Intrinsic functional connectivity of the central nucleus of the amygdala and bed nucleus of the stria terminalis

Adam X Gorka, Salvatore Torrisi, Alexander J Shackman, Christian Grillon, Monique Ernst, Adam X Gorka, Salvatore Torrisi, Alexander J Shackman, Christian Grillon, Monique Ernst

Abstract

The central nucleus of the amygdala (CeA) and bed nucleus of the stria terminalis (BNST), two nuclei within the central extended amygdala, function as critical relays within the distributed neural networks that coordinate sensory, emotional, and cognitive responses to threat. These structures have overlapping anatomical projections to downstream targets that initiate defensive responses. Despite these commonalities, researchers have also proposed a functional dissociation between the CeA and BNST, with the CeA promoting responses to discrete stimuli and the BNST promoting responses to diffuse threat. Intrinsic functional connectivity (iFC) provides a means to investigate the functional architecture of the brain, unbiased by task demands. Using ultra-high field neuroimaging (7-Tesla fMRI), which provides increased spatial resolution, this study compared the iFC networks of the CeA and BNST in 27 healthy individuals. Both structures were coupled with areas of the medial prefrontal cortex, hippocampus, thalamus, and periaqueductal gray matter. Compared to the BNST, the bilateral CeA was more strongly coupled with the insula and regions that support sensory processing, including thalamus and fusiform gyrus. In contrast, the bilateral BNST was more strongly coupled with regions involved in cognitive and motivational processes, including the dorsal paracingulate gyrus, posterior cingulate cortex, and striatum. Collectively, these findings suggest that responses to sensory stimulation are preferentially coordinated by the CeA and cognitive and motivational responses are preferentially coordinated by the BNST.

Trial registration: ClinicalTrials.gov NCT00047853.

Keywords: 7-Tesla fMRI; Bed nucleus of the stria terminalis BNST; Central nucleus of the amygdala; Intrinsic functional connectivity; Resting state networks.

Published by Elsevier Inc.

Figures

Figure 1
Figure 1
Seed ROIs for intrinsic connectivity analyses. A): central nucleus of the amygdala (CeA); B): bed nucleus of the stria terminalis (BNST).
Figure 2
Figure 2
Shared coupling. Regions showing significant iFC with both the CeA and BNST are depicted in red (p<.05 whole-brain corrected a thalamus and hippocampus. b amygdala including regions of the lateral basal nuclei. c striatum caudate putamen ventral striatum. d midbrain pag. e mpfc. f superior temporal sulcus.>

Figure 3

Distinct connections. Regions with greater…

Figure 3

Distinct connections. Regions with greater CeA iFC are depicted in red-yellow, whereas regions…

Figure 3
Distinct connections. Regions with greater CeA iFC are depicted in red-yellow, whereas regions with greater BNST iFC are depicted in blue (p<.05 whole-brain corrected cea-preferring regions include the middle insula ventral posterior thalamus postcentral and supramarginal gyri fusiform gyrus. bnst-preferring paracingulate gyrus cingulate head body of caudate nucleus bilaterally extending into striatum.>

Figure 4

Seed ROI x Hemisphere Effects…

Figure 4

Seed ROI x Hemisphere Effects within Ventromedial Prefrontal Cortex. (A) Statistical image depicting…

Figure 4
Seed ROI x Hemisphere Effects within Ventromedial Prefrontal Cortex. (A) Statistical image depicting results within the ventromedial prefrontal cortex (vmPFC) that exhibit a significant interaction between seed ROI (CeA vs. BNST) and hemisphere (left vs. right). (B) Bar graphs depicting mean iFC values from the vmPFC as a function of ROI and hemisphere. iFC values are reported in arbitrary units (A.U.). Error bars reflect 1 standard error.
Similar articles
Cited by
References
    1. AAhs F, Kragel PA, Zielinski DJ, Brady R, LaBar KS. Medial prefrontal pathways for the contextual regulation of extinguished fear in humans. NeuroImage. 2015;122:262–271. - PMC - PubMed
    1. Aggleton JP, Mishkin M. Projections of the amygdala to the thalamus in the cynomolgus monkey. The Journal of Comparative Neurology. 1984;222(1):56–68. https://doi.org/10.1002/cne.902220106. - DOI - PubMed
    1. Alitto HJ, Usrey WM. Corticothalamic feedback and sensory processing. Current Opinion in Neurobiology. 2003;13(4):440–445. https://doi.org/10.1016/S0959-4388(03)00096-5. - DOI - PubMed
    1. Andersen SL, Teicher MH. Serotonin laterality in amygdala predicts performance in the elevated plus maze in rats. Neuroreport. 1999;10(17):3497–3500. - PubMed
    1. Antoniadis EA, McDonald RJ. Fornix, medial prefrontal cortex, nucleus accumbens, and mediodorsal thalamic nucleus: Roles in a fear-based context discrimination task. Neurobiology of Learning and Memory. 2006;85(1):71–85. https://doi.org/10.1016/j.nlm.2005.08.011. - DOI - PubMed
Show all 89 references
Publication types
MeSH terms
Associated data
Related information
[x]
Cite
Copy Download .nbib .nbib
Format: AMA APA MLA NLM
Figure 3
Figure 3
Distinct connections. Regions with greater CeA iFC are depicted in red-yellow, whereas regions with greater BNST iFC are depicted in blue (p<.05 whole-brain corrected cea-preferring regions include the middle insula ventral posterior thalamus postcentral and supramarginal gyri fusiform gyrus. bnst-preferring paracingulate gyrus cingulate head body of caudate nucleus bilaterally extending into striatum.>

Figure 4

Seed ROI x Hemisphere Effects…

Figure 4

Seed ROI x Hemisphere Effects within Ventromedial Prefrontal Cortex. (A) Statistical image depicting…

Figure 4
Seed ROI x Hemisphere Effects within Ventromedial Prefrontal Cortex. (A) Statistical image depicting results within the ventromedial prefrontal cortex (vmPFC) that exhibit a significant interaction between seed ROI (CeA vs. BNST) and hemisphere (left vs. right). (B) Bar graphs depicting mean iFC values from the vmPFC as a function of ROI and hemisphere. iFC values are reported in arbitrary units (A.U.). Error bars reflect 1 standard error.
Figure 4
Figure 4
Seed ROI x Hemisphere Effects within Ventromedial Prefrontal Cortex. (A) Statistical image depicting results within the ventromedial prefrontal cortex (vmPFC) that exhibit a significant interaction between seed ROI (CeA vs. BNST) and hemisphere (left vs. right). (B) Bar graphs depicting mean iFC values from the vmPFC as a function of ROI and hemisphere. iFC values are reported in arbitrary units (A.U.). Error bars reflect 1 standard error.

References

    1. AAhs F, Kragel PA, Zielinski DJ, Brady R, LaBar KS. Medial prefrontal pathways for the contextual regulation of extinguished fear in humans. NeuroImage. 2015;122:262–271.
    1. Aggleton JP, Mishkin M. Projections of the amygdala to the thalamus in the cynomolgus monkey. The Journal of Comparative Neurology. 1984;222(1):56–68. .
    1. Alitto HJ, Usrey WM. Corticothalamic feedback and sensory processing. Current Opinion in Neurobiology. 2003;13(4):440–445. .
    1. Andersen SL, Teicher MH. Serotonin laterality in amygdala predicts performance in the elevated plus maze in rats. Neuroreport. 1999;10(17):3497–3500.
    1. Antoniadis EA, McDonald RJ. Fornix, medial prefrontal cortex, nucleus accumbens, and mediodorsal thalamic nucleus: Roles in a fear-based context discrimination task. Neurobiology of Learning and Memory. 2006;85(1):71–85. .
    1. Avery SN, Clauss JA, Blackford JU. The Human BNST: Functional Role in Anxiety and Addiction. Neuropsychopharmacology. 2016;41(1):126–141. .
    1. Avery Suzanne N, Clauss JA, Winder DG, Woodward N, Heckers S, Blackford JU. BNST neurocircuitry in humans. NeuroImage. 2014;91:311–323. .
    1. Baas D, Aleman A, Kahn RS. Lateralization of amygdala activation: a systematic review of functional neuroimaging studies. Brain Research Reviews. 2004;45(2):96–103. .
    1. Bandler R, Keay KA, Floyd N, Price J. Central circuits mediating patterned autonomic activity during active vs. passive emotional coping. Brain Research Bulletin. 2000;53(1):95–104.
    1. Berman MG, Peltier S, Nee DE, Kross E, Deldin PJ, Jonides J. Depression, rumination and the default network. Social Cognitive and Affective Neuroscience. 2010;nsq080 .
    1. Berridge KC, Robinson TE, Aldridge JW. Dissecting components of reward: “liking”, “wanting”, and learning. Current Opinion in Pharmacology. 2009;9(1):65–73. .
    1. Bienkowski MS, Rinaman L. Common and distinct neural inputs to the medial central nucleus of the amygdala and anterior ventrolateral bed nucleus of stria terminalis in rats. Brain Structure and Function. 2012;218(1):187–208. .
    1. Bijsterbosch J, Smith S, Bishop SJ. Functional connectivity under anticipation of shock: Correlates of trait anxious affect versus induced anxiety. Journal of Cognitive Neuroscience. 2015 Retrieved from .
    1. Birn RM, Shackman AJ, Oler JA, Williams LE, McFarlin DR, Rogers GM, et al. Kalin NH. Evolutionarily conserved prefrontal-amygdalar dysfunction in early-life anxiety. Molecular Psychiatry. 2014;19(8):915–922. .
    1. Birn Rasmus M, Smith MA, Jones TB, Bandettini PA. The respiration response function: the temporal dynamics of fMRI signal fluctuations related to changes in respiration. Neuroimage. 2008;40(2):644–654.
    1. Blair HT, Schafe GE, Bauer EP, Rodrigues SM, LeDoux JE. Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learning & Memory. 2001;8(5):229–242.
    1. Bradbury AJ, Costall B, Domeney AM, Naylor RJ. Laterality of dopamine function and neuroleptic action in the amygdala in the rat. Neuropharmacology. 1985;24(12):1163–1170. .
    1. Casey KL, Morrow TJ. Ventral posterior thalamic neurons differentially responsive to noxious stimulation of the awake monkey. Science. 1983;221(4611):675–677.
    1. Cohen AL, Fair DA, Dosenbach NUF, Miezin FM, Dierker D, Van Essen DC, et al. Petersen SE. Defining functional areas in individual human brains using resting functional connectivity MRI. NeuroImage. 2008;41(1):45–57. .
    1. Cooney RE, Joormann J, Eugène F, Dennis EL, Gotlib IH. Neural correlates of rumination in depression. Cognitive, Affective, & Behavioral Neuroscience. 2010;10(4):470–478. .
    1. Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research. 1996;29(3):162–173.
    1. Cox RW, Reynolds RC, Taylor PA. AFNI and Clustering: False Positive Rates Redux. bioRxiv. 2016;065862
    1. Craig AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nature Reviews Neuroscience. 2002;3(8):655–666. .
    1. Cullinan WE, Herman JP, Watson SJ. Ventral subicular interaction with the hypothalamic paraventricular nucleus: Evidence for a relay in the bed nucleus of the stria terminalis. The Journal of Comparative Neurology. 1993;332(1):1–20. .
    1. Davis M, Shi C. The extended amygdala: are the central nucleus of the amygdala and the bed nucleus of the stria terminalis differentially involved in fear versus anxiety? Annals of the New York Academy of Sciences. 1999;877(1):281–291.
    1. Davis M, Walker DL, Miles L, Grillon C. Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology. 2010;35(1):105–135.
    1. Deco G, Jirsa VK, McIntosh AR. Emerging concepts for the dynamical organization of resting-state activity in the brain. Nature Reviews Neuroscience. 2011;12(1):43–56. .
    1. Deen B, Pitskel NB, Pelphrey KA. Three Systems of Insular Functional Connectivity Identified with Cluster Analysis. Cerebral Cortex. 2011;21(7):1498–1506. .
    1. Dong HW, Swanson LW. Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis. Journal of Comparative Neurology. 2004;468(2):277–298.
    1. Dziobek I, Bahnemann M, Convit A, Heekeren HR. THe role of the fusiform-amygdala system in the pathophysiology of autism. Archives of General Psychiatry. 2010;67(4):397–405. .
    1. Eklund A, Nichols TE, Knutsson H. Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences. 2016;113(28):7900–7905. .
    1. First MB, Spitzer RL, Gibbon M, Williams JB. Structured clinical interview for DSM-IV-TR axis I disorders—non-patient edition. New York State Psychiatric Institute, New York 2001
    1. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 2002;33(3):341–355.
    1. Fonov V, Evans AC, Botteron K, Almli CR, McKinstry RC, Collins DL, et al. Unbiased average age-appropriate atlases for pediatric studies. NeuroImage. 2011;54(1):313–327.
    1. Fonov VS, Evans AC, McKinstry RC, Almli CR, Collins DL. Unbiased nonlinear average age-appropriate brain templates from birth to adulthood. NeuroImage. 2009;47:S102.
    1. Fox AS, Shelton SE, Oakes TR, Converse AK, Davidson RJ, Kalin NH. Orbitofrontal cortex lesions alter anxiety-related activity in the primate bed nucleus of stria terminalis. The Journal of Neuroscience. 2010;30(20):7023–7027.
    1. Fox MD, Raichle ME. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Reviews Neuroscience. 2007;8(9):700–711.
    1. Fullana MA, Harrison BJ, Soriano-Mas C, Vervliet B, Cardoner N, Àvila-Parcet A, Radua J. Neural signatures of human fear conditioning: an updated and extended meta-analysis of fMRI studies. Molecular Psychiatry. 2016;21(4):500–508. .
    1. Glover GH, Li TQ, Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magnetic Resonance in Medicine. 2000;44(1):162–167.
    1. Grosso A, Cambiaghi M, Concina G, Sacco T, Sacchetti B. Auditory cortex involvement in emotional learning and memory. Neuroscience. 2015;299:45–55.
    1. Hahn A, Stein P, Windischberger C, Weissenbacher A, Spindelegger C, Moser E, et al. Lanzenberger R. Reduced resting-state functional connectivity between amygdala and orbitofrontal cortex in social anxiety disorder. Neuroimage. 2011;56(3):881–889.
    1. Hurley KM, Herbert H, Moga MM, Saper CB. Efferent projections of the infralimbic cortex of the rat. The Journal of Comparative Neurology. 1991;308(2):249–276. .
    1. Hutton C, Josephs O, Stadler J, Featherstone E, Reid A, Speck O, et al. Weiskopf N. The impact of physiological noise correction on fMRI at 7T. Neuroimage. 2011;57(1):101–112.
    1. Jaisinghani S, Rosenkranz JA. Repeated social defeat stress enhances the anxiogenic effect of bright light on operant reward-seeking behavior in rats. Behavioural Brain Research. 2015;290:172–179. .
    1. Ji G, Neugebauer V. Hemispheric Lateralization of Pain Processing by Amygdala Neurons. Journal of Neurophysiology. 2009;102(4):2253–2264. .
    1. Jo HJ, Saad ZS, Simmons WK, Milbury LA, Cox RW. Mapping sources of correlation in resting state FMRI, with artifact detection and removal. Neuroimage. 2010;52(2):571–582.
    1. Kilpatrick LA, Zald DH, Pardo JV, Cahill LF. Sex-related differences in amygdala functional connectivity during resting conditions. NeuroImage. 2006;30(2):452–461. .
    1. Kim MJ, Gee DG, Loucks RA, Davis FC, Whalen PJ. Anxiety dissociates dorsal and ventral medial prefrontal cortex functional connectivity with the amygdala at rest. Cerebral Cortex (New York, N.Y.: 1991) 2011;21(7):1667–1673. .
    1. Koob GF, Volkow ND. Neurocircuitry of Addiction. Neuropsychopharmacology. 2010;35(1):217–238. .
    1. Krüger O, Shiozawa T, Kreifelts B, Scheffler K, Ethofer T. Three distinct fiber pathways of the bed nucleus of the stria terminalis to the amygdala and prefrontal cortex. Cortex. 2015;66:60–68.
    1. LeDoux JE, Iwata J, Cicchetti P, Reis DJ. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. The Journal of Neuroscience. 1988;8(7):2517–2529.
    1. Leech R, Sharp DJ. The role of the posterior cingulate cortex in cognition and disease. Brain. 2014;137(1):12–32. .
    1. Liljeholm M, O'Doherty JP. Contributions of the striatum to learning, motivation, and performance: an associative account. Trends in Cognitive Sciences. 2012;16(9):467–475. .
    1. Makovac E, Meeten F, Watson DR, Herman A, Garfinkel SN, Critchley HD, Ottaviani C. Alterations in Amygdala-Prefrontal Functional Connectivity Account for Excessive Worry and Autonomic Dysregulation in Generalized Anxiety Disorder. Biological Psychiatry. 2016;80(10):786–795. .
    1. Maren S, Phan KL, Liberzon I. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nature Reviews Neuroscience. 2013;14(6):417–428. .
    1. Mechias ML, Etkin A, Kalisch R. A meta-analysis of instructed fear studies: implications for conscious appraisal of threat. NeuroImage. 2010;49(2):1760–1768. .
    1. Milad MR, Wright CI, Orr SP, Pitman RK, Quirk GJ, Rauch SL. Recall of Fear Extinction in Humans Activates the Ventromedial Prefrontal Cortex and Hippocampus in Concert. Biological Psychiatry. 2007;62(5):446–454. .
    1. Motzkin JC, Philippi CL, Oler JA, Kalin NH, Baskaya MK, Koenigs M. Ventromedial prefrontal cortex damage alters resting blood flow to the bed nucleus of stria terminalis. Cortex. 2015;64:281–288. .
    1. Nichols T, Brett M, Andersson J, Wager T, Poline JB. Valid conjunction inference with the minimum statistic. NeuroImage. 2005;25(3):653–660. .
    1. Northoff G, Heinzel A, de Greck M, Bermpohl F, Dobrowolny H, Panksepp J. Self-referential processing in our brain—A meta-analysis of imaging studies on the self. NeuroImage. 2006;31(1):440–457. .
    1. Okon-Singer H, Hendler T, Pessoa L, Shackman AJ. The neurobiology of emotion–cognition interactions: fundamental questions and strategies for future research. Frontiers in Human Neuroscience. 2015;9:58. .
    1. Oler JA, Birn RM, Patriat R, Fox AS, Shelton SE, Burghy CA, et al. Kalin NH. Evidence for coordinated functional activity within the extended amygdala of non-human and human primates. NeuroImage. 2012;61(4):1059–1066. .
    1. Oler JA, Tromp DPM, Fox AS, Kovner R, Davidson RJ, Alexander AL, et al. Fudge JL. Connectivity between the central nucleus of the amygdala and the bed nucleus of the stria terminalis in the non-human primate: neuronal tract tracing and developmental neuroimaging studies. Brain Structure and Function. 2016:1–19. .
    1. Olmos JS, Heimer L. The concepts of the ventral striatopallidal system and extended amygdala. Annals of the New York Academy of Sciences. 1999;877(1):1–32.
    1. Paré D, Quirk GJ, Ledoux JE. New vistas on amygdala networks in conditioned fear. Journal of Neurophysiology. 2004;92(1):1–9.
    1. Paulesu E, Sambugaro E, Torti T, Danelli L, Ferri F, Scialfa G, et al. Sassaroli S. Neural correlates of worry in generalized anxiety disorder and in normal controls: a functional MRI study. Psychological Medicine. 2010;40(01):117–124.
    1. Phelps EA, Delgado MR, Nearing KI, LeDoux JE. Extinction learning in humans: role of the amygdala and vmPFC. Neuron. 2004;43(6):897–905. .
    1. Raichle ME. A Paradigm Shift in Functional Brain Imaging. The Journal of Neuroscience. 2009;29(41):12729–12734. .
    1. Roberts WW. Fearlike behavior elicited from dorsomedial thalamus of cat. Journal of Comparative and Physiological Psychology. 1962;55(2):191–197. .
    1. Roy AK, Shehzad Z, Margulies DS, Kelly AMC, Uddin LQ, Gotimer K, et al. Milham MP. Functional connectivity of the human amygdala using resting state fMRI. NeuroImage. 2009;45(2):614–626. .
    1. Sarter M, Markowitsch HJ. Involvement of the amygdala in learning and memory: A critical review, with emphasis on anatomical relations. Behavioral Neuroscience. 1985;99(2):342–380. .
    1. Shackman AJ, Fox AS. Contributions of the Central Extended Amygdala to Fear and Anxiety. The Journal of Neuroscience. 2016;36(31):8050–8063. .
    1. Shackman AJ, Salomons TV, Slagter HA, Fox AS, Winter JJ, Davidson RJ. The integration of negative affect, pain and cognitive control in the cingulate cortex. Nature Reviews Neuroscience. 2011;12(3):154–167.
    1. Shen X, Papademetris X, Constable RT. Graph-theory based parcellation of functional subunits in the brain from resting-state fMRI data. NeuroImage. 2010;50(3):1027–1035. .
    1. Shergill SS, White TP, Joyce DW, Bays PM, Wolpert DM, Frith CD. Modulation of somatosensory processing by action. NeuroImage. 2013;70:356–362. .
    1. Shi CJ, Cassell Md. Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. The Journal of Comparative Neurology. 1998;399(4):440–468. .
    1. Shin LM, Liberzon I. The Neurocircuitry of Fear, Stress, and Anxiety Disorders. Neuropsychopharmacology. 2009;35(1):169–191. .
    1. Simon O, Mangin JF, Cohen L, Le Bihan D, Dehaene S. Topographical Layout of Hand, Eye, Calculation, and Language-Related Areas in the Human Parietal Lobe. Neuron. 2002;33(3):475–487. .
    1. Spreng RN, Mar RA, Kim ASN. The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis. Journal of Cognitive Neuroscience. 2008;21(3):489–510. .
    1. Stamatakis AM, Sparta DR, Jennings JH, McElligott ZA, Decot H, Stuber GD. Amygdala and bed nucleus of the stria terminalis circuitry: implications for addiction-related behaviors. Neuropharmacology. 2014;76:320–328.
    1. Strange BA, Witter MP, Lein ES, Moser EI. Functional organization of the hippocampal longitudinal axis. Nature Reviews Neuroscience. 2014;15(10):655–669. .
    1. Sullivan GM, Apergis J, Bush DEA, Johnson LR, Hou M, Ledoux JE. Lesions in the bed nucleus of the stria terminalis disrupt corticosterone and freezing responses elicited by a contextual but not by a specific cue-conditioned fear stimulus. Neuroscience. 2004;128(1):7–14. .
    1. Torrisi S, O'Connell K, Davis A, Reynolds R, Balderston N, Fudge JL, et al. Ernst M. Resting state connectivity of the bed nucleus of the stria terminalis at ultra-high field. Human Brain Mapping. 2015;36(10):4076–4088. .
    1. Tyler LK, Chiu S, Zhuang J, Randall B, Devereux BJ, Wright P, et al. Taylor KI. Objects and Categories: Feature Statistics and Object Processing in the Ventral Stream. Journal of Cognitive Neuroscience. 2013;25(10):1723–1735. .
    1. Tyszka JM, Pauli WM. In vivo delineation of subdivisions of the human amygdaloid complex in a high-resolution group template. Human Brain Mapping. 2016 Retrieved from .
    1. Venkatraman V, Rosati AG, Taren AA, Huettel SA. Resolving response, decision, and strategic control: evidence for a functional topography in dorsomedial prefrontal cortex. The Journal of Neuroscience. 2009;29(42):13158–13164.
    1. Vuilleumier P, Driver J. Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions. Philosophical Transactions of the Royal Society of London B: Biological Sciences. 2007;362(1481):837–855. .
    1. Waddell J, Morris RW, Bouton ME. Effects of bed nucleus of the stria terminalis lesions on conditioned anxiety: Aversive conditioning with long-duration conditional stimuli and reinstatement of extinguished fear. Behavioral Neuroscience. 2006;120(2):324–336. .
    1. Wright CI, Fischer Hakan, Whalen PJ, McInerney SC, Shin LM, Rauch SL. Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli. Neuroreport. 2001;12(2):379–383.

Source: PubMed

3
Abonner