Mild traumatic brain injury in the rat alters neuronal number in the limbic system and increases conditioned fear and anxiety-like behaviors

Experimental Neurology

Volumn 235, Issue 2, 2012, Pages 574-587

  Meyer, Danielle L ^a   Davies, Daniel R ^a   Barr, Jeffrey L ^a,b   Manzerra, Pasquale ^a   Forster, Gina L ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Amygdala; Anxiety; Apoptosis; Concussive injury; Hippocampus; Mild traumatic brain injury; Posttraumatic stress disorder

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANXIETY; APOPTOSIS; ARTICLE; BREATHING RATE; CONTROLLED STUDY; COORDINATION; EXPERIMENTAL TEST; FEAR; FOOTSHOCK; HEART RATE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HISTOPATHOLOGY; LIMBIC CORTEX; LIMBIC SYSTEM; LOCOMOTION; MALE; MAZE TEST; MOTOR PERFORMANCE; MUSCLE STRENGTH; NOCICEPTION; NONHUMAN; OXYGEN SATURATION; POSTTRAUMATIC STRESS DISORDER; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; ROTAROD TEST; TAIL WITHDRAWAL TEST; TRAUMATIC BRAIN INJURY;

ANIMALS; ANXIETY; BRAIN INJURIES; CELL COUNT; CONDITIONING (PSYCHOLOGY); FEAR; LIMBIC SYSTEM; MALE; NEURONS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84860376259     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.03.012     Document Type: Article

References (78)

1. Akasu T., Muraoka N., Hasuo H. Hyperexcitability of hippocampal CA1 neurons after fluid percussion injury of the rat cerebral cortex. Neurosci. Lett. 2002, 329:305-308.
2. Anderson C.V., Wood D.M.G., Bigler E.D., Blatter D.D. Lesion volume, injury severity, and thalamic integrity following head injury. J. Neurotrauma 1996, 13:59-65.
3. Armony J.L., Corbo V., Clément M.H., Brunet A. Amygdala response in patients with acute PTSD to masked and unmasked emotional facial expression. Am. J. Psychiatry 2005, 162:1961-1963.
4. Baratz R., Rubovitch V., Frenk H., Pick C.G. The influence of alcohol on behavioral recovery after mTBI in mice. J. Neurotrauma 2009, 27:555-563.
5. Barr J.L., Renner K.J., Forster G.L. Withdrawal from chronic amphetamine produces persistent anxiety-like behavior but temporally-limited reductions in monoamines and neurogenesis in the adult rat dentate gyrus. Neuropharmacology 2010, 59:395-405.
6. Bay E.H., Liberzon I. Early stress response: a vulnerability framework for functional impairment following mild traumatic brain injury. Res. Theory Nurs. Pract. 2009, 23:42-61.
7. Beauchamp M.H., Ditchfield M., et al. Hippocampus, amygdala and global brain changes 10 years after childhood traumatic brain injury. Int. J. Dev. Neurosci. 2011, 29(2):137-143.
8. Belanger H.G., Vanderploeg R.D., Curtiss G., Warden D.L. Recent neuroimaging techniques in mild traumatic brain injury. J. Neuropsychiatry Clin. Neurosci. 2007, 19:5-20.
9. Biebl M., Cooper C.M., Winkler J., Kuhn H.G. Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci. Lett. 2000, 291:17-20.
10. Bonne O., Gilboa A., Louzoun Y., Kempf-Sherf O., Katz M., Fishman Y., Ben-Nahum Z., Krausz Y., Bocher M., Lester H., Chisin R., Lerer B. Cerebral blood flow in chronic symptomatic mild traumatic brain injury. Psychiatry Res. Neuroimaging 2003, 124:141-152.
11. Bremner J.D., Vythilingam M., Vermetter E., Southwick S.M., McGlashan T., Staib L.H., Soufer R., Charney D.S. Neural correlates of declarative memory for emotionally valenced words in women with posttraumatic stress disorder related to early childhood sexual abuse. Biol. Psychiatry 2003, 53:879-889.
12. Bremner J.D., Vermetter E., Vythilingam M., Afzal N., Schmahl C., Elzinga B., Charney D.S. Neural correlates of the classic color and emotional stroop in women with abuse-related posttraumatic stress disorder. Biol. Psychiatry 2004, 55:612-620.
13. Bryant R.A. Disentangling mild traumatic brain injury and stress reaction. N. Engl. J. Med. 2008, 358:525-527.
14. Bryant R.A., Felmingham K., Kemp A., Das P., Hughes G., Peduto A., Williams L. Amygdala and ventral anterior cingulate activation predicts treatment response to cognitive behavior therapy for post-traumatic stress disorder. Psychol. Med. 2008, 38:555-561.
15. Bye N., Carron S., Han X., Agyapomaa D., Ng S.Y., Yan E., Rosenfeld J.V., Morganti-Kossmann M.C. Neurogenesis and glial proliferation are stimulated following diffuse traumatic brain injury in adult rats. J. Neurosci. Res. 2011, 89:986-1000.
16. Clark R.S., Chen J., Watkins S.C., Kochanek P.M., Chen M., Stetler R.A., Loeffert J.E., Graham S.H. Apoptosis-suppressor gene bcl-2 expression after traumatic brain injury in rats. J. Neurosci. 1997, 17:9172-9182.
17. Dash P.K., Mach S.A., Moore A.N. Enhanced neurogenesis in the rodent hippocampus following traumatic brain injury. J. Neurosci. Res. 2001, 63:313-319.
18. Ehninger D., Kempermann G. Neurogenesis in the adult hippocaomus. Cell and Tissue Res. 2008, 331:243-250.
19. Emery D.L., Fulp C.T., Saatman K.E., Schutz C., Neugebauer E., McIntosh T.K. Newly born granule cells in the dentate gyrus rapidly extend axons into the hippocampal CA3 region following experimental brain injury. Journal of Neurotrauma 2005, 22:978-988.
20. Etkin A., Prater K.E., Schatzberg A.F., Menon V., Greicius M.D. Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. Arch. Gen. Psychiatry 2009, 66:1361-1372.
21. Fanselow M.S., LeDoux J.E. Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neurons 1999, 23:229-232.
22. Feng N., Telefont M., Kelly K.J., Orchinik M., Forster G.L., Renner K.J., Lowry C.A. Local perfusion of corticosterone in the rat medial hypothalamus potentiates d-fenfluramine-induced elevations of extracellular 5-HT concentrations. Horm. Behav. 2009, 56:149-157.
23. Forster G.L., Feng N., Watt M.J., Korzan W.J., Mouw N.J., Summers C.H., Renner K.J. Cotricotropin-releasing factor in the dorsal raphe elicits temporally distinct serotonergic responses in the limbic system in relation to fear behavior. Neuroscience 2006, 141:1047-1055.
24. Fujiki M., Kubo T., Kamida T., Sugita K., Hikawa T., Abe T., Ishii K., Kobayashi H. Neuroprotective and antiamnesic effect of donepezil, nicotinic acetylcholine-receptor activator, on rats with concussive mild traumatic brain injury. J. Clin. Neurosci. 2008, 15:791-796.
25. Gaylord K.M., Cooper D.B., Mercado J.M., Kennedy J.E., Yoder L.H., Holcomb J.B. Traumatic brain injury in burned service members: preliminary report. J. Trauma 2008, 64:S200-S206.
26. Goosens K.A., Maren S. Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learn. Mem. 2001, 8:148-155.
27. Grillon C. Startle reactivity and anxiety disorders; aversive conditioning, context, and neurobiology. Biol. Psychiatry 2002, 52:958-975.
28. Grillon C., Morgan C.A. Fear-potentiated startle conditioning to explicit and contextual cues in Gulf War veterans with posttraumatic stress disorder. J. Abnorm. Psychol. 1999, 180:134-142.
29. Helmstetter F.J., Parsons R.G., Gafford G.M. Macromolecular synthesis, distributed synaptic plasticity, and fear conditioning. Neurobiol. Learn. Mem. 2008, 89:324-337.
30. Henninger N., Dützmann S., Sicard K.M., Kollmar R., Bardutzky J., Schwab S. Impaired spatial learning in a novel rat model of mild cerebral concussion injury. Exp. Neurol. 2005, 195:447-457.
31. Henninger N., Sicard K.M., Li X., Kulkarni P., Dützmann S., Urbanek C., Schwab S., Fisher M. Differential recovery of behavioral status and brain function assessed with functional magnetic resonance imaging after mild traumatic brain injury in the rat. Crit. Care Med. 2007, 35:2607-2614.
32. Herman J.P., Ostrander M.M., Mueller N.K., Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29:1201-1213.
33. Hoge C.W., McGurk D., Thomas J.L., Cox A.L., Engel C.C., Castro C.A. Mild traumatic brain injury in U.S. soldiers returning from Iraq. N. Engl. J. Med. 2008, 358:453-463.
34. Hopper J.W., Frewen P.A., van der Kolk B.A., Lanius R.A. Neural correlates of re-experiencing, avoidance and dissociation in PTSD: symptoms dimensions and emotion dysregulation in responses to script-driven trauma imagery. J. Trauma. Stress 2007, 20:713-725.
35. Hunsaker M.R., Kesner R.P. Dissociation across the dorsal-ventral axis of CA3 and CA1 for encoding and retrieval of contextual and auditory-cued fear. Neurobiol. Learn. Mem. 2008, 89:61-69.
36. Kennedy J.E., Jaffee M.S., Leskin G.A., Stokes J.W., Leal F.O., Fitzpatrick P.J. Posttraumatic stress disorder and posstraumatic stress disorder-like symptoms and mild traumatic brain injury. J. Rehabil. Res. Dev. 2007, 44:895-920.
37. Kreisman N.R., Soliman S., Gozal D. Regional differences in hypoxic depolarization and swelling in hippocampal slices. J. Neurophysiol. 2000, 83:1031-1038.
38. Kwon S.-K.C., Kovesdi E., Gyorgy A.B., Wingo D., Kamnaksh A., Walker J., Long J.B., Agoston D.V. Stress and traumatic brain injury; a behavioral, proteomics and histological study. Front. Neurol. 2011, 2:1-13.
39. Lewine J.D., Davis J.T., Bigler E.D., Thoma R., Hill D., Funke M., Sloan J.H., Hall S., Orrison W.W. Objective documentation of traumatic brain injury subsequent to mild head trauma: mulitmodal brain imaging with MEG, SPECT, and MRI. J. Head Trauma Rehabil. 2007, 22:141-155.
40. Liberzon I., Taylor S.F., Amdur R., Jung T.D., Chamberlain K.R., Minoshima S., Koeppe R.A., Fig L.M. Brain activation in PTSD in response to trauma-related stimuli. Biol. Psychiatry 1999, 45:817-826.
41. Lukkes J.L., Mokin M.V., Scholl J.L., Forster G.L. Adult rats exposed to early-life social isolation exhibit increased anxiety and conditioned fear behavior, and altered hormonal stress responses. Horm. Behav. 2009, 55:248-256.
42. Madathil S.K., Evans H.N., Saatman K.E. Temporal and regional changes in IGF-1/IGF-1R signaling in the mouse brain after traumatic brain injury. J. Neurotrauma 2010, 27:95-107.
43. 2 receptor. Br. J. Pharmacol. 2009, 156:1326-1341.
44. McNaughton N., Corr P.J. A two-dimentional neuropsychology of defense: fear/anxiety and defensive distance. Neurosci. Biobehav. Rev. 2004, 28:285-305.
45. Milad M.R., Rauch S.L., Pitman R.K., Quirk G.J. Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol. Psychol. 2006, 73:61-71.
46. Milad M.R., Orr S.P., Lasko N.B., Chang Y., Rauch S.L., Pitman R.K. Presence and acquired origin of reduced recall for fear extinction in PTSD: results of a twin study. J. Psychiatr. Res. 2008, 42:515-520.
47. Moore E.L., Terryberry-Spohr L., Hope D.A. Mild traumatic brain injury and anxiety sequelae: a review of the literature. Brain Inj. 2006, 20:117-132.
48. Morales D.M., Marklund N., Lebold D., Thompson H.J., Pitkanen A., Maxwell W.L., Longhi L., Laurer H., Maegele M., Neugebauer E., Graham D.I., Stocchetti N., McIntosh T.K. Experimental models of traumatic brain injury: do we really need to build a better mousetrap?. Neuroscience 2005, 136:971-989.
49. Mullen R.J., Buck C.R., Smith A.M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 1992, 116:201-211.
50. Noshita N., Lewen A., Sugawara T., Chan P.H. Akt phosphorylation and neuronal survival after traumatic brain injury in mice. Neurobiol. Dis. 2002, 9:294-304.
51. Okuda H., Tatsumi K., et al. Environmental enrichment stimulates progenitor cell proliferation in the amygdala. J. Neurosci. Res. 2009, 87(16):3546-3553.
52. Ooba S., Hasuo H., Shigemori M., Yamashita S., Akasu T. Mild hypothermia prevents post-traumatic hyperactivity of excitatory synapses in rat hippocampal CA1 pyramidal neurons. Kurume Med. J. 2009, 56:49-59.
53. Paxinos C., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, New York. 3rd ed.
54. Ptito A., Chen J.K., Johnston K.M. Contributions of functional magnetic resonance imaging (fMRI) to sport concussion evaluation. NeuroRehabilitation 2007, 22:217-227.
55. Quirk G.J., Likhtik E., Pelletier J.G., Paré D. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J. Neurosci. 2003, 23:8800-8807.
56. Quirk G.J., Garcia R., Gonzalez-Lima F. Prefrontal mechanisms in extinction of conditioned fear. Biol. Psychiatry 2006, 60:337-343.
57. Rauch S.L., Whalen P.J., Shin L.M., McInerney S.C., Macklin M.L., Lasko N.B., Orr S.P., Pitman R.K. Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol. Psychiatry 2000, 47:769-776.
58. Rauch S.L., Shin L.M., Phelps E.A. Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research-past, present, and future. Biol. Psychiatry 2006, 60:376-382.
59. Rubovich V., Edut S., Sarfstein R., Werner H., Pick C.G. The intricate involvement of the insulin-like growth factor receptor signaling in mild traumatic brain injury in mice. Neurobiol. Dis. 2010, 38:299-303.
60. Schienle A., Ebner F., Schäfer A. Localized gray matter volume abnormalities in generalized anxiety disorder. Eur. Arch. Psychiatry Clin. Neurosci. 2011, 261:303-307.
61. Schmidt-Kastner R., Freund T.F. Selective vulnerability of the hippocampus in brain ischemia. Neuroscience 1991, 40:599-636.
62. Shapira M., Licht A., Milman A., Picj C.G., Shohami E., Elder-Finkelman H. Role of glycogen synthase kinase-3B in early depressive behavior induced by mild traumatic brain injury. Mol. Cell. Neurosci. 2007, 34:571-577.
63. Shin L.M., Whalen P.J., Pitman R.K., Bush G., Macklin M.L., Lasko N.B., Orr S.P., McInerney S.C., Rauch S.L. An fMRI study of anterior cingulate function in posttraumatic stress disorder. Biol. Psychiatry 2001, 50:932-942.
64. Shin L.M., Orr S.P., Carson M.A., Rauch S.L., Macklin M.L., Lasko N.B., Peters P.M., Metzger L.J., Daugherty D.D., Cannistraro P.A., Alpert N.M., Fischman A.J., Pitman R.K. Regional cerebral blood flow in the amygdala and medial prefrontal cortex during traumatic imagery in male and female Vietnam veterans with PTSD. Arch. Gen. Psychiatry 2004, 61:168-176.
65. Shin L.M., Wright C.I., Cannistraro P.A., Wedig M.M., McMullin K., Martis B., Macklin M.L., Lasko N.B., Cavanagh S.R., Krangel T.S., Orr S.P., Pitman R.K., Whalen P.J., Rauch S.L. A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Arch. Gen. Psychiatry 2005, 62:273-281.
66. Slomianka L., West M.J. Estimators of the precision of stereological estimates: an example bases on the CA1 pyramidal cell layers of rats. Neuroscience 2005, 136:757-767.
67. Sun D., McGinn M.J., Zhou Z., Harvey H.B., Bullock M.R., Colello R.J. Anatomical integration of newly generated dentate granule neurons following traumatic brain injury in adult rats and its association to cognitive recovery. Exp. Neurol. 2007, 204:264-272.
68. Tang Y.P., Noda Y., Hasegawa T., Nabeshima T. A concussive-like brain injury model in mice (I): impairment in learning and memory. J. Neurotrauma 1997, 14:851-862.
69. Tang Y.P., Noda Y., Hasegawa T., Nabeshima T. A concussive-like brain injury model in mice (II): selective neuronal loss in the cortex and hippocampus. J. Neurotrauma 1997, 14:863-873.
70. Tashlykov V., Katz Y., Gazit V., Zohar O., Schreiber S., Pick C.G. Apoptotic changes in the cortex and hippocampus following minimal brain trauma in mice. Brain Res. 2007, 1130:197-205.
71. Tashlykov V., Katz Y., Volkov A., Gazit V., Schreiber S., Zohar O., Pick C. Minimal traumatic brain injury induce apoptotic cell death in mice. J. Mol. Neurosci. 2009, 37:16-24.
72. Tweedie D., Milman A., Holloway H.W., Li Y., Harvey B.K., Shen H., Pistell P.J., Lahiri D.K., Hoffer B.J., Wang Y., Pick C.G., Greig N.H. Apoptotic and behavioral sequelae of mild brain trauma in mice. J. Neurosci. Res. 2007, 85:805-815.
73. Vuong S.M., Oliver H.A., Scholl J.L., Oliver K.M., Forster G.L. Increased anxiety-like behavior of rats during amphetamine withdrawal is reversed by CRF2 receptor antagonism. Behav. Brain Res. 2010, 208:278-281.
74. Wallesch C.W., Curio N., Galazky I., Jost S., Synowitz H. The neuropsychology of blunt head injury in the early postacute stage: effects of focal lesions and diffuse axonal injury. J. Neurotrauma 2001, 18:11-20.
75. Weber J.T. Experimental models of repetitive brain injuries. Prog. Brain Res. 2007, 161:253-261.
76. West M.J. New stereological methods for counting neurons. Neurobiol. Aging 1993, 14:275-285.
77. Yoshino A., Hovda D.A., Katayama Y., Kawamata T., Becker D.P. Hippocampal CA3 lesion prevents postconcussive metabolic dysfunction in CA1. J. Cereb. Blood Flow Metab. 1996, 12:996-1006.
78. Zhang X., Chen Y., Ikonomovic M.D., Nathanial P.D., Kochanek P.M., Marion D.W., DeKosky S.T., Jenkins L.W., Clark R.S. Increased phosphorylation of protein kinase B and related substrates after traumatic brain injury in humans and rats. J. Cereb. Blood Flow Metab. 2006, 26:915-926.