Posterior insular cortex is necessary for conditioned inhibition of fear

Neurobiology of Learning and Memory

Volumn 134, Issue Part B, 2016, Pages 317-327

  Foilb, Allison R ^a   Flyer Adams, Johanna G ^b   Maier, Steven F ^b   Christianson, John P ^a,b  

^a BOSTON COLLEGE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Fear; Inhibition; Insula; Plasticity; Rat

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; MUSCIMOL; 2-AMINO-5-PHOSPHOPENTANOIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; VALINE;

ADULT; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; CONDITIONED INHIBITION OF FEAR; CONDITIONING; CONTROLLED STUDY; FEAR; INHIBITION (PSYCHOLOGY); LEARNING; MALE; NERVE CELL PLASTICITY; NONHUMAN; PERCEPTIVE DISCRIMINATION; POSTERIOR INSULA; RAT; RECALL; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN CORTEX; CONDITIONED REFLEX; DRUG EFFECTS; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CEREBRAL CORTEX; CONDITIONING, CLASSICAL; FEAR; GABA-A RECEPTOR AGONISTS; INHIBITION (PSYCHOLOGY); MALE; MENTAL RECALL; MUSCIMOL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; VALINE;

EID: 84992108773     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2016.08.004     Document Type: Article

References (77)

1. Amano, T., Unal, C.T., Paré, D., Synaptic correlates of fear extinction in the amygdala. Nature Neuroscience 13 (2010), 489–494, 10.1038/nn.2499.
2. Amat, J., Baratta, M.V., Paul, E., Bland, S.T., Watkins, L.R., Maier, S.F., Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nature Neuroscience 8 (2005), 365–371, 10.1038/nn1399.
3. Amat, J., Christianson, J.P., Aleksejev, R.M., Kim, J., Richeson, K.R., Watkins, L.R., Maier, S.F., Control over a stressor involves the posterior dorsal striatum and the act/outcome circuit. European Journal of Neuroscience 40 (2014), 2352–2358, 10.1111/ejn.12609.
4. Bast, T., da Silva, B.M., Morris, R.G., Distinct contributions of hippocampal NMDA and AMPA receptors to encoding and retrieval of one-trial place memory. Journal of Neuroscience 25 (2005), 5845–5856, 10.1523/JNEUROSCI.0698-05.2005.
5. Benison, A.M., Rector, D.M., Barth, D.S., Hemispheric mapping of secondary somatosensory cortex in the rat. Journal of Neurophysiology 97 (2007), 200–207, 10.1152/jn.00673.2006.
6. Bermudez-Rattoni, F., The forgotten insular cortex: Its role on recognition memory formation. Neurobiology of Learning and Memory 109 (2014), 207–216, 10.1016/j.nlm.2014.01.001.
7. Bouton, M.E., Westbrook, R.F., Corcoran, K.A., Maren, S., Contextual and temporal modulation of extinction: Behavioral and biological mechanisms. Biological Psychiatry 60 (2006), 352–360, 10.1016/j.biopsych.2005.12.015.
8. Campeau, S., Falls, W.A., Cullinan, W.E., Helmreich, D.L., Davis, M., Watson, S.J., Elicitation and reduction of fear: Behavioural and neuroendocrine indices and brain induction of the immediate-early gene c-fos. Neuroscience 78 (1997), 1087–1104.
9. Campolattaro, M.M., Freeman, J.H., Perirhinal cortex lesions impair feature-negative discrimination. Neurobiology of Learning and Memory 86 (2006), 205–213, 10.1016/j.nlm.2006.03.001.
10. Casanova, J.P., Madrid, C., Contreras, M., Rodríguez, M., Vasquez, M., Torrealba, F., A role for the interoceptive insular cortex in the consolidation of learned fear. Behavioural Brain Research 296 (2016), 70–77, 10.1016/j.bbr.2015.08.032.
11. Chen, V.M., Foilb, A.R., Christianson, J.P., Inactivation of ventral hippocampus interfered with cued-fear acquisition but did not influence later recall or discrimination. Behavioural Brain Research 296 (2015), 249–253, 10.1016/j.bbr.2015.09.008.
12. Christianson, J.P., Benison, A.M., Jennings, J., Sandsmark, E.K., Amat, J., Kaufman, R.D.,.. Maier, S.F., The sensory insular cortex mediates the stress-buffering effects of safety signals but not behavioral control. Journal of Neuroscience 28 (2008), 13703–13711, 10.1523/JNEUROSCI.4270-08.2008.
13. Christianson, J.P., Fernando, A.B., Kazama, A.M., Jovanovic, T., Ostroff, L.E., Sangha, S., Inhibition of fear by learned safety signals: A mini-symposium review. Journal of Neuroscience 32 (2012), 14118–14124, 10.1523/JNEUROSCI.3340-12.2012.
14. Christianson, J.P., Flyer-Adams, J.G., Drugan, R.C., Amat, J., Daut, R.A., Foilb, A.R.,.. Maier, S.F., Learned stressor resistance requires extracellular signal-regulated kinase in the prefrontal cortex. Frontiers in Behavioral Neuroscience, 8, 2014, 348.
15. Christianson, J.P., Jennings, J.H., Ragole, T., Flyer, J.G., Benison, A.M., Barth, D.S.,.. Maier, S.F., Safety signals mitigate the consequences of uncontrollable stress via a circuit involving the sensory insular cortex and bed nucleus of the stria terminalis. Biological Psychiatry 70 (2011), 458–464, 10.1016/j.biopsych.2011.04.004.
16. Etkin, A., Wager, T.D., Functional neuroimaging of anxiety: A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry 164 (2007), 1476–1488, 10.1176/appi.ajp.2007.07030504.
17. Falls, W.A., Bakken, K.T., Heldt, S.A., Lesions of the perirhinal cortex interfere with conditioned excitation but not with conditioned inhibition of fear. Behavioral Neuroscience 111 (1997), 476–486.
18. Falls, W.A., Davis, M., Lesions of the central nucleus of the amygdala block conditioned excitation, but not conditioned inhibition of fear as measured with the fear-potentiated startle effect. Behavioral Neuroscience 109 (1995), 379–387.
19. Flynn, F.G., Anatomy of the insula functional and clinical correlates. Aphasiology 13 (1999), 55–78.
20. Foilb, A.R., Christianson, J.P., Serotonin 2C receptor antagonist improves fear discrimination and subsequent safety signal recall. Progress in Neuro-Psychopharmacology and Biological Psychiatry 65 (2015), 78–84, 10.1016/j.pnpbp.2015.08.017.
21. Gastelum, E.D., Guilhardi, P., Burwell, R.D., The effects of combined perirhinal and postrhinal damage on complex discrimination tasks. Hippocampus 22 (2012), 2059–2067, 10.1002/hipo.22063.
22. Genud-Gabai, R., Klavir, O., Paz, R., Safety signals in the primate amygdala. Journal of Neuroscience 33 (2013), 17986–17994, 10.1523/JNEUROSCI.1539-13.2013.
23. Gewirtz, J.C., Falls, W.A., Davis, M., Normal conditioned inhibition and extinction of freezing and fear-potentiated startle following electrolytic lesions of medical prefrontal cortex in rats. Behavioral Neuroscience 111 (1997), 712–726.
24. Gogolla, N., Takesian, A.E., Feng, G., Fagiolini, M., Hensch, T.K., Sensory integration in mouse insular cortex reflects GABA circuit maturation. Neuron 83 (2014), 894–905, 10.1016/j.neuron.2014.06.033.
25. Guldin, W.O., Markowitsch, H.J., Cortical and thalamic afferent connections of the insular and adjacent cortex of the rat. Journal of Comparative Neurology 215 (1983), 135–153, 10.1002/cne.902150203.
26. Heldt, S.A., Falls, W.A., Destruction of the auditory thalamus disrupts the production of fear but not the inhibition of fear conditioned to an auditory stimulus. Brain Research 813 (1998), 274–282.
27. Heldt, S.A., Falls, W.A., Posttraining lesions of the auditory thalamus, but not cortex, disrupt the inhibition of fear conditioned to an auditory stimulus. European Journal of Neuroscience 23 (2006), 765–779, 10.1111/j.1460-9568.2006.04604.x.
28. Holland, P.C., Role of amygdala central nucleus in feature negative discriminations. Behavioral Neuroscience 126 (2012), 670–680, 10.1037/a0029600.
29. Izquierdo, I., Quillfeldt, J.A., Zanatta, M.S., Quevedo, J., Schaeffer, E., Schmitz, P.K., Medina, J.H., Sequential role of hippocampus and amygdala, entorhinal cortex and parietal cortex in formation and retrieval of memory for inhibitory avoidance in rats. European Journal of Neuroscience 9 (1997), 786–793.
30. Johansen, J.P., Cain, C.K., Ostroff, L.E., LeDoux, J.E., Molecular mechanisms of fear learning and memory. Cell 147 (2011), 509–524, 10.1016/j.cell.2011.10.009.
31. Josselyn, S.A., Falls, W.A., Gewirtz, J.C., Pistell, P., Davis, M., The nucleus accumbens is not critically involved in mediating the effects of a safety signal on behavior. Neuropsychopharmacology 30 (2005), 17–26, 10.1038/sj.npp.1300530.
32. Jovanovic, T., Norrholm, S.D., Blanding, N.Q., Davis, M., Duncan, E., Bradley, B., Ressler, K.J., Impaired fear inhibition is a biomarker of PTSD but not depression. Depress Anxiety 27 (2010), 244–251, 10.1002/da.20663.
33. Kim, J.J., Jung, M.W., Neural circuits and mechanisms involved in Pavlovian fear conditioning: A critical review. Neuroscience and Biobehavioral Reviews 30 (2006), 188–202, 10.1016/j.neubiorev.2005.06.005.
34. Kong, E., Monje, F.J., Hirsch, J., Pollak, D.D., Learning not to fear: Neural correlates of learned safety. Neuropsychopharmacology 39 (2014), 515–527, 10.1038/npp.2013.191.
35. Konorski, J. (1948). Conditioned reflexes and neuron organization.
36. Konorski, J. (1967). Integrative activity of the brain.
37. LeDoux, J.E., Coming to terms with fear. Proceedings of the National Academy of Sciences of the United States of America 111 (2014), 2871–2878, 10.1073/pnas.1400335111.
38. Likhtik, E., Stujenske, J.M., Topiwala, M.A., Harris, A.Z., Gordon, J.A., Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety. Nature Neuroscience 17 (2014), 106–113, 10.1038/nn.3582.
39. Lister, S., Pearce, J.M., Butcher, S.P., Collard, K.J., Foster, G.A., Acquisition of conditioned inhibition in rats is impaired by ablation of serotoninergic pathways. European Journal of Neuroscience 8 (1996), 415–423.
40. MacLeod, J.E., Bucci, D.J., Contributions of the subregions of the medial prefrontal cortex to negative occasion setting. Behavioral Neuroscience 124 (2010), 321–328, 10.1037/a0019344.
41. Maren, S., Neurobiology of Pavlovian fear conditioning. Annual Review of Neuroscience 24 (2001), 897–931, 10.1146/annurev.neuro.24.1.897.
42. McDonald, A.J., Shammah-Lagnado, S.J., Shi, C., Davis, M., Cortical afferents to the extended amygdala. Annals of the New York Academy of Sciences 877 (1999), 309–338.
43. McNally, G.P., Westbrook, R.F., Predicting danger: The nature, consequences, and neural mechanisms of predictive fear learning. Learning & Memory 13 (2006), 245–253, 10.1101/lm.196606.
44. Meyer, H.C., Bucci, D.J., The contribution of medial prefrontal cortical regions to conditioned inhibition. Behavioral Neuroscience 128 (2014), 644–653, 10.1037/bne0000023.
45. Miller, M.W., Vogt, B.A., Direct connections of rat visual cortex with sensory, motor, and association cortices. Journal of Comparative Neurology 226 (1984), 184–202, 10.1002/(ISSN)1096-9861.
46. Morris, R.G., NMDA receptors and memory encoding. Neuropharmacology 74 (2013), 32–40, 10.1016/j.neuropharm.2013.04.014.
47. Moscarello, J.M., LeDoux, J.E., Active avoidance learning requires prefrontal suppression of amygdala-mediated defensive reactions. Journal of Neuroscience 33 (2013), 3815–3823, 10.1523/JNEUROSCI.2596-12.2013.
48. Mufson, E.J., Mesulam, M.M., Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum. Journal of Comparative Neurology 212 (1982), 23–37, 10.1002/cne.902120103.
49. Myers, K.M., Davis, M., AX+, BX-discrimination learning in the fear-potentiated startle paradigm: Possible relevance to inhibitory fear learning in extinction. Learning & Memory 11 (2004), 464–475, 10.1101/lm.74704.
50. Ostroff, L.E., Cain, C.K., Bedont, J., Monfils, M.H., Ledoux, J.E., Fear and safety learning differentially affect synapse size and dendritic translation in the lateral amygdala. Proceedings of the National Academy of Sciences of the United States of America 107 (2010), 9418–9423, 10.1073/pnas.0913384107.
51. Pavlov, I. P. (1927). Conditioned reflexes: An investigation of the physiological activity of cerebral cortex (Anrep, G. V., Trans.). London, Oxford University Press.
52. Paxinos, G., Watson, C., The rat brain in stereotaxic coordinates. 6th ed.: Hard Cover Edition, 2007, Academic Press.
53. Phelps, E.A., O'Connor, K.J., Gatenby, J.C., Gore, J.C., Grillon, C., Davis, M., Activation of the left amygdala to a cognitive representation of fear. Nature Neuroscience 4 (2001), 437–441, 10.1038/86110.
54. Ploghaus, A., Tracey, I., Gati, J.S., Clare, S., Menon, R.S., Matthews, P.M., Rawlins, J.N., Dissociating pain from its anticipation in the human brain. Science 284 (1999), 1979–1981.
55. Polack, C.W., Laborda, M.A., Miller, R.R., Extinction context as a conditioned inhibitor. Learning & Behavior 40 (2012), 24–33, 10.3758/s13420-011-0039-1.
56. Pollak, D.D., Monje, F.J., Zuckerman, L., Denny, C.A., Drew, M.R., Kandel, E.R., An animal model of a behavioral intervention for depression. Neuron 60 (2008), 149–161, 10.1016/j.neuron.2008.07.041.
57. Rauch, S.L., Shin, L.M., Phelps, E.A., Neurocircuitry models of posttraumatic stress disorder and extinction: Human neuroimaging research–past, present, and future. Biological Psychiatry 60 (2006), 376–382, 10.1016/j.biopsych.2006.06.004.
58. Remple, M.S., Henry, E.C., Catania, K.C., Organization of somatosensory cortex in the laboratory rat (Rattus norvegicus): Evidence for two lateral areas joined at the representation of the teeth. Journal of Comparative Neurology 467 (2003), 105–118, 10.1002/cne.10909.
59. Rescorla, R.A., Conditioned inhibition of fear resulting from negative CS-US contingencies. Journal of Comparative and Physiological Psychology 67 (1969), 504–509.
60. Rhodes, S.E., Killcross, A.S., Lesions of rat infralimbic cortex result in disrupted retardation but normal summation test performance following training on a Pavlovian conditioned inhibition procedure. European Journal of Neuroscience 26 (2007), 2654–2660, 10.1111/j.1460-9568.2007.05855.x.
61. Robinson, C.J., Burton, H., Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insula of M. fascicularis. Journal of Comparative Neurology 192 (1980), 69–92, 10.1002/cne.901920105.
62. Robinson, C.J., Burton, H., Somatic submodality distribution within the second somatosensory (SII), 7b, retroinsular, postauditory, and granular insular cortical areas of M. fascicularis. Journal of Comparative Neurology 192 (1980), 93–108, 10.1002/cne.901920106.
63. Robinson, C.J., Burton, H., Somatotopographic organization in the second somatosensory area of M. fascicularis. Journal of Comparative Neurology 192 (1980), 43–67, 10.1002/cne.901920104.
64. Robinson, S., Keene, C.S., Iaccarino, H.F., Duan, D., Bucci, D.J., Involvement of retrosplenial cortex in forming associations between multiple sensory stimuli. Behavioral Neuroscience 125 (2011), 578–587, 10.1037/a0024262.
65. Rodgers, K.M., Benison, A.M., Klein, A., Barth, D.S., Auditory, somatosensory, and multisensory insular cortex in the rat. Cerebral Cortex 18 (2008), 2941–2951, 10.1093/cercor/bhn054.
66. Rogan, M.T., Leon, K.S., Perez, D.L., Kandel, E.R., Distinct neural signatures for safety and danger in the amygdala and striatum of the mouse. Neuron 46 (2005), 309–320, 10.1016/j.neuron.2005.02.017.
67. Rosen, J.B., Hitchcock, J.M., Miserendino, M.J., Falls, W.A., Campeau, S., Davis, M., Lesions of the perirhinal cortex but not of the frontal, medial prefrontal, visual, or insular cortex block fear-potentiated startle using a visual conditioned stimulus. Journal of Neuroscience 12 (1992), 4624–4633.
68. Rosenzweig, M.R., Bennett, E.L., Psychobiology of plasticity: Effects of training and experience on brain and behavior. Behavioural Brain Research 78 (1996), 57–65.
69. Sangha, S., Chadick, J.Z., Janak, P.H., Safety encoding in the basal amygdala. Journal of Neuroscience 33 (2013), 3744–3751, 10.1523/JNEUROSCI.3302-12.2013.
70. Sangha, S., Robinson, P.D., Greba, Q., Davies, D.A., Howland, J.G., Alterations in reward, fear and safety cue discrimination after inactivation of the rat prelimbic and infralimbic cortices. Neuropsychopharmacology 39 (2014), 2405–2413, 10.1038/npp.2014.89.
71. Shi, C.J., Cassell, M.D., Cascade projections from somatosensory cortex to the rat basolateral amygdala via the parietal insular cortex. Journal of Comparative Neurology 399 (1998), 469–491.
72. Shi, C.J., Cassell, M.D., Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. Journal of Comparative Neurology 399 (1998), 440–468.
73. Shi, C., Davis, M., Pain pathways involved in fear conditioning measured with fear-potentiated startle: Lesion studies. Journal of Neuroscience 19 (1999), 420–430.
74. Sudakov, K., MacLean, P.D., Reeves, A., Marino, R., Unit study of exteroceptive inputs to claustrocortex in awake, sitting, squirrel monkey. Brain Research 28 (1971), 19–34.
75. Tronson, N.C., Corcoran, K.A., Jovasevic, V., Radulovic, J., Fear conditioning and extinction: Emotional states encoded by distinct signaling pathways. Trends in Neurosciences 35 (2012), 145–155, 10.1016/j.tins.2011.10.003.
76. Wagner, A.R., Logan, F.A., Haberlandt, K., Price, T., Stimulus selection in animal discrimination learning. Journal of Experimental Psychology 76 (1968), 171–180.
77. Watkins, L.R., Wiertelak, E.P., McGorry, M., Martinez, J., Schwartz, B., Sisk, D., Maier, S.F., Neurocircuitry of conditioned inhibition of analgesia: Effects of amygdala, dorsal raphe, ventral medullary, and spinal cord lesions on antianalgesia in the rat. Behavioral Neuroscience 112 (1998), 360–378.