Concussive brain injury enhances fear learning and excitatory processes in the amygdala

Biological Psychiatry

Volumn 71, Issue 4, 2012, Pages 335-343

  Reger, Maxine L ^a,b   Poulos, Andrew M ^b   Buen, Floyd ^d   Giza, Christopher C ^a,c   Hovda, David A ^a,b   Fanselow, Michael S ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MATTEL CHILDREN S HOSPITAL   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Concussion; fear conditioning; GAD 67; NMDA; PTSD; traumatic brain injury

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; BRAIN CONCUSSION; FEAR; HIPPOCAMPUS; HISTOPATHOLOGY; MALE; MEMORY; NONHUMAN; PRIORITY JOURNAL; RAT; UPREGULATION;

AFFECTIVE SYMPTOMS; AMYGDALA; ANIMALS; BEHAVIOR, ANIMAL; BRAIN CONCUSSION; CONDITIONING (PSYCHOLOGY); FEAR; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; HIPPOCAMPUS; HUMANS; ISOENZYMES; MEMORY; MODELS, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RISK FACTORS; STRESS DISORDERS, POST-TRAUMATIC; SYNAPTIC TRANSMISSION;

EID: 84855989559     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2011.11.007     Document Type: Article

References (57)

1. Centers for Disease Control and Prevention, National Center for Injury Prevention and Control Traumatic brain injury http://www.cdc.gov/ncipc/tbi/TBI. htm Accessed October 13, 2011
2. RAND Corporation, Center for Military Health Policy Research Invisible Wounds of War: Psychological and Cognitive Injuries, Their Consequences, and Services to Assist Recovery MG-720-CCF http://www.rand.org/pubs/monographs/ MG720/ 2008 Accessed October 13, 2011
3. E.L. Moore, L. Terryberry-Spohr, D.A. Hope Mild traumatic brain injury and anxiety sequelae: A review of literature Brain Inj 2 2006 117 132 (Pubitemid 43158174)
4. H.J. Thompson, J. Lifshitz, N. Marklund, M.S. Grady, D.I. Graham, D.A. Hovda, T.K. McIntosh Lateral fluid percussion brain injury: A 15-year review and evaluation J Neurotrauma 27 2005 42 75
5. C.C. Giza, D.A. Hovda The neurometabolic cascade of concussion J Athl Train 36 2001 228 235 (Pubitemid 33685230)
6. V. Rau, J.P. DeCola, M.S. Fanselow Stress-induced enhancement of fear learning: An animal of posttraumatic stress disorder Neurosci Biobehav Rev 29 2005 1207 1223 (Pubitemid 41446896)
7. R. Stam PTSD and stress sensitization: A tale of brain and body Part 2: Animal models Neurosci Biobehav Rev 31 2007 558 584 (Pubitemid 46527884)
8. M. Fendt, M.S. Fanselow The neuroanatomical and neurochemical basis of conditioned fear Neurosci Biobehav Rev 23 1999 743 760 (Pubitemid 29282023)
9. D.A. Hovda, A. Yoshino, T. Kawamata, Y. Katayama, D.P. Becker Diffuse prolonged depression of cerebral oxidative metabolism following concussive brain injury in the rat: A cytochrome oxidase histochemistry study Brain Res 567 1991 1 10
10. M.L. Prins, D.A. Hovda Mapping cerebral glucose metabolism during spatial learning: Interaction of development and traumatic brain injury J Neurotrauma 18 2001 31 46 (Pubitemid 32055454)
11. M.J. Miserendino, C.B. Sananes, K.R. Melia, M. Davis Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala Nature 345 1990 716 718
12. M.S. Fanselow, J.J. Kim Acquisition of contextual Pavlovian fear conditioning is blocked by application of an NMDA receptor antagonist D, L-2-amino-5-phosphonovaleric acid to basolateral amygdala Behav Neurosci 108 1994 210 212 (Pubitemid 24097761)
13. J.J. Kim, M.S. Fanselow Modality-specific retrograde amnesia of fear Science 256 1992 675 677
14. S.M. Rodrigues, G.E. Schafe, J.E. LeDoux Intra-amygdala blockade of the NR2B subunit of the NMDA receptor disrupts the acquisition but not the expression of fear conditioning J Neurosci 21 2001 6889 6896 (Pubitemid 32781131)
15. I. Ehrlich, Y. Humeau, F. Grenier, S. Ciocchi, C. Herry, A. Lthi Amygdala inhibitory circuits and the control of fear memory Neuron 62 2009 757 771
16. S.R. Makkar, Q.Z. Shirley, J. Cranney Behavioral and neural analysis of GABA in the acquisition, consolidation, reconsolidation, and extinction of fear memory Neuropsychopharmacology 35 2010 1625 1652
17. S. Cull-Candy, S. Brickley, M. Farrant NMDA receptor subunits: Diversity, development and disease Curr Opin Neurobiol 11 2001 327 335 (Pubitemid 32524098)
18. R.M. Shin, E. Tsvetkov, V.Y. Bolshakov Spatiotemporal asymmetry of associative synaptic plasticity in fear conditioning pathways Neuron 52 2006 883 896 (Pubitemid 44828443)
19. D.L. Walker, M. Davis Amygdala infusions of an NR2B-selective of an NR2A-preferring NMDA receptor antagonist differentially influence fear conditioning and expression in the fear-potentiated startle test Learn Mem 15 2008 67 74 (Pubitemid 351281568)
20. B.J. Wiltgen, B.P. Godsil, Z. Peng, F. Saab, H.L. June, M.L. Linn The alpha1 subunit of the GABA(A) receptor modulates fear learning and plasticity in the lateral amygdala Front Behav Neurosci 3 2009 37
21. F. Crestani, M. Lorez, K. Baer, C. Essrich, D. Benke, J.P. Laurent Decreased GABAA-receptor clustering results in enhanced anxiety and a bias for threat cues Nat Neurosci 2 1999 833 839 (Pubitemid 30491177)
22. R.M. Mihalek, P.K. Banerjee, E.R. Korpi, J.J. Quinlan, L.L. Firestone, Z.P. Mi Attenuated sensitivity to neuroactive steroids in γ-aminobutyrate type A receptor δ subunit knockout mice Proc Natl Acad Sci U S A 96 1999 12905 12910 (Pubitemid 29513601)
23. F. Crestani, R. Keist, J.M. Fritsch, D. Benke, K. Vogt, L. Prut Trace fear conditioning involves hippocampal α5 GABAA Proc Natl Acad Sci U S A 99 2002 8980 8985
24. B.J. Wiltgen, M.J. Sanders, C. Ferguson, G.E. Homanics, M.S. Fanselow Trace fear conditioning in enhanced in mice lacking δ subunit of the GABAA receptor Learn Mem 12 2005 327 333 (Pubitemid 40958344)
25. L.P. Miller, B.G. Lyeth, L.W. Jenkins, L. Oleniak, D. Panchision, R.J. Hamm Excitatory amino acid receptor subtype binding following traumatic brain injury Brain Res 526 1990 103 107 (Pubitemid 20273567)
26. V. Santhakumar, A.D. Razliff, J. Jeng, Z. Toth, I. Soltesz Long-term hyperexcitability in the hippocampus after experimental head trauma Ann Neurol 50 2001 708 717 (Pubitemid 33116130)
27. A. Kumar, L. Zou, X. Yuan, Y. Long, K. Yang N-methyl-D-aspartate receptors: Transient loss of NR1/NR2A/NR2B subunits after traumatic brain injury in a rodent model J Neurosci Res 67 2002 781 786 (Pubitemid 34226290)
28. C.L. Osteen, C.C. Giza, D.A. Hovda Injury-induced alterations in N-methyl-D-aspartate receptor subunit composition contribute to prolonged 45calcium accumulation following lateral fluid percussion Neuroscience 125 2004 305 322 (Pubitemid 39200478)
29. G. Liu Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites Nat Neurosci 7 2004 373 379 (Pubitemid 38429177)
30. B.M. Witgen, J. Lifshitz, M.L. Smith, E. Schwarzbach, S.-L. Liang, M.S. Grady, A.S. Cohen Regional hippcampal alteration associated with cognitive deficit following experimental brain injury: A systems, network and cellular evaluation Neuroscience 133 2005 1 15 (Pubitemid 40694154)
31. I. Fineman, C.C. Giza, B.V. Nahed, S.M. Lee, D.A. Hovda Inhibition of neocortical plasticity during development by a moderate concussive brain injury J Neurotrauma 17 2000 739 749
32. R. Raghupahti, T.K. McIntosh Regionally and temporally distinct patterns of induction of c-fos, c-jun, and junB mRNSs following experimental brain injury in the rat Brain Res Mol Brain Res 37 1996 134 144 (Pubitemid 26147983)
33. J.-J. Soghomonian, D.L. Martin Two isoforms of glutamate decarboxylase: Why? Trends Pharmacol Sci 19 1998 500 505 (Pubitemid 29008539)
34. C.C. Giza, N.S. Maria, D.A. Hovda N-methyl-D-aspartate receptor subunit changes after traumatic injury to the developing brain J Neurotrauma 23 2006 950 961 (Pubitemid 43962854)
35. J.E. Kennedy, M.S. Jaffee, G.A. Leskin, J.W. Stokes, F.O. Leal, P.J. Fitzpatrick Posttraumatic stress disorder and posttraumatic stress disorder-like symptoms and mild traumatic brain injury J Rehabil Res Dev 44 2007 895 920
36. C.W. Hoge, D. McGurk, J.L. Thomas, A.L. Cox, C.C. Engel, C.A. Castro Mild traumatic brain injury in U.S. soldiers returning from Iraq N Engl J Med 358 2008 453 463 (Pubitemid 351185801)
37. R. Sbordone, J. Liter Mild traumatic brain injury does not produce post traumatic stress disorder Brain Inj 9 1995 405 412
38. R. Sbordone, G.D. Seyranina, R.M. Ruff Are the subjective complaints of traumatically brain injured patients reliable? Brain Inj 12 1998 505 515 (Pubitemid 28274147)
39. M. Koenigs, E.D. Huey, V. Raymont, B. Cheon, J. Solomon, E.M. Wasserman, J. Grafman Focal brain damage protects against post-traumatic stress disorder in combat veterans Nat Neurosci 11 2008 232 237 (Pubitemid 351170492)
40. B.P. Godsil, J.R. Spooner, S.G. Anagnostaras, M.S. Fanselow Quantification of the unconditional response to footshock in the rat: Measurement of the activity burst with the use of computer-based image analysis Annual Meeting of the Society for Neuroscience; October 25-30; New Orleans, La 1997 Abstract 23, 1612
41. E. Foa, J. Huppert, S. Cahill Emotional processing theory: An update B. Rothbaum, Pathological Anxiety: Emotional Processing in Etiology and Treatment 2006 Guilford Press New York 3 24
42. S.P. Orr, L.J. Metzger, N.B. Lasko, M.L. Macklin, T. Peri, R.K. Pitman De novo conditioning in trauma exposed individuals with and without posttraumatic stress disorder J Abnorm Psychol 109 2000 290 298 (Pubitemid 30616926)
43. N.S. Jacobs, J.D. Cushman, M.S. Fanselow The accurate measurement of fear memory in Pavlovian conditioning: Resolving the baseline issue J Neurosci Methods 190 2010 235 239
44. B.O. Rothbaum, M.J. Kozak, E.B. Foa, D.J. Whitaker Posttraumatic stress disorder in rape victims: Autonomic habituation to auditory stimuli J Trauma Stress 14 2001 283 293 (Pubitemid 32641694)
45. S. Hogg, P.C. Moser, D.J. Sanger Mild traumatic lesion of the right parietal cortex of the rat: Selective behavioural deficits in the absence of neurological impairment Behav Brain Res 93 1998 143 155 (Pubitemid 28289433)
46. S.T. Fujimoto, L. Longhi, K.E. Saatman, T.K. McIntosh Motor and cognitive function evaluation following experimental traumatic brain injury Neurosci Biobehav Rev 28 2004 365 378 (Pubitemid 39077928)
47. A. Slj, B. Svensson, M. Mayorga, A. Hamberger, H. Bolouri Low-level blasts raise intracranial pressure and impair cognitive function in rats J Neurotrauma 26 2009 1345 1352
48. M.L. Schwarzbold, D. Rial, T. De Bem, D.G. Machado, M.P. Cunha, A.A. dos Santos Effects of traumatic brain injury of different severities on emotional, cognitive, and oxidative stress-related parameters in mice J Neurotrauma 27 2010 1883 1892
49. S. Hogg, P.C. Moser, D.J. Sanger Mild traumatic lesion of the right parietal cortex of the rat: Characterisation of a conditioned freezing deficit and its reversal by dizocilpine Behav Brain Res 93 1998 157 165 (Pubitemid 28289434)
50. S. Hogg, C. Perron, P. Barneoud, D.J. Sanger, P.C. Moser Neuroprotective effect of eliprodil: Attenuation of a conditioned freezing deficit induced by traumatic injury of the right parietal cortex in the rat J Neurotrauma 15 1998 545 553 (Pubitemid 28313412)
51. D.N. Abrous, J. Rodriguez, M. le Moal, P.A. Moser, P. Barneoud Effects of mild traumatic brain injury on immunoreactivity for the inducible transcription factors of c-Fos, c-Jun, JunB, and Krox-24 in cerebral regions associated with conditioned fear responding Brain Res 826 1999 181 192 (Pubitemid 29222932)
52. J. Lifshitz, B.M. Witgen, M.S. Grady Acute cognitive impairment after lateral fluid percussion brain injury recovers by 1 month: Evaluation by conditioned fear response Behav Brain Res 177 2007 347 357 (Pubitemid 46149900)
53. M.S. Fanselow, R.C. Bolles Triggering of the endorphin analgesic reaction by a cue previously associated with shock: Reversal by naloxone Bull Psychon Soc 14 1979 88 90
54. M.I. Cordero, J.J. Merino, C. Sandi Correlational relationship between shock intensity and corticosterone secretion on the establishment and subsequent expression of contextual fear conditioning Behav Neurosci 112 1998 885 891 (Pubitemid 28397370)
55. S. Maren Overtraining does not mitigate contextual fear conditioning deficits produced by neurotoxic lesions of the basolateral amygdala J Neurosci 18 1998 3088 3097 (Pubitemid 28163238)
56. G.D. Gale, S.G. Anagnostaras, B.P. Godsil, S. Mitchell, T. Nozawa, J.R. Sage Role of the basolateral amygdala in the storage of far memories across the adult lifetime of rats J Neurosci 24 2004 3810 3815 (Pubitemid 38509411)
57. J.K. Kim, M.W. Jung Neural circuits and mechanisms involved in Pavlovian fear conditioning: A critical review Neurosci Biobehav Rev 30 2006 188 202 (Pubitemid 41821808)