Extending the amygdala in theories of threat processing

Trends in Neurosciences

Volumn 38, Issue 5, 2015, Pages 319-329

  Fox, Andrew S ^a,b,c   Oler, Jonathan A ^a,b   Tromp, Do P M ^a,b   Fudge, Julie L ^d   Kalin, Ned H ^a,b,c  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Anxiety; Cross species; Extended amygdala; Gene expression connectivity; Neuroimaging

Indexed keywords

AMYGDALOID NUCLEUS; ANXIETY; ANXIETY DISORDER; BRAIN FUNCTION; CONNECTOME; FEAR; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; META ANALYSIS (TOPIC); NEUROANATOMY; NONHUMAN; PRIMATE; PRIORITY JOURNAL; REVIEW; STRIA TERMINALIS; TEMPERAMENT; THREAT; AMYGDALA; ANIMAL; CYTOLOGY; GENE EXPRESSION; NERVE CELL; NERVE TRACT; NEUROIMAGING; PHYSIOLOGY;

AMYGDALA; ANIMALS; FEAR; GENE EXPRESSION; HUMANS; NEURAL PATHWAYS; NEUROIMAGING; NEURONS;

EID: 84928419337     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2015.03.002     Document Type: Review

References (117)

1. Adolphs R. The biology of fear. Curr. Biol. 2013, 23:R79-R93.
2. Ledoux J. The Emotional Brain: The Mysterious Underpinnings of Emotional Life 1998, Simon and Schuster.
3. Lindquist K.A., et al. The brain basis of emotion: a meta-analytic review. Behav. Brain Sci. 2012, 35:121-143.
4. Paré D., et al. New vistas on amygdala networks in conditioned fear. J. Neurophysiol. 2004, 92:1-9.
5. Phelps E.A. Emotion and cognition: insights from studies of the human amygdala. Annu. Rev. Psychol. 2006, 57:27-53.
6. Rauch S.L., et al. Neuroimaging studies of amygdala function in anxiety disorders. Ann. N. Y. Acad. Sci. 2003, 985:389-410.
7. Ressler K.J., Mayberg H.S. Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic. Nat. Neurosci. 2007, 10:1116-1124.
8. Alheid G.F., Heimer L. New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 1988, 27:1-39.
9. Swanson L.W., Petrovich G.D. What is the amygdala?. Trends Neurosci. 1998, 21:323-331.
10. Walker D.L., et al. Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur. J. Pharmacol. 2003, 463:199-216.
11. Takahashi L.K. Olfactory systems and neural circuits that modulate predator odor fear. Front. Behav. Neurosci. 2014, 8:72.
12. Johnston J.B. Further contributions to the study of the evolution of the forebrain. J. Comp. Neurol. 1923, 35:337-481.
13. Dong H.W., et al. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res. Brain Res. Rev. 2001, 38:192-246.
14. Yilmazer-Hanke D.M. Amygdala. The Human Nervous System 2012, 759-834. Elsevier Academic Press. 3rd edn. J.K. Mai, G. Paxinos (Eds.).
15. Gross C.T., Canteras N.S. The many paths to fear. Nat. Rev. Neurosci. 2012, 13:651-658.
16. Everitt B.J., et al. Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems. Ann. N. Y. Acad. Sci. 1999, 877:412-438.
17. McDonald A.J. Is there an amygdala and how far does it extend? An anatomical perspective. Ann. N. Y. Acad. Sci. 2003, 985:1-21.
18. Zahm D.S. Is the caudomedial shell of the nucleus accumbens part of the extended amygdala? A consideration of connections. Crit. Rev. Neurobiol. 1998, 12:245-265.
19. Davis M., Whalen P.J. The amygdala: vigilance and emotion. Mol. Psychiatry 2001, 6:13-34.
20. Dong H.W., et al. Basic organization of projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis in adult rat brain. J. Comp. Neurol. 2001, 436:430-455.
21. Dong H-W., Swanson L.W. Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis. J. Comp. Neurol. 2004, 468:277-298.
22. Ferry A.T., et al. Prefrontal cortical projections to the striatum in macaque monkeys: evidence for an organization related to prefrontal networks. J. Comp. Neurol. 2000, 425:447-470.
23. Freedman L.J., et al. Subcortical projections of area 25 (subgenual cortex) of the macaque monkey. J. Comp. Neurol. 2000, 421:172-188.
24. McDonald A.J., et al. Cortical afferents to the extended amygdala. Ann. N. Y. Acad. Sci. 1999, 877:309-338.
25. Saper C.B. Convergence of autonomic and limbic connections in the insular cortex of the rat. J. Comp. Neurol. 1982, 210:163-173.
26. Bota M., Swanson L.W. Online workbenches for neural network connections. J. Comp. Neurol. 2007, 500:807-814.
27. Avery S.N., et al. BNST neurocircuitry in humans. Neuroimage 2014, 91:311-323.
28. Roy A.K., et al. Functional connectivity of the human amygdala using resting state fMRI. Neuroimage 2009, 45:614-626.
29. Oler J.A., et al. Evidence for coordinated functional activity within the extended amygdala of non-human and human primates. Neuroimage 2012, 61:1059-1066.
30. De Olmos J.S., Heimer L. The concepts of the ventral striatopallidal system and extended amygdala. Ann. N. Y. Acad. Sci. 1999, 877:1-32.
31. McDonald A.J. Cytoarchitecture of the central amygdaloid nucleus of the rat. J. Comp. Neurol. 1982, 208:401-418.
32. McDonald A.J. Neurons of the bed nucleus of the stria terminalis: a golgi study in the rat. Brain Res. Bull. 1983, 10:111-120.
33. Gray T.S., Magnuson D.J. Peptide immunoreactive neurons in the amygdala and the bed nucleus of the stria terminalis project to the midbrain central gray in the rat. Peptides 1992, 13:451-460.
34. Bupesh M., et al. Genetic and experimental evidence supports the continuum of the central extended amygdala and a mutiple embryonic origin of its principal neurons. J. Comp. Neurol. 2011, 519:3507-3531.
35. Lein E.S., et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
36. Grange P., et al. Cell-type-based model explaining coexpression patterns of genes in the brain. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:5397-5402.
37. Ng L., et al. An anatomic gene expression atlas of the adult mouse brain. Nat. Neurosci. 2009, 12:356-362.
38. Preuss T.M., et al. Distinctive compartmental organization of human primary visual cortex. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:11601-11606.
39. Yellin A.M., Jerison H.J. Visual evoked potentials and inter-stimulus intervals in the rat. Electroencephalogr. Clin. Neurophysiol. 1973, 34:429-432.
40. Pitkänen A., Amaral D.G. Organization of the intrinsic connections of the monkey amygdaloid complex: projections originating in the lateral nucleus. J. Comp. Neurol. 1998, 398:431-458.
41. Turner B.H., et al. Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey. J. Comp. Neurol. 1980, 191:515-543.
42. Chareyron L.J., et al. Stereological analysis of the rat and monkey amygdala. J. Comp. Neurol. 2011, 519:3218-3239.
43. deCampo D.M., Fudge J.L. Where and what is the paralaminar nucleus? A review on a unique and frequently overlooked area of the primate amygdala. Neurosci. Biobehav. Rev. 2012, 36:520-535.
44. Andy O.J., Stephan H. The septum in the human brain. J. Comp. Neurol. 1968, 133:383-410.
45. Price J.L., et al. The limbic region. II. The amygdaloid complex. Handbook of Chemical Neuroanatomy 1987, 279-381. Elsevier. B. Hokfelt, L.W. Swanson (Eds.).
46. Stephan H., Andy O.J. Quantitative comparison of the amygdala in insectivores and primates. Acta Anat. (Basel) 1977, 98:130-153.
47. Davis M., et al. Amygdala and bed nucleus of the stria terminalis: differential roles in fear and anxiety measured with the acoustic startle reflex. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 1997, 352:1675-1687.
48. Davis M., et al. Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 2010, 35:105-135.
49. Waddell J., et al. Effects of bed nucleus of the stria terminalis lesions on conditioned anxiety: aversive conditioning with long-duration conditional stimuli and reinstatement of extinguished fear. Behav. Neurosci. 2006, 120:324-336.
50. Sink K.S., et al. Calcitonin gene-related peptide in the bed nucleus of the stria terminalis produces an anxiety-like pattern of behavior and increases neural activation in anxiety-related structures. J. Neurosci. 2011, 31:1802-1810.
51. Sink K.S., et al. CGRP antagonist infused into the bed nucleus of the stria terminalis impairs the acquisition and expression of context but not discretely cued fear. Learn. Mem. 2013, 20:730-739.
52. Walker D.L., Davis M. Quantifying fear potentiated startle using absolute versus proportional increase scoring methods: implications for the neurocircuitry of fear and anxiety. Psychopharmacology (Berl.) 2002, 164:318-328.
53. Duvarci S., et al. The bed nucleus of the stria terminalis mediates inter-individual variations in anxiety and fear. J. Neurosci. 2009, 29:10357-10361.
54. Likhtik E., et al. Amygdala intercalated neurons are required for expression of fear extinction. Nature 2008, 454:642-645.
55. Royer S., et al. An inhibitory interface gates impulse traffic between the input and output stations of the amygdala. J. Neurosci. 1999, 19:10575-10583.
56. Ciocchi S., et al. Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 2010, 468:277-282.
57. Viviani D., et al. Oxytocin selectively gates fear responses through distinct outputs from the central amygdala. Science 2011, 333:104-107.
58. Haubensak W., et al. Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 2010, 468:270-276.
59. Pape H-C., Pare D. Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol. Rev. 2010, 90:419-463.
60. Pare D., Duvarci S. Amygdala microcircuits mediating fear expression and extinction. Curr. Opin. Neurobiol. 2012, 22:717-723.
61. Kim S-Y., et al. Diverging neural pathways assemble a behavioural state from separable features in anxiety. Nature 2013, 496:219-223.
62. Fox A.S., Kalin N.H. A translational neuroscience approach to understanding the development of social anxiety disorder and its pathophysiology. Am. J. Psychiatry 2014, 171:1162-1173.
63. Oler J.A., et al. The central nucleus of the amygdala is a critical substrate for individual differences in anxiety. To appear in Living without an amygdala 2015, Guilford Press, in press. D.G. Amaral, R. Adolphs (Eds.).
64. Kalin N.H., Shelton S.E. Defensive behaviors in infant rhesus monkeys: environmental cues and neurochemical regulation. Science 1989, 243:1718-1721.
65. Fox A.S., et al. Calling for help is independently modulated by brain systems underlying goal-directed behavior and threat perception. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:4176-4179.
66. Fox A.S., et al. Trait-like brain activity during adolescence predicts anxious temperament in primates. PLoS ONE 2008, 3:e2570.
67. Kalin N.H., et al. Brain regions associated with the expression and contextual regulation of anxiety in primates. Biol. Psychiatry 2005, 58:796-804.
68. Oler J.A., et al. Serotonin transporter availability in the amygdala and bed nucleus of the stria terminalis predicts anxious temperament and brain glucose metabolic activity. J. Neurosci. 2009, 29:9961-9966.
69. Oler J.A., et al. Amygdalar and hippocampal substrates of anxious temperament differ in their heritability. Nature 2010, 466:864-868.
70. Shackman A.J., et al. Neural mechanisms underlying heterogeneity in the presentation of anxious temperament. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:6145-6150.
71. Fox A.S., et al. Central amygdala nucleus (Ce) gene expression linked to increased trait-like Ce metabolism and anxious temperament in young primates. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:18108-18113.
72. Kalin N.H., et al. The role of the central nucleus of the amygdala in mediating fear and anxiety in the primate. J. Neurosci. 2004, 24:5506-5515.
73. Kalin N.H., et al. The primate amygdala mediates acute fear but not the behavioral and physiological components of anxious temperament. J. Neurosci. 2001, 21:2067-2074.
74. Kalin N.H., et al. Role of the primate orbitofrontal cortex in mediating anxious temperament. Biol. Psychiatry 2007, 62:1134-1139.
75. Machado C.J., Bachevalier J. Behavioral and hormonal reactivity to threat: effects of selective amygdala, hippocampal or orbital frontal lesions in monkeys. Psychoneuroendocrinology 2008, 33:926-941.
76. Murray E.A., Izquierdo A. Orbitofrontal cortex and amygdala contributions to affect and action in primates. Ann. N. Y. Acad. Sci. 2007, 1121:273-296.
77. Fox A.S., et al. Orbitofrontal cortex lesions alter anxiety-related activity in the primate bed nucleus of stria terminalis. J. Neurosci. 2010, 30:7023-7027.
78. Whalen P.J., et al. A functional MRI study of human amygdala responses to facial expressions of fear versus anger. Emotion 2001, 1:70-83.
79. Somerville L.H., et al. Human bed nucleus of the stria terminalis indexes hypervigilant threat monitoring. Biol. Psychiatry 2010, 68:416-424.
80. Mobbs D., et al. Neural activity associated with monitoring the oscillating threat value of a tarantula. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:20582-20586.
81. Mobbs D., et al. When fear is near: threat imminence elicits prefrontal-periaqueductal gray shifts in humans. Science 2007, 317:1079-1083.
82. Coaster M., et al. Variables influencing the neural correlates of perceived risk of physical harm. Cogn. Affect. Behav. Neurosci. 2011, 11:494-507.
83. Somerville L.H., et al. Interactions between transient and sustained neural signals support the generation and regulation of anxious emotion. Cereb. Cortex 2013, 23:49-60.
84. Grupe D.W., et al. Dissecting the anticipation of aversion reveals dissociable neural networks. Cereb. Cortex 2013, 23:1874-1883.
85. Alvarez R.P., et al. Phasic and sustained fear in humans elicits distinct patterns of brain activity. Neuroimage 2011, 55:389-400.
86. Choi J.M., et al. Impact of state anxiety on the interaction between threat monitoring and cognition. Neuroimage 2012, 59:1912-1923.
87. Klumpers F., et al. Dorsomedial prefrontal cortex mediates the impact of serotonin transporter linked polymorphic region genotype on anticipatory threat reactions. Biol. Psychiatry 2014, Published Online: August 26, 2014. 10.1016/j.biopsych.2014.07.034.
88. Motzkin J.C., et al. Ventromedial prefrontal cortex damage alters resting blood flow to the bed nucleus of stria terminalis. Cortex 2014, 64C:281-288.
89. 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 2007, 164:1476-1488.
90. Handbook of Emotions 2008, The Guilford Press. 3rd edn. M. Lewis (Ed.).
91. Mechias M-L., et al. A meta-analysis of instructed fear studies: implications for conscious appraisal of threat. Neuroimage 2010, 49:1760-1768.
92. Yarkoni T., et al. Large-scale automated synthesis of human functional neuroimaging data. Nat. Methods 2011, 8:665-670.
93. Coan J.A., et al. Lending a hand: social regulation of the neural response to threat. Psychol. Sci. 2006, 17:1032-1039.
94. Dunsmoor J.E., et al. Neurobehavioral mechanisms of human fear generalization. Neuroimage 2011, 55:1878-1888.
95. Levita L., et al. Avoidance of harm and anxiety: a role for the nucleus accumbens. Neuroimage 2012, 62:189-198.
96. Morey R.A., et al. The role of trauma-related distractors on neural systems for working memory and emotion processing in posttraumatic stress disorder. J. Psychiatr. Res. 2009, 43:809-817.
97. Yassa M.A., et al. Functional MRI of the amygdala and bed nucleus of the stria terminalis during conditions of uncertainty in generalized anxiety disorder. J. Psychiatr. Res. 2012, 46:1045-1052.
98. Mai J.K., et al. Atlas of the Human Brain 2007, Academic Press. 3rd edn.
99. Paxinos G. The Rhesus Monkey Brain in Stereotaxic Coordinates 2009, Academic Press. 2nd edn.
100. Heimer L., et al. The human basal forebrain. Part II. Handbook of Chemical Neuroanatomy 1999, Vol. 15:57-226. Elsevier.
101. Holland P.C., Gallagher M. Amygdala circuitry in attentional and representational processes. Trends Cogn. Sci. 1999, 3:65-73.
102. Comoli E., et al. Functional mapping of the prosencephalic systems involved in organizing predatory behavior in rats. Neuroscience 2005, 130:1055-1067.
103. Knapska E., et al. Functional internal complexity of amygdala: focus on gene activity mapping after behavioral training and drugs of abuse. Physiol. Rev. 2007, 87:1113-1173.
104. Jennings J.H., et al. Distinct extended amygdala circuits for divergent motivational states. Nature 2013, 496:224-228.
105. Choi J.M., et al. Pervasive competition between threat and reward in the brain. Soc. Cogn. Affect. Neurosci. 2014, 9:737-750.
106. Reynolds S.M., Berridge K.C. Emotional environments retune the valence of appetitive versus fearful functions in nucleus accumbens. Nat. Neurosci. 2008, 11:423-425.
107. Gabriel M., et al. Consideration of a unified model of amygdalar associative functions. Ann. N. Y. Acad. Sci. 2003, 985:206-217.
108. Stamatakis A.M., et al. Amygdala and bed nucleus of the stria terminalis circuitry: implications for addiction-related behaviors. Neuropharmacology 2014, 76B:320-328.
109. Canteras N.S., et al. Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J. Comp. Neurol. 1995, 360:213-245.
110. Kemble E.D., et al. Taming in wild rats following medial amygdaloid lesions. Physiol. Behav. 1984, 32:131-134.
111. Roseboom P.H., et al. Predator threat induces behavioral inhibition, pituitary-adrenal activation and changes in amygdala CRF-binding protein gene expression. Psychoneuroendocrinology 2007, 32:44-55.
112. Martinez R.C., et al. Amygdalar roles during exposure to a live predator and to a predator-associated context. Neuroscience 2011, 172:314-328.
113. Wallis J.D. Cross-species studies of orbitofrontal cortex and value-based decision-making. Nat. Neurosci. 2012, 15:13-19.
114. Buhle J.T., et al. Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. Cereb. Cortex 2014, 11:2981-2990.
115. Wilent W.B., et al. Induction of panic attack by stimulation of the ventromedial hypothalamus. J. Neurosurg. 2010, 112:1295-1298.
116. Nashold B.S., et al. Sensations evoked by stimulation in the midbrain of man. J. Neurosurg. 1969, 30:14-24.
117. McMenamin B.W., et al. Network organization unfolds over time during periods of anxious anticipation. J. Neurosci. 2014, 34:11261-11273.