1932

Abstract

Regions of the prefrontal and cingulate cortices play important roles in the regulation of behaviors elicited by threat. Dissecting out their differential involvement will greatly increase our understanding of the varied etiology of symptoms of anxiety. I review evidence for altered activity within the major divisions of the prefrontal cortex, including orbitofrontal, ventrolateral, dorsolateral, and ventromedial sectors, along with the anterior cingulate cortex in patients with clinical anxiety. This review is integrated with a discussion of current knowledge about the causal role of these different prefrontal and cingulate regions in threat-elicited behaviors from experimental studies in rodents and monkeys. I highlight commonalities and inconsistencies between species and discuss the current state of our translational success in relating findings across species. Finally, I identify key issues that, if addressed, may improve that success in the future.

[Erratum, Closure]

An erratum has been published for this article:
Erratum: Prefrontal Regulation of Threat-Elicited Behaviors: A Pathway to Translation
Loading

Article metrics loading...

/content/journals/10.1146/annurev-psych-010419-050905
2020-01-04
2024-04-14
Loading full text...

Full text loading...

/deliver/fulltext/psych/71/1/annurev-psych-010419-050905.html?itemId=/content/journals/10.1146/annurev-psych-010419-050905&mimeType=html&fmt=ahah

Literature Cited

  1. Adhikari A, Lerner TN, Finkelstein J, Pak S, Jennings JH et al. 2015. Basomedial amygdala mediates top-down control of anxiety and fear. Nature 527:179–85
    [Google Scholar]
  2. Admon R, Lubin G, Stern O, Rosenberg K, Sela L et al. 2009. Human vulnerability to stress depends on amygdala's predisposition and hippocampal plasticity. PNAS 106:14120–25
    [Google Scholar]
  3. Admon R, Milad MR, Hendler T 2013. A causal model of post-traumatic stress disorder: disentangling predisposed from acquired neural abnormalities. Trends Cogn. Sci. 17:337–47
    [Google Scholar]
  4. Agustín-Pavón C, Braesicke K, Shiba Y, Santangelo AM, Mikheenko Y et al. 2012. Lesions of ventrolateral prefrontal or anterior orbitofrontal cortex in primates heighten negative emotion. Biol. Psychiatry 72:266–72
    [Google Scholar]
  5. Alexander L, Clarke HF, Roberts AC, Alexander L, Clarke HF, Roberts AC 2019a. A focus on the functions of area 25. Brain Sci 9:129
    [Google Scholar]
  6. Alexander L, Gaskin PLR, Sawiak SJ, Fryer TD, Hong YT et al. 2019b. Fractionating blunted reward processing characteristic of anhedonia by over-activating primate subgenual anterior cingulate cortex. Neuron 101:307–20.e6
    [Google Scholar]
  7. Amemori K, Graybiel AM. 2012. Localized microstimulation of primate pregenual cingulate cortex induces negative decision-making. Nat. Neurosci. 15:776–85
    [Google Scholar]
  8. Antoniadis EA, Winslow JT, Davis M, Amaral DG 2007. Role of the primate amygdala in fear-potentiated startle: effects of chronic lesions in the rhesus monkey. J. Neurosci. 27:7386–96
    [Google Scholar]
  9. Aylward J, Hales C, Robinson E, Robinson OJ 2019. Translating a rodent measure of negative bias into humans: the impact of induced anxiety and unmedicated mood and anxiety disorders. Psychol. Med. In press. https://doi.org/10.1017/s0033291718004117
    [Crossref] [Google Scholar]
  10. Balleine BW, O'Doherty JP. 2010. Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 35:48–69
    [Google Scholar]
  11. Baratta MV, Zarza CM, Gomez DM, Campeau S, Watkins LR, Maier SF 2009. Selective activation of dorsal raphe nucleus-projecting neurons in the ventral medial prefrontal cortex by controllable stress. Eur. J. Neurosci. 30:1111–16
    [Google Scholar]
  12. Bari A, Theobald DE, Caprioli D, Mar AC, Aidoo-Micah A et al. 2010. Serotonin modulates sensitivity to reward and negative feedback in a probabilistic reversal learning task in rats. Neuropsychopharmacology 35:1290–301
    [Google Scholar]
  13. Barthas F, Sellmeijer J, Hugel S, Waltisperger E, Barrot M, Yalcin I 2015. The anterior cingulate cortex is a critical hub for pain-induced depression. Biol. Psychiatry 77:236–45
    [Google Scholar]
  14. Bi L-L, Wang J, Luo Z-Y, Chen S-P, Geng F et al. 2013. Enhanced excitability in the infralimbic cortex produces anxiety-like behaviors. Neuropharmacology 72:148–56
    [Google Scholar]
  15. Bijsterbosch J, Smith S, Forster S, John OP, Bishop SJ 2014. Resting state correlates of subdimensions of anxious affect. J. Cogn. Neurosci. 26:914–26
    [Google Scholar]
  16. Birn RM, Shackman AJ, Oler JA, Williams LE, McFarlin DR et al. 2014. Extreme early-life anxiety is associated with an evolutionarily conserved reduction in the strength of intrinsic functional connectivity between the dorsolateral prefrontal cortex and the central nucleus of the amygdala. Mol. Psychiatry 19:853–53
    [Google Scholar]
  17. Bissière S, McAllister KH, Olpe H-R, Cryan JF 2006. The rostral anterior cingulate cortex modulates depression but not anxiety-related behavior in the rat. Behav. Brain Res. 175:195–99
    [Google Scholar]
  18. Bissière S, Plachta N, Hoyer D, McAllister KH, Olpe H-R et al. 2008. The rostral anterior cingulate cortex modulates the efficiency of amygdala-dependent fear learning. Biol. Psychiatry 63:821–31
    [Google Scholar]
  19. Boureau Y-L, Dayan P. 2011. Opponency revisited: competition and cooperation between dopamine and serotonin. Neuropsychopharmacology 36:74–97
    [Google Scholar]
  20. Braunstein LM, Gross JJ, Ochsner KN 2017. Explicit and implicit emotion regulation: a multi-level framework. Soc. Cogn. Affect. Neurosci. 12:1545–57
    [Google Scholar]
  21. Bravo-Rivera C, Roman-Ortiz C, Brignoni-Perez E, Sotres-Bayon F, Quirk GJ 2014. Neural structures mediating expression and extinction of platform-mediated avoidance. J. Neurosci. 34:9736–42
    [Google Scholar]
  22. Britton JC, Grillon C, Lissek S, Norcross MA, Szuhany KL et al. 2013. Response to learned threat: an fMRI study in adolescent and adult anxiety. Am. J. Psychiatry 170:1195–204
    [Google Scholar]
  23. Britton JC, Lissek S, Grillon C, Norcross MA, Pine DS 2011. Development of anxiety: the role of threat appraisal and fear learning. Depression Anxiety 28:5–17
    [Google Scholar]
  24. Brown JS, Kalish HI, Farber IE 1951. Conditioned fear as revealed by magnitude of startle response to an auditory stimulus. J. Exp. Psychol. 41:317–28
    [Google Scholar]
  25. Broyd SJ, Demanuele C, Debener S, Helps SK, James CJ, Sonuga-Barke EJ 2009. Default-mode brain dysfunction in mental disorders: a systematic review. Neurosci. Biobehav. Rev. 33:279–96
    [Google Scholar]
  26. Carlisi CO, Robinson OJ. 2018. The role of prefrontal-subcortical circuitry in negative bias in anxiety: translational, developmental and treatment perspectives. Brain Neurosci. Adv. 2: https://doi.org/10.1177/2398212818774223
    [Crossref] [Google Scholar]
  27. Caseras X, Garner M, Bradley BP, Mogg K 2007. Biases in visual orienting to negative and positive scenes in dysphoria: an eye movement study. J. Abnorm. Psychol. 116:491–97
    [Google Scholar]
  28. Christianson JP, Flyer-Adams JG, Drugan RC, Amat J, Daut RA et al. 2014. Learned stressor resistance requires extracellular signal-regulated kinase in the prefrontal cortex. Front. Behav. Neurosci. 8:348
    [Google Scholar]
  29. Clarke HF, Horst NK, Roberts AC 2015. Regional inactivations of primate ventral prefrontal cortex reveal two distinct mechanisms underlying negative bias in decision making. PNAS 112:4176–81
    [Google Scholar]
  30. Coplan JD, Webler R, Gopinath S, Abdallah CG, Mathew SJ 2018. Neurobiology of the dorsolateral prefrontal cortex in GAD: aberrant neurometabolic correlation to hippocampus and relationship to anxiety sensitivity and IQ. J. Affect. Disord. 229:1–13
    [Google Scholar]
  31. Corbetta M, Shulman GL. 2002. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3:201–15
    [Google Scholar]
  32. Corcoran KA, Quirk GJ. 2007. Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J. Neurosci. 27:840–44
    [Google Scholar]
  33. Costanzi M, Saraulli D, Cannas S, D'Alessandro F, Florenzano F et al. 2014. Fear but not fright: Re-evaluating traumatic experience attenuates anxiety-like behaviors after fear conditioning. Front. Behav. Neurosci. 8:279
    [Google Scholar]
  34. Croteau JD, Schulkin J, Shepard JD 2017. Behavioral effects of chronically elevated corticosterone in subregions of the medial prefrontal cortex. Behav. Brain Res. 316:82–86
    [Google Scholar]
  35. Davis M, Walker DL, Miles L, Grillon C 2010. Phasic versus sustained fear in rats and humans: role of the extended amygdala in fear versus anxiety. Neuropsychopharmacology 35:105–35
    [Google Scholar]
  36. Dias R, Robbins TW, Roberts AC 1996. Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380:69–72
    [Google Scholar]
  37. Dunsmoor JE, Kroes MCW, Li J, Daw ND, Simpson HB, Phelps EA 2019. Role of human ventromedial prefrontal cortex in learning and recall of enhanced extinction. J. Neurosci. 39:3264–76
    [Google Scholar]
  38. Etkin A, Prater KE, Schatzberg AF, Menon V, Greicius MD 2009. Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. Arch. Gen. Psychiatry 66:136172
    [Google Scholar]
  39. Etkin A, Wager TD. 2007. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am. J. Psychiatry 164:1476–88
    [Google Scholar]
  40. Fullana MA, Albajes-Eizagirre A, Soriano-Mas C, Vervliet B, Cardoner N et al. 2018. Fear extinction in the human brain: a meta-analysis of fMRI studies in healthy participants. Neurosci. Biobehav. Rev. 88:16–25
    [Google Scholar]
  41. Gasull-Camós J, Tarrés-Gatius M, Artigas F, Castañé A 2017. Glial GLT-1 blockade in infralimbic cortex as a new strategy to evoke rapid antidepressant-like effects in rats. Transl. Psychiatry 7:e1038
    [Google Scholar]
  42. Giustino TF, Maren S. 2015. The role of the medial prefrontal cortex in the conditioning and extinction of fear. Front. Behav. Neurosci. 9:298
    [Google Scholar]
  43. Gold AL, Steuber ER, White LK, Pacheco J, Sachs JF et al. 2017. Cortical thickness and subcortical gray matter volume in pediatric anxiety disorders. Neuropsychopharmacology 42:2423–33
    [Google Scholar]
  44. Greicius MD, Flores BH, Menon V, Glover GH, Solvason HB et al. 2007. Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol. Psychiatry 62:429–37
    [Google Scholar]
  45. Grillon C, Davis M. 1997. Fear-potentiated startle conditioning in humans: explicit and contextual cue conditioning following paired versus unpaired training. Psychophysiology 34:451–58
    [Google Scholar]
  46. Guyer AE, Lau JYF, McClure-Tone EB, Parrish J, Shiffrin ND et al. 2008. Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. Arch. Gen. Psychiatry 65:130312
    [Google Scholar]
  47. Hartley CA, Phelps EA. 2010. Changing fear: the neurocircuitry of emotion regulation. Neuropsychopharmacology 35:136–46
    [Google Scholar]
  48. Heilbronner SR, Rodriguez-Romaguera J, Quirk GJ, Groenewegen HJ, Haber SN 2016. Circuit-based corticostriatal homologies between rat and primate. Biol. Psychiatry 80:509–21
    [Google Scholar]
  49. Hernandez CM, McQuail JA, Schwabe MR, Burke SN, Setlow B, Bizon JL 2018. Age-related declines in prefrontal cortical expression of metabotropic glutamate receptors that support working memory. eNeuro 5: https://doi.org/10.1523/ENEURO.0164-18.2018
    [Crossref] [Google Scholar]
  50. Hirstein W, Iversen P, Ramachandran VS 2001. Autonomic responses of autistic children to people and objects. Proc. Biol. Sci. 268:1883–88
    [Google Scholar]
  51. Hu Y, Dolcos S. 2017. Trait anxiety mediates the link between inferior frontal cortex volume and negative affective bias in healthy adults. Soc. Cogn. Affect. Neurosci. 12:775–82
    [Google Scholar]
  52. Insel T, Cuthbert B, Garvey M, Heinssen R, Pine DS et al. 2010. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am. J. Psychiatry 167:748–51
    [Google Scholar]
  53. Iwata J, LeDoux JE. 1988. Dissociation of associative and nonassociative concomitants of classical fear conditioning in the freely behaving rat. Behav. Neurosci. 102:66–76
    [Google Scholar]
  54. Izquierdo A, Wellman CL, Holmes A 2006. Brief uncontrollable stress causes dendritic retraction in infra-limbic cortex and resistance to fear extinction in mice. J. Neurosci. 26:5733–38
    [Google Scholar]
  55. Jeon D, Kim S, Chetana M, Jo D, Ruley HE et al. 2010. Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nat. Neurosci. 13:482–88
    [Google Scholar]
  56. Jinks AL, McGregor IS. 1997. Modulation of anxiety-related behaviors following lesions of the prelimbic or infralimbic cortex in the rat. Brain Res 772:181–90
    [Google Scholar]
  57. Johansen JP, Fields HL. 2004. Glutamatergic activation of anterior cingulate cortex produces an aversive teaching signal. Nat. Neurosci. 7:398–403
    [Google Scholar]
  58. Joormann J, Stanton CH. 2016. Examining emotion regulation in depression: a review and future directions. Behav. Res. Ther. 86:35–49
    [Google Scholar]
  59. Kalin NH. 2017. Mechanisms underlying the early risk to develop anxiety and depression: a translational approach. Eur. Neuropsychopharmacol. 27:543–53
    [Google Scholar]
  60. Kalisch R, Korenfeld E, Stephan KE, Weiskopf N, Seymour B, Dolan RJ 2006. Context-dependent human extinction memory is mediated by a ventromedial prefrontal and hippocampal network. J. Neurosci. 26:9503–11
    [Google Scholar]
  61. Kennerley SW, Wallis JD. 2009. Reward-dependent modulation of working memory in lateral prefrontal cortex. J. Neurosci. 29:3259–70
    [Google Scholar]
  62. Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE 2005. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the national comorbidity survey replication. Arch. Gen. Psychiatry 62:593602
    [Google Scholar]
  63. Kim SS, Wang H, Li X-Y, Chen T, Mercaldo V et al. 2011. Neurabin in the anterior cingulate cortex regulates anxiety-like behavior in adult mice. Mol. Brain 4:6
    [Google Scholar]
  64. Klavir O, Genud-Gabai R, Paz R 2012. Low-frequency stimulation depresses the primate anterior-cingulate-cortex and prevents spontaneous recovery of aversive memories. J. Neurosci. 32:8589–97
    [Google Scholar]
  65. Klavir O, Genud-Gabai R, Paz R 2013. Functional connectivity between amygdala and cingulate cortex for adaptive aversive learning. Neuron 80:1290–300
    [Google Scholar]
  66. Koster EHW, Crombez G, Verschuere B, Van Damme S, Wiersema JR 2006. Components of attentional bias to threat in high trait anxiety: facilitated engagement, impaired disengagement, and attentional avoidance. Behav. Res. Ther. 44:1757–71
    [Google Scholar]
  67. Koster EHW, De Lissnyder E, Derakshan N, De Raedt R 2011. Understanding depressive rumination from a cognitive science perspective: the impaired disengagement hypothesis. Clin. Psychol. Rev. 31:138–45
    [Google Scholar]
  68. Krabbe S, Gründemann J, Lüthi A 2018. Amygdala inhibitory circuits regulate associative fear conditioning. Biol. Psychiatry 83:800–9
    [Google Scholar]
  69. Lacroix L, Spinelli S, Heidbreder CA, Feldon J 2000. Differential role of the medial and lateral prefrontal cortices in fear and anxiety. Behav. Neurosci. 114:1119–30
    [Google Scholar]
  70. Lang PJ, McTeague LM, Bradley MM 2016. RDoC, DSM, and the reflex physiology of fear: a biodimensional analysis of the anxiety disorders spectrum. Psychophysiology 53:336–47
    [Google Scholar]
  71. Laubach M, Amarante LM, Swanson K, White SR 2018. What, if anything, is rodent prefrontal cortex?. eNeuro 5: https://doi.org/10.1523/eneuro.0315-18.2018
    [Crossref] [Google Scholar]
  72. LeDoux JE. 2000. Emotion circuits in the brain. Annu. Rev. Neurosci. 23:155–84
    [Google Scholar]
  73. LeDoux JE, Pine DS. 2016. Using neuroscience to help understand fear and anxiety: a two-system framework. Am. J. Psychiatry 173:1083–93
    [Google Scholar]
  74. Li L, Hu X, Preuss TM, Glasser MF, Damen FW et al. 2013. Mapping putative hubs in human, chimpanzee and rhesus macaque connectomes via diffusion tractography. NeuroImage 80:462–74
    [Google Scholar]
  75. Mahfouz A, Huisman SMH, Lelieveldt BPF, Reinders MJT 2017. Brain transcriptome atlases: a computational perspective. Brain Struct. Funct. 222:1557–80
    [Google Scholar]
  76. Maier SF. 2015. Behavioral control blunts reactions to contemporaneous and future adverse events: medial prefrontal cortex plasticity and a corticostriatal network. Neurobiol. Stress 1:12–22
    [Google Scholar]
  77. Makovac E, Meeten F, Watson DR, Herman A, Garfinkel SN et al. 2016. Alterations in amygdala-prefrontal functional connectivity account for excessive worry and autonomic dysregulation in generalized anxiety disorder. Biol. Psychiatry 80:786–95
    [Google Scholar]
  78. Malooly AM, Genet JJ, Siemer M 2013. Individual differences in reappraisal effectiveness: the role of affective flexibility. Emotion 13:302–13
    [Google Scholar]
  79. Mars RB, Verhagen L, Gladwin TE, Neubert F-X, Sallet J, Rushworth MFS 2016. Comparing brains by matching connectivity profiles. Neurosci. Biobehav. Rev. 60:90–97
    [Google Scholar]
  80. Menon V. 2011. Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn. Sci. 15:483–506
    [Google Scholar]
  81. Mikheenko Y, Shiba Y, Sawiak S, Braesicke K, Cockcroft G et al. 2015. Serotonergic, brain volume and attentional correlates of trait anxiety in primates. Neuropsychopharmacology 40:1395–404
    [Google Scholar]
  82. Milad MR, Quirk GJ. 2012. Fear extinction as a model for translational neuroscience: ten years of progress. Annu. Rev. Psychol. 63:129–51
    [Google Scholar]
  83. Milad MR, Quirk GJ, Pitman RK, Orr SP, Fischl B, Rauch SL 2007a. A role for the human dorsal anterior cingulate cortex in fear expression. Biol. Psychiatry 62:1191–94
    [Google Scholar]
  84. Milad MR, Rauch SL, Pitman RK, Quirk GJ 2006. Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol. Psychol. 73:61–71
    [Google Scholar]
  85. Milad MR, Wright CI, Orr SP, Pitman RK, Quirk GJ, Rauch SL 2007b. Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol. Psychiatry 62:446–54
    [Google Scholar]
  86. Mobbs D, Kim JJ. 2015. Neuroethological studies of fear, anxiety, and risky decision-making in rodents and humans. Curr. Opin. Behav. Sci. 5:8–15
    [Google Scholar]
  87. Moench KM, Maroun M, Kavushansky A, Wellman C 2016. Alterations in neuronal morphology in infralimbic cortex predict resistance to fear extinction following acute stress. Neurobiol. Stress 3:23–33
    [Google Scholar]
  88. Monk CS, Nelson EE, McClure EB, Mogg K, Bradley BP et al. 2006. Ventrolateral prefrontal cortex activation and attentional bias in response to angry faces in adolescents with generalized anxiety disorder. Am. J. Psychiatry 163:1091–97
    [Google Scholar]
  89. Monk CS, Telzer EH, Mogg K, Bradley BP, Mai X et al. 2008. Amygdala and ventrolateral prefrontal cortex activation to masked angry faces in children and adolescents with generalized anxiety disorder. Arch. Gen. Psychiatry 65:568–76
    [Google Scholar]
  90. Moriya J, Tanno Y. 2009. Competition between endogenous and exogenous attention to nonemotional stimuli in social anxiety. Emotion 9:739–43
    [Google Scholar]
  91. Moscarello JM, LeDoux JE. 2013. Active avoidance learning requires prefrontal suppression of amygdala-mediated defensive reactions. J. Neurosci. 33:3815–23
    [Google Scholar]
  92. Murphy FC, Michael A, Robbins TW, Sahakian BJ 2003. Neuropsychological impairment in patients with major depressive disorder: the effects of feedback on task performance. Psychol. Med. 33:455–67
    [Google Scholar]
  93. Murray EA, Rudebeck PH. 2018. Specializations for reward-guided decision-making in the primate ventral prefrontal cortex. Nat. Rev. Neurosci. 19:404–17
    [Google Scholar]
  94. Myers-Schulz B, Koenigs M. 2012. Functional anatomy of ventromedial prefrontal cortex: implications for mood and anxiety disorders. Mol. Psychiatry 17:132–41
    [Google Scholar]
  95. Neubert F-X, Mars RB, Sallet J, Rushworth MFS 2015. Connectivity reveals relationship of brain areas for reward-guided learning and decision making in human and monkey frontal cortex. PNAS 112:E2695–704
    [Google Scholar]
  96. Oathes DJ, Patenaude B, Schatzberg AF, Etkin A 2015. Neurobiological signatures of anxiety and depression in resting-state functional magnetic resonance imaging. Biol. Psychiatry 77:385–93
    [Google Scholar]
  97. Ochsner KN, Gross J. 2005. The cognitive control of emotion. Trends Cogn. Sci. 9:242–49
    [Google Scholar]
  98. Ochsner KN, Silvers JA, Buhle JT 2012. Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion. Ann. N. Y. Acad. Sci. 1251:E1–24
    [Google Scholar]
  99. Okon-Singer H, Hendler T, Pessoa L, Shackman AJ 2015. The neurobiology of emotion-cognition interactions: fundamental questions and strategies for future research. Front. Hum. Neurosci. 9:58
    [Google Scholar]
  100. Ongür D, Price JL. 2000. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb. Cortex 10:206–19
    [Google Scholar]
  101. Orsini CA, Trotta RT, Bizon JL, Setlow B 2015. Dissociable roles for the basolateral amygdala and orbitofrontal cortex in decision-making under risk of punishment. J. Neurosci. 35:1368–79
    [Google Scholar]
  102. Pacheco-Unguetti AP, Acosta A, Callejas A, Lupiáñez J 2010. Attention and anxiety: different attentional functioning under state and trait anxiety. Psychol. Sci. 21:298–304
    [Google Scholar]
  103. Palomero-Gallagher N, Zilles K. 2015. Isocortex. The Rat Nervous System G Paxinos 601–25 Amsterdam: Elsevier
    [Google Scholar]
  104. Panayi MC, Killcross S. 2018. Functional heterogeneity within the rodent lateral orbitofrontal cortex dissociates outcome devaluation and reversal learning deficits. eLife 7:e37357
    [Google Scholar]
  105. Paniccia M, Paniccia D, Thomas S, Taha T, Reed N 2017. Clinical and non-clinical depression and anxiety in young people: a scoping review on heart rate variability. Auton. Neurosci. 208:1–14
    [Google Scholar]
  106. Paré D, Quirk GJ, Ledoux JE 2004. New vistas on amygdala networks in conditioned fear. J. Neurophysiol. 92:1–9
    [Google Scholar]
  107. Patel R, Spreng RN, Shin LM, Girard TA 2012. Neurocircuitry models of posttraumatic stress disorder and beyond: a meta-analysis of functional neuroimaging studies. Neurosci. Biobehav. Rev. 36:2130–42
    [Google Scholar]
  108. Paxinos G. 2012. The Marmoset Brain in Stereotaxic Coordinates Amsterdam: Elsevier
  109. Paxinos G, Watson C. 1983. The Rat Brain in Stereotaxic Coordinates Amsterdam: Elsevier
  110. Paxinos G, Watson C. 1998. The Rat Brain in Stereotaxic Coordinates Amsterdam: Elsevier. , 4th ed..
  111. Paxinos G, Watson C. 2013. The Rat Brain in Stereotaxic Coordinates Amsterdam: Elsevier. , 7th ed..
  112. Petrides M, Tomaiuolo F, Yeterian EH, Pandya DN 2012. The prefrontal cortex: comparative architectonic organization in the human and the macaque monkey brains. Cortex 48:46–57
    [Google Scholar]
  113. Phelps EA, Delgado MR, Nearing KI, LeDoux JE 2004. Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43:897–905
    [Google Scholar]
  114. Preuss TM. 1995. Do rats have prefrontal cortex? The Rose-Woolsey-Akert program reconsidered. J. Cogn. Neurosci. 7:1–24
    [Google Scholar]
  115. Price JL. 2007. Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Ann. N. Y. Acad. Sci. 1121:54–71
    [Google Scholar]
  116. Prut L, Belzung C. 2003. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 463:3–33
    [Google Scholar]
  117. Pujara MS, Rudebeck PH, Ciesinski NK, Murray EA 2019. Heightened defensive responses following subtotal lesions of macaque orbitofrontal cortex. J. Neurosci. 39:4133–41
    [Google Scholar]
  118. Ray MH, Hanlon E, McDannald MA 2018. Lateral orbitofrontal cortex partitions mechanisms for fear regulation and alcohol consumption. PLOS ONE 13:e0198043
    [Google Scholar]
  119. Reekie YL, Braesicke K, Man MS, Roberts AC 2008. Uncoupling of behavioral and autonomic responses after lesions of the primate orbitofrontal cortex. PNAS 105:9787–92
    [Google Scholar]
  120. Rich EL, Shapiro ML. 2007. Prelimbic/infralimbic inactivation impairs memory for multiple task switches, but not flexible selection of familiar tasks. J. Neurosci. 27:4747–55
    [Google Scholar]
  121. Roberts AC, Tomic DL, Parkinson CH, Roeling TA, Cutter DJ et al. 2007. Forebrain connectivity of the prefrontal cortex in the marmoset monkey (Callithrix jacchus): an anterograde and retrograde tract-tracing study. J. Comp. Neurol. 502:86–112
    [Google Scholar]
  122. Robinson OJ, Overstreet C, Letkiewicz A, Grillon C 2012. Depressed mood enhances anxiety to unpredictable threat. Psychol. Med. 42:1397–407
    [Google Scholar]
  123. Rodgers RJ, Dalvi A. 1997. Anxiety, defence and the elevated plus-maze. Neurosci. Biobehav. Rev. 21:801–10
    [Google Scholar]
  124. Rodriguez-Romaguera J, Do-Monte FH, Tanimura Y, Quirk GJ, Haber SN 2015. Enhancement of fear extinction with deep brain stimulation: evidence for medial orbitofrontal involvement. Neuropsychopharmacology 40:1726–33
    [Google Scholar]
  125. Roseboom PH, Nanda SA, Bakshi VP, Trentani A, Newman SM, Kalin NH 2007. Predator threat induces behavioral inhibition, pituitary-adrenal activation and changes in amygdala CRF-binding protein gene expression. Psychoneuroendocrinology 32:44–55
    [Google Scholar]
  126. Rudebeck PH, Murray EA. 2014. The orbitofrontal oracle: cortical mechanisms for the prediction and evaluation of specific behavioral outcomes. Neuron 84:1143–56
    [Google Scholar]
  127. Rudebeck PH, Saunders RC, Prescott AT, Chau LS, Murray EA 2013. Prefrontal mechanisms of behavioral flexibility, emotion regulation and value updating. Nat. Neurosci. 16:1140–45
    [Google Scholar]
  128. Rudebeck PH, Walton ME, Millette BHP, Shirley E, Rushworth MFS, Bannerman DM 2007. Distinct contributions of frontal areas to emotion and social behavior in the rat. Eur. J. Neurosci. 26:2315–26
    [Google Scholar]
  129. Rygula R, Clarke HF, Cardinal RN, Cockcroft GJ, Xia J et al. 2015. Role of central serotonin in anticipation of rewarding and punishing outcomes: effects of selective amygdala or orbitofrontal 5-HT depletion. Cereb. Cortex 25:3064–76
    [Google Scholar]
  130. Sanchez A, Vazquez C, Marker C, LeMoult J, Joormann J 2013. Attentional disengagement predicts stress recovery in depression: an eye-tracking study. J. Abnorm. Psychol. 122:303–13
    [Google Scholar]
  131. Sarlitto MC, Foilb AR, Christianson JP 2018. Inactivation of the ventrolateral orbitofrontal cortex impairs flexible use of safety signals. Neuroscience 379:350–58
    [Google Scholar]
  132. Seidlitz J, Váša F, Shinn M, Romero-Garcia R, Whitaker KJ et al. 2018. Morphometric similarity networks detect microscale cortical organization and predict inter-individual cognitive variation. Neuron 97:231–247.e7
    [Google Scholar]
  133. Sekiguchi A, Sugiura M, Taki Y, Kotozaki Y, Nouchi R et al. 2013. Brain structural changes as vulnerability factors and acquired signs of post-earthquake stress. Mol. Psychiatry 18:618–23
    [Google Scholar]
  134. Seligman MEP. 1974. Depression and learned helplessness. The Psychology of Depression: Contemporary Theory and Research RJ Friedman, MM Katz 83–113 New York: Winston-Wiley
    [Google Scholar]
  135. Seligman MEP, Beagley G. 1975. Learned helplessness in the rat. J. Comp. Physiol. Psychol. 88:534–41
    [Google Scholar]
  136. Shackman AJ, Fox AS, Oler JA, Shelton SE, Davidson RJ, Kalin NH 2013. Neural mechanisms underlying heterogeneity in the presentation of anxious temperament. PNAS 110:6145–50
    [Google Scholar]
  137. Shah AA, Treit D. 2003. Excitotoxic lesions of the medial prefrontal cortex attenuate fear responses in the elevated-plus maze, social interaction and shock probe burying tests. Brain Res 969:183–94
    [Google Scholar]
  138. Sharpe MJ, Killcross S. 2018. Modulation of attention and action in the medial prefrontal cortex of rats. Psychol. Rev. 125:822–43
    [Google Scholar]
  139. Sharpe MJ, Schoenbaum G. 2016. Back to basics: making predictions in the orbitofrontal-amygdala circuit. Neurobiol. Learn. Mem. 131:201–6
    [Google Scholar]
  140. Shi Q, Yang L, Shi W, Wang L, Zhou S et al. 2017. The novel cannabinoid receptor GPR55 mediates anxiolytic-like effects in the medial orbital cortex of mice with acute stress. Mol. Brain 10:38
    [Google Scholar]
  141. Shiba Y, Kim C, Santangelo AM, Roberts AC 2015. Lesions of either anterior orbitofrontal cortex or ventrolateral prefrontal cortex in marmoset monkeys heighten innate fear and attenuate active coping behaviors to predator threat. Front. Syst. Neurosci. 8:250
    [Google Scholar]
  142. Shiba Y, Oikonomidis L, Sawiak S, Fryer TD, Hong YT et al. 2017. Converging prefronto-insula-amygdala pathways in negative emotion regulation in marmoset monkeys. Biol. Psychiatry 82:895–903
    [Google Scholar]
  143. Shiba Y, Santangelo AM, Roberts AC 2016. Beyond the medial regions of prefrontal cortex in the regulation of fear and anxiety. Front. Syst. Neurosci. 10:12
    [Google Scholar]
  144. Shin LM, Liberzon I. 2010. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35:169–91
    [Google Scholar]
  145. Sierra-Mercado D, Padilla-Coreano N, Quirk GJ 2010. Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36:529–38
    [Google Scholar]
  146. Stern CAJ, Do Monte FHM, Gazarini L, Carobrez AP, Bertoglio LJ 2010. Activity in prelimbic cortex is required for adjusting the anxiety response level during the elevated plus-maze retest. Neuroscience 170:214–22
    [Google Scholar]
  147. Stevenson CW. 2011. Role of amygdala-prefrontal cortex circuitry in regulating the expression of contextual fear memory. Neurobiol. Learn. Mem. 96:315–23
    [Google Scholar]
  148. Strawn JR, Wehry AM, Chu W-J, Adler CM, Eliassen JC et al. 2013. Neuroanatomic abnormalities in adolescents with generalized anxiety disorder: a voxel-based morphometry study. Depression Anxiety 30:842–48
    [Google Scholar]
  149. Suo X, Lei D, Chen F, Wu M, Li L et al. 2017. Anatomic insights into disrupted small-world networks in pediatric posttraumatic stress disorder. Radiology 282:826–34
    [Google Scholar]
  150. Suzuki S, Saitoh A, Ohashi M, Yamada M, Oka J-I, Yamada M 2016. The infralimbic and prelimbic medial prefrontal cortices have differential functions in the expression of anxiety-like behaviors in mice. Behav. Brain Res. 304:120–24
    [Google Scholar]
  151. Sylvester CM, Corbetta M, Raichle ME, Rodebaugh TL, Schlaggar BL et al. 2012. Functional network dysfunction in anxiety and anxiety disorders. Trends Neurosci 35:527–35
    [Google Scholar]
  152. Tye KM. 2018. Neural circuit motifs in valence processing. Neuron 100:436–52
    [Google Scholar]
  153. van den Heuvel MP, Bullmore ET, Sporns O 2016. Comparative connectomics. Trends Cogn. Sci. 20:345–61
    [Google Scholar]
  154. Van Essen DC, Glasser MF 2018. Parcellating cerebral cortex: how invasive animal studies inform noninvasive mapmaking in humans. Neuron 99:640–63
    [Google Scholar]
  155. Vogt BA, Hof PR, Zilles K, Vogt LJ, Herold C, Palomero-Gallagher N 2013. Cingulate area 32 homologies in mouse, rat, macaque and human: cytoarchitecture and receptor architecture. J. Comp. Neurol. 521:4189–204
    [Google Scholar]
  156. Vogt BA, Paxinos G. 2014. Cytoarchitecture of mouse and rat cingulate cortex with human homologies. Brain Struct. Funct. 219:185–92
    [Google Scholar]
  157. Wallis CU, Cardinal RN, Alexander L, Roberts AC, Clarke HF 2017. Opposing roles of primate areas 25 and 32 and their putative rodent homologs in the regulation of negative emotion. PNAS 114:E4075–84
    [Google Scholar]
  158. Wallis CU, Cockcroft GJ, Cardinal RN, Roberts AC, Clarke HF 2019. Hippocampal interaction with area 25, but not area 32, regulates marmoset approach–avoidance behavior. Cereb. Cortex. In press. https://doi.org/10.1093/cercor/bhz015
    [Crossref] [Google Scholar]
  159. Wellman CL, Moench KM. 2018. Preclinical studies of stress, extinction, and prefrontal cortex: intriguing leads and pressing questions. Psychopharmacology 236:59–72
    [Google Scholar]
  160. Williams L, Lea M, Das P, Liddell BJ, Olivieri G, Peduto AS et al. 2007. Fronto-limbic and autonomic disjunctions to negative emotion distinguish schizophrenia subtypes. Psychiatry Res. Neuroimaging 155:29–44
    [Google Scholar]
  161. Wise SP. 2008. Forward frontal fields: phylogeny and fundamental function. Trends Neurosci 31:599–608
    [Google Scholar]
  162. Zelinski EL, Hong NS, Tyndall AV, Halsall B, McDonald RJ 2010. Prefrontal cortical contributions during discriminative fear conditioning, extinction, and spontaneous recovery in rats. Exp. Brain Res. 203:285–97
    [Google Scholar]
  163. Zeredo JL, Quah SKL, Wallis CU, Alexander L, Cockcroft GJ et al. 2019. Glutamate within the marmoset anterior hippocampus interacts with area 25 to regulate the behavioral and cardiovascular correlates of high-trait anxiety. J. Neurosci. 39:3094–107
    [Google Scholar]
  164. Zhao M-G, Toyoda H, Lee Y-S, Wu L-J, Ko SW et al. 2005. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 47:859–72
    [Google Scholar]
  165. Zimmermann KS, Li C, Rainnie DG, Ressler KJ, Gourley SL 2018. Memory retention involves the ventrolateral orbitofrontal cortex: comparison with the basolateral amygdala. Neuropsychopharmacology 43:373–83
    [Google Scholar]
/content/journals/10.1146/annurev-psych-010419-050905
Loading
/content/journals/10.1146/annurev-psych-010419-050905
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error