a   Brammer, Michael J ^a   Lawrence, Natalia ^a   Maier, Markus A ^d   Russell, Tamara A ^a   Simmons, Andrew ^a   Ecker, Christine ^a   Joraschky, Peter ^b   Phillips, Mary L ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

Amygdala; fMRI; Human attachment; Insula; Middle temporal gyrus; Semantic conceptual priming; Skin conductance level; Ventral striatum; XBAM

Indexed keywords

ADULT; ARTICLE; BRAIN MAPPING; CORPUS STRIATUM; EMOTIONAL ATTACHMENT; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INSULA; MALE; NORMAL HUMAN; PRIORITY JOURNAL; PSYCHOPHYSIOLOGY; SEMANTICS; SKIN CONDUCTANCE;

ADULT; AFFECTIVE SYMPTOMS; AMYGDALA; ANXIETY, SEPARATION; AUTONOMIC NERVOUS SYSTEM; BASAL GANGLIA; BRAIN MAPPING; FEMALE; FUNCTIONAL LATERALITY; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MATERNAL DEPRIVATION; NEURAL PATHWAYS; PSYCHOPHYSICS; STRESS, PSYCHOLOGICAL; TEMPORAL LOBE;

EID: 33746860834     PISSN: 10659471     EISSN: None     Source Type: Journal    
DOI: 10.1002/hbm.20206     Document Type: Article

References (45)

1. Amaral DG, Capitanio JP, Lavenex P, Mason WA, Mauldin-Jourdain ML, Mendoza SP (2003): The amygdala: is it an essential component of the neural network for social cognition? Neuropsychologia 41:517-522.
2. Anders S, Lotze M, Erb M, Grodd W, Birbaumer N (2004): Brain activity underlying emotional valence and arousal: a response-related fMRI study. Hum Brain Mapp 23:200-209.
3. Bale TL, Davis AM, Auger AP, Dorsa DM, McCarthy MM (2001): CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior. J Neurosci 21:2546-2552.
4. Bartels A, Zeki S (2004): The neural correlates of maternal and romantic love. Neuroimage 21:1155-1166.
5. Baumann MD, Lavenex P, Mason WA, Capitanio JP, Amaral DG (2004): The development of mother-infant interactions after neonatal amygdala lesions in rhesus monkeys. J Neurosci 24:711-721.
6. Brammer MJ, Bullmore ET, Simmons A, Williams SCR, Grasby PM, Howard RJ, Woodruff PWR, Rabe-Hesketh S (1997): Generic brain activation mapping in functional magnetic resonance imaging: a nonparametric approach. Magn Reson Imaging 15:763-770.
7. Breakspear M, Brammer MJ, Bullmore ET, Das P, Williams LM (2004): Spatiotemporal wavelet resampling for functional neuroimaging data. Hum Brain Mapp 23:1-25.
8. Breakspear M, Brammer MJ, Robinson PA (2003): Construction of multivariate surrogate sets from nonlinear data using the wavelet transform. Physica D 182:1-22.
9. Bullmore ET, Brammer MJ, Rabe-Hesketh S, Curtis VA, Morris RG, Williams SCR, Sharma T, McGuire PK (1999): Methods for diagnosis and treatment of stimulus-correlated motion in generic brain activation studies using fMRI. Hum Brain Mapp 7:38-48.
10. Bullmore ET, Long C, Suckling J, Fadili MJ, Calvert G, Zelaya F, Carpenter TA, Brammer MJ (2001): Color noise and computational inference in neurophysiological (fMRI) time series analysis: resampling methods in time and wavelet domains. Hum Brain Mapp 12:61-78.
11. Calder AJ, Lawrence AD, Young AW (2001): Neuropsychology of fear and loathing. Nat Rev Neurosci 2:352-363.
12. Carter CS (1998): Neuroendocrine perspectives on social attachment and love. Psychoendocrinology 23:779-818.
13. Dehaene S, Naccache L, Le Clec HG, Koechlin E, Müller M, Dehaene-Lambertz G, van de Moortele PF, Le Bihan D (1998): Imaging unconscious semantic priming. Nature 395:597-600.
14. Fadili MJ, Bullmore ET (2002): Wavelet-generalized least squares: a new BLU estimator of linear regression models with 1/f errors. Neuroimage 15:217-232.
15. Ferguson JN, Aldag JM, Insel TR, Young LJ (2001): Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 21:8278-8285.
16. Henson RN (2001): Repetition effects for words and nonwords as indexed by event-related fMRI: a preliminary study. Scand J Psychol 42:179-198.
17. Horn G (1985): Memory, imprinting, and the brain: an inquiry into mechanisms. Oxford, UK: Clarendon Press. 312 pp.
18. Insel TR (1997): A neurobiological basis of social attachment. Am J Psychiatry 154:726-735.
19. Insel TR, Shapiro LE (1992): Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc Natl Acad Sci USA 89:5981-5985.
20. Insel TR, Young LJ (2001): The neurobiology of attachment. Nat Rev Neurosci 2:129-136.
21. Kensinger EA, Corkin S (2004): Two routes for emotional memory: distinct neural processes for valence and arousal. Proc Natl Acad Sci USA 101:3310-3315.
22. Kiehl KA, Liddle PF, Hopfinger JB (2000): Error processing and the rostral anterior cingulate: an event-related fMRI study. Psychophysiology 37:216-223.
23. Kraemer GW (1992): A psychobiological theory of attachment. Behav Brain Sci 15:493-541.
24. Kristoff K, Grabrieli JD (2000): The frontopolar cortex and human cognition: evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex. Psychobiology 28:168-186.
25. Leibenluft E, Gobbini MA, Harrison T, Haxby JV (2004): Mothers' neural activation in response to pictures of their children and other children. Biol Psychiatry 56:225-232.
26. Lemche E, Klann-Delius G, Koch R, Joraschky P (2004): Mentalizing language development in a longitudinal attachment sample: implications for alexithymia. Psychother Psychosom 73:366-374.
27. Loup F, Tribollet E, Dubois-Dauphin M, Dreifuss JJ (1991): Localization of high-affinity binding sites for oxytocin and vasopressin in the human brain. Brain Res 555:220-232.
28. Lovic V, Gonzalez A, Fleming AS (2001): Maternally separated rats show deficits in maternal care in adulthood. Dev Psychobiol 39:19-33.
29. Maier MA, Bernier A, Pekrun R, Zimmermann P, Grossmann KE (2004): Attachment working models as unconscious structures: an experimental test. Int J Behav Dev 28:180-189.
30. McCabe BJ, Nicol AU (1999): The recognition memory of imprinting: biochemistry and electrophysiology. Behav Brain Res 98:253-260.
31. Morris JS, Friston KJ, Büchel C, Frith CD, Young AW, Calder AJ, Dolan RJ (1998): A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain 121:47-57.
32. Oldfield RC (1971): The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 7:97-113.
33. Pagnoni G, Zink CF, Montague PR, Berns S (2002): Activity in human ventral striatum locked to errors of reward prediction. Nat Neurosci 5:97-98.
34. Phillips ML, Young AW, Senior C, Brammer MJ, Andrew CM, Calder AJ, Bullmore ET, Perret DI, Rowland D, Williams SCR, Gray JA, David AS (1997): A specific neural substrate for perceiving facial expressions of disgust. Nature 389:495-498.
35. Poeggel G, Helmeke C, Abraham A, Schwabe T, Friedrich P, Braun K (2003): Juvenile emotional experience alters synaptic composition in the rodent cortex, hippocampus, and lateral amygdala. Proc Natl Acad Sci USA 100:16137-16142.
36. Rossell SL, Bullmore ET, Williams SCR, David AS (2001): Brain activation during automatic and controlled processing of semantic relations: a priming experiment using lexical-decision. Neuropsychologia 39:1167-1176.
37. Spangler G, Grossmann KE (1993): Biobehavioral organization in securely and insecurely attached infants. Child Dev 62:1439-1450.
38. Spangler G, Schieche M (1998): Emotional and adrenocortical responses of infants to the Strange Situation: the differential function of emotional expression. Int J Behav Dev 22:681-706.
39. Spielberger CD (1983): Manual for the State-Trait Anxiety Inventory (STAI). Palo Alto, CA: Consulting Psychologists Press. 76 pp.
40. Surguladze SA, Brammer MJ, Young AW, Andrew C, Travis MJ, Williams SCR, Phillips ML (2003): A differential modulation of visual cortical activation by displays of danger, reward and distress. Neuroimage 19:1317-1328.
41. Talairach J, Tournoux P (1988): Co-planar stereotaxic atlas of the human brain. Stuttgart, Germany. Thieme Medical Publishers. 122 p.
42. Tomizawa K, Iga N, Lu YF, Moriwaki A, Matsushita M, Li S-T, Miyamoto O, Itano T, Matsui H (2003): Oxytocin improves long-lasting spatial memory during motherhood through MAP kinase cascade. Nat Neurosci 6:384-390.
43. Vandenberghe R, Nobre AC, Price CJ (2002): The response of left temporal cortex to sentences. J Cogn Neurosci 14:550-560.
44. Whalen PJ, Shin LM, Mclnerney SC, Fischer H, Wright CI, Rauch SL (2001): A functional MRI study of human amygdala responses to facial expressions of fear versus anger. Emotion 1:70-83.
45. World Medical Association (1999): Code of ethics: declaration of Helsinki. British Medical Journal 302:1194.