Abstract
Traumatic brain injury (TBI) has reached epidemic proportions around the world and is a major public health concern in the United States. Approximately 2.8 million individuals sustain a traumatic brain injury and are treated in an Emergency Department yearly in the U.S., and about 50,000 of them die. Persistent symptoms develop in 10–15% of the cases including neuropsychiatric disorders. Anxiety is the second most common neuropsychiatric disorder that develops in those with persistent neuropsychiatric symptoms after TBI. Abnormalities or atrophy in the temporal lobe has been shown in the overwhelming number of TBI cases. The basolateral amygdala (BLA), a temporal lobe structure that consolidates, stores and generates fear and anxiety-based behavioral outputs, is a critical brain region in the anxiety circuitry. In this review, we sought to capture studies that characterized the relationship between human post-traumatic anxiety and structural/functional alterations in the amygdala. We compared the human findings with results obtained with a reproducible mild TBI animal model that demonstrated a direct relationship between the alterations in the BLA and an anxiety-like phenotype. From this analysis, both preliminary insights, and gaps in knowledge, have emerged which may open new directions for the development of rational and more efficacious treatments.
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Almeida-Suhett CP, Prager EM, Pidoplichko V, Figueiredo TH, Marini AM, Li Z, Eiden LE, Braga MFM (2014) Reduced GABAergic inhibition in the basolateral amygdala and the development of anxiety-like behaviors after mild traumatic brain injury. PLoS ONE 9:e102627. https://doi.org/10.1371/journal.pone.0102627
Alway Y, Gould KR, Johnston L, McKenzie D, Ponsford J (2016) A prospective examination of Axis I psychiatric disorders in the first 5 years following moderate to severe traumatic brain injury. Psychol Med 2016:1331–1341. https://doi.org/10.1017/S0033291715002986
American Congress of Rehabilitation Medicine (1993) Definition of mild traumatic brain injury. Head Trauma Rehabil 8(3):86–87
American Psychiatric Association: Diagnostic and Statistical Manual of Mental Disorders, 5th ed. Arlington, VA: American Psychiatric Association, 2013
Anderson CV, Wood DM, Bigler ED, Blatter DD (1996) Lesion volume, injury severity, and thalamic integrity following head injury. J Neurotrauma 13:59–65. https://doi.org/10.1089/neu.1996.13.59
Aroniadou-Anderjaska V, Pidoplichko VI, Figueiredo TH, Almeida-Suhett CP, Prager EM, Braga MF (2012) Presynaptic facilitation of glutamate release in the basolateral amygdala: a mechanism for the anxiogenic and seizurogenic function of GluK1 receptors. Neuroscience 221:157–169. https://doi.org/10.1016/j.neuroscience.2012.07.006
Arun P, Rossetti F, Wilder DM, Sajja S, Van Albert SA, Wang Y, Gist ID, Long JB (2020) Blast exposure leads to accelerated cellular senescence in the rat brain. Front Neurol 11:438. https://doi.org/10.3389/fneur.2020.00438
Ashman TA, Spielman LA, Hibbard MR, Silver JM, Chandna T, Gordon WA (2004) Psychiatric challenges in the first 6 years after traumatic brain injury: cross-sequential analyses of Axis I disorders. Arch Phys Med Rehabil 85(4 Suppl 2):S36-42. https://doi.org/10.1016/j.apmr.2003.08.117
Barazangi N, Role LW (2001) Nicotine-induced enhancement of glutamatergic and GABAergic synaptic transmission in the mouse amygdala. J Neurophysiol 86(1):463–474. https://doi.org/10.1152/jn.2001.86.1.463
Bazarian JJ, McClung J, Shah MN, Cheng YT, Flesher W, Kraus J (2005) Mild traumatic brain injury in the United States, 1998–2000. Brain Inj 19:85–91. https://doi.org/10.1080/02699050410001720158
Beauchamp MH, Ditchfield M, Maller JJ, Catroppa C, Godfrey C, Rosenfeld JV, Kean MJ, Anderson VA (2011a) Hippocampus, amygdala and global brain changes 10 years after childhood traumatic brain injury. Int J Devl Neuroscience 29:137–143. https://doi.org/10.1016/j.ijdevneu.2010.12.003
Beauchamp MH, Ditchfield M, Catroppa C, Kean M, Godfrey C, Rosenfeld JV, Anderson V (2011b) Focal thinning of the posterior corpus callosum: normal variant or post-traumatic? Brain Inj 25:950–957. https://doi.org/10.3109/02699052.2011.589791
Behlke LM, Foster RA, Liu J, Benke D, Benham RS, Nathanson AJ, Yee BK, Zeilhofer HU, Engin E, Rudolph UA (2016) Pharmacogenetic ‘Restriction-of-Function’ approach reveals evidence for anxiolytic-like actions mediated by α5-containing GABAA receptors in mice. Neuropsychopharmacology 41:2492–2501. https://doi.org/10.1038/npp.2016.49
Beitchman JA, Griffiths DR, Hur Y, Ogle SB, Bromberg CE, Morrison HW, Lifshitz J, Adelson PD, Thomas TC (2020) Experimental traumatic brain injury induces chronic glutamatergic dysfunction in amygdala circuitry known to regulate anxiety-like behavior. Front Neurosci 13:1434. https://doi.org/10.3389/fnins.2019.01434
Bell MJ, Kochanek PM (2013) Pediatric traumatic brain injury in 2012, the year with new guidelines and common data elements. Curit Care Clin 29:223–238. https://doi.org/10.1016/j.ccc.2012.11.004
Bigler ED (2001) Quantitative magnetic resonance imaging in traumatic brain injury. J Head Trauma Rehabil 16:117–134. https://doi.org/10.1097/00001199-200104000-00003
Bigler ED, Kurth SM, Blatter D, Abildskov TJ (1992) Degenerative changes in traumatic brain injury: post-injury magnetic resonance identified ventricular expansion compared to pre-injury levels. Brain Res Bull 28:651–653. https://doi.org/10.1016/0361-9230(92)90119-i
Bigler ED, Anderson CV, Blatter DD (2002) Temporal lobe morphology in normal aging and traumatic brain injury. AJNR Am J Neuroradiol 23:255–266
Bogdanov Y, Michels G, Armstrong-Gold C, Haydon PG, Lindstrom J, Pangalos M, Moss SJ (2006) Synaptic GABAA receptors are directly recruited from their extrasynaptic counterparts. EMBO J 25:4381–4389. https://doi.org/10.1038/sj.emboj.7601309
Botta P, Demmou L, Kasugai Y, Markovic M, Xu C, Fadok JP, Lu T, Poe MM, Xu L, Cook JM, Rudolph U, Sah P, Ferraguti F, Lüthi A (2015) Regulating anxiety with extrasynaptic inhibition. Nat Neurosci 18:1493–1500. https://doi.org/10.1038/nn.4102
Braga LW, Souza LN, Najjar YJ, Dellatolas G (2007) Magnetic resonance imaging (MRI) findings and neuropsychological sequelae in children after severe traumatic brain injury: the role of cerebellar lesion. J Child Neurol 22:1084–1089. https://doi.org/10.1177/0883073807306246
Brandon N, Javanovic J, Moss S (2002) Multiple roles of protein kinases in the modulation of γ-aminobutyric acidA receptor function and cell surface expression. Pharmacol Ther 94:113–122. https://doi.org/10.1016/s0163-7258(02)00175-4
Bremner JD, Innis RB, White T, Fujita M, Silbersweig D, Goddard AW, Staib L, Stern E, Cappiello A, Woods S, Baldwin R, Charney DS (2000) SPECT [I-123]iomazenil measurement of the benzodiazepine receptor in panic disorder. Biol Psychiatry 47:96–106. https://doi.org/10.1016/s0006-3223(99)00188-2
Brizuela M, Blizzard CA, Chuckowree JA, Pitman KA, Young KM, Dickson T (2017) Mild traumatic brain injury leads to decreased inhibition and a differential response of calretinin positive interneurons in the injured cortex. J Neurotrauma 34(17):2504–2517. https://doi.org/10.1089/neu.2017.4977
Broussard JI, Acion L, De Jesús-Cortés H, Yin T, Britt JK, Salas R, Costa-Mattioli M, Robertson C, Pieper AA, Arciniegas DB, Jorge R (2018) Repeated mild traumatic brain injury produces neuroinflammation, anxietylike behaviour and impaired spatial memory in mice. Brain Inj 32:113–122. https://doi.org/10.1080/02699052.2017.1380228
Bryant RA (2008) Disentangling mild traumatic brain injury and stress reactions. N Engl J Med 358:525–527. https://doi.org/10.1056/NEJMe078235
Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929. https://doi.org/10.1126/science.1099745
Byrd M, Dixon CE, Lucke-Wold B (2018) Examining the correlation between acute behavioral manifestations of concussion and the underlying pathophysiology of chronic traumatic encephalopathy: a pilot study. J Neurol Psychol. https://doi.org/10.13188/2332-3469.1000037
Carlsen J (1988) Immunocytochemical localization of glutamate decarboxylase in the rat basolateral amygdaloid nucleus, with special reference to GABAergic innervation of amygdalostriatal projection neurons. J Comp Neurol 273:513–526. https://doi.org/10.1002/cne.902730407
Carron SF, Yan EB, Alwis DS, Rajan R (2016) Differential susceptibility of cortical and subcortical inhibitory neurons and astrocytes in the long term following diffuse traumatic brain injury. J Comp Neurol 524(17):3530–3560. https://doi.org/10.1002/cne.24014
Carron SF, Yan EB, Allitt BJ, Rajan R (2018) Immediate and medium-term changes in cortical and hippocampal inhibitory neuronal populations after diffuse TBI. Neuroscience 388:152–170. https://doi.org/10.1016/j.neuroscience.2018.07.020
Carron SF, Sun M, Shultz SR, Rajan R (2020) Inhibitory neuronal changes following a mixed diffuse-focal model of traumatic brain injury. J Comp Neurol 528:175–198. https://doi.org/10.1002/cne.24746
Centers for Disease Control (2008) Department of Defense and Veterans Affairs working group proposal_definition of TBI. Centers for Disease Control, Atlanta
Centers for Disease Control and Prevention (2015) Report to Congress on Traumatic Brain Injury in the United States: Epidemiology and Rehabilitation. National Center for Injury Prevention and Control; Division of Unintentional Injury Prevention. Atlanta, GA
Cernak I, Merkle AC, Koliatsos VE, Bilik JM, Luong QT, Mahota TM, Xu L, Slack N, Windle D, Ahmed FA (2011) The pathobiology of blast injuries and blast-induced neurotrauma as identified using a new experimental model of injury in mice. Neurobiol Dis 41:538–551. https://doi.org/10.1016/j.nbd.2010.10.025
Chiba S, Numakawa T, Ninomiya M, Richards MC, Wakabayashi C, Kunugi H (2012) Chronic restraint stress causes anxiety- and depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Prog NeuropsYchopharmacol Biol Psychiatry 39:112–119. https://doi.org/10.1016/j.pnpbp.2012.05.018
Coughlin JM, Wang Y, Munro CA, Ma S, Yue C, Chen S, Airan R, Kim PK, Adams AV, Garcia C, Higgs C, Sair HI, Sawa A, Smith G, Lyketsos CG, Caffo B, Kassiou M, Guilarte TR, Pomper MG (2015) Neuroinflammation and brain atrophy in former NFL players: an in vivo multimodal imaging pilot study. Neurobiol Dis 74:58–65. https://doi.org/10.1016/j.nbd.2014.10.019
Cowley DS, Ha EH, Roy-Byrne PP (1997) Determinants of pharmacologic treatment failure in panic disorder. J Clin Psychiatry 58:555–561. https://doi.org/10.4088/jcp.v58n1208
D’Hulst C, Kooy RF (2007) The GABA(A) receptor: a novel target for treatment of fragile X? Trends Neurosci 30:425–431. https://doi.org/10.1016/j.tins.2007.06.003
D’Hulst C, Atack JR, Kooy RF (2009) The complexity of the GABAA receptor shapes unique pharmacological profiles. Drug Discovery Today 14:866–875. https://doi.org/10.1016/j.drudis.2009.06.009
Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1–105. https://doi.org/10.1016/s0301-0082(00)00067-8 (PMID: 11369436)
Davis M, Rainnie D, Cassell M (1994) Neurotransmission in the rat amygdala related to fear and anxiety. Trends Neurosci 17:208–214. https://doi.org/10.1016/0166-2236(94)90106-6
Del-Ben CM, Ferreira CA, Sanchez TA, Alves-Neto WC, Guapo VG, de Araujo DB, Graeff FG (2012) Effects of diazepam on BOLD activation during the processing of aversive faces. J Psychopharmacol 26:443–451. https://doi.org/10.1177/0269881110389092
Divljaković J, Milić M, Namjoshi OA, Tiruveedhula VV, Timić T, Cook JM, Savić MM (2013) βCCT, an antagonist selective for α(1)GABA(A) receptors, reverses diazepam withdrawal-induced anxiety in rats. Brain Res Bull 91:1–7. https://doi.org/10.1016/j.brainresbull.2012.10.011
Durant C, Christmas D, Nutt DJ (2009) The pharmacology of anxiety. In: Steckler T (ed) Stein MB. Behavioral Neurobiology of Anxiety and its treatment, Springer, pp 303–330
Ehrlich L, Humeau Y, Grenier F, Cocchi S, Luthi HC (2009) Amygdala inhibitory circuits and the control of fear memory. Neuron 62:757–771. https://doi.org/10.1016/j.neuron.2009.05.026
Elder GA, Dorr NP, De Gasperi R, Gama Sosa MA, Shaughness MC, Maudlin-Jeronimo E, Hall AA, McCarron RM, Ahlers ST (2012) Blast exposure induces post-traumatic stress disorder-related traits in a rat model of mild traumatic brain injury. J Neurotrauma 29:2564–2575. https://doi.org/10.1089/neu.2012.2510
Engin E, Benham RS, Rudolph U (2018) An emerging circuit pharmacology of GABAA receptors. Trends Pharmacol Sci 39:710–732. https://doi.org/10.1016/j.tips.2018.04.003
Faul M, Xu L, Wald MM and Coronado VG (2010) Traumatic brain injury in the United States: Emergency department visits, hospitalizations, and deaths 2002–2006. Atlanta, GA: Centers for Disease Control and Prevention, National Center for Injury Prevention and Control
Figueiredo TH, Qashu F, Apland JP, Aroniadou-Anderjaska V, Souza AP, Braga MF (2011) The GluK1 (GluR5) Kainate/{alpha}-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor antagonist LY293558 reduces soman-induced seizures and neuropathology. J Pharmacol Exp Ther 336:303–312. https://doi.org/10.1124/jpet.110.171835
Figueiredo TH, Harbert CL, Pidoplichko V, Almeida-Suhett CP, Pan H, Rossetti K, Braga MFM, Marini AM (2018) Alpha-linolenic acid treatment reduces the contusion and prevents the development of anxiety-like behavior induced by a mild traumatic brain injury in rats. Mol Neurobiol 55:187–200. https://doi.org/10.1007/s12035-017-0732-y
Fiorentino H, Kuczewski N, Diabira D, Frrand N, Pangalos MN, Porcher C, Gaiarsa JL (2009) GABAB receptor activation triggers BDNF release and promotes the maturation of GABAergic synapses. J Neurosci 29:11650–11661. https://doi.org/10.1523/JNEUROSCI.3587-09.2009
Fisher AC, Rushby JA, McDonald S, Parks N, Figuet O (2015) Neurophysiological correlates of dysregulated emotional arousal in severe traumatic brain injury. Clin Neurophysiol 126:314–324. https://doi.org/10.1016/j.clinph.2014.05.033
Ford JH, Giovanello KS, Guskiewicz KM (2013) Episodic memory in former professional football players with a history of concussion: an event-related functional neuroimaging study. J Neurotrauma 30:1683–1701. https://doi.org/10.1089/neu.2012.2535
Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347–370. https://doi.org/10.1002/(SICI)1098-1063(1996)6:4%3c347::AID-HIPO1%3e3.0.CO;2-I
Fritsch B, Qashu F, Figueiredo TH, Aroniadou-Anderjaska V, Rogawski MA, Braga MF (2009) Pathological alterations in GABAergic interneurons and reduced tonic inhibition in the basolateral amygdala during epileptogenesis. Neuroscience 163:415–429. https://doi.org/10.1016/j.neuroscience.2009.06.034
Fritschy JM, Brünig I (2003) Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol Ther 98:299–323. https://doi.org/10.1016/s0163-7258(03)00037-8
Fritschy JM, Mohler H (1995) GABAA receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359:154–194. https://doi.org/10.1002/cne.903590111
Fromm L, Heath DL, Vink R, Nimmo AJ (2004) Magnesium attenuates post-traumatic depression/anxiety following diffuse traumatic brain injury in rats. J Am Coll Nutr 23:529S-533S. https://doi.org/10.1080/07315724.2004.10719396
Gale SD, Johnson SC, Bigler ED, Blatter DD (1995) Nonspecific white matter degeneration following traumatic brain injury. J Int Neuropsychol Soc 1:17–28. https://doi.org/10.1017/s1355617700000060
Ganong BR, Loomis CR, Hannun YA (1986) Specificity and mechanism of protein kinase C activation by sn-1,2-diacylglycerols. Proc Natl Acad Sci 83:1184–1188. https://doi.org/10.1073/pnas.83.5.1184
Goossens L, Sunaert S, Peeters R, Griez EJ, Schruers KR (2007) Amygdala hyperfunction in phobic fear normalizes after exposure. Biol Psychiatry 62:1119–1125. https://doi.org/10.1016/j.biopsych.2007.04.024
Gould KR, Ponsford JL, Johnston L, Schönberger M (2011) The nature, frequency and course of psychiatric disorders in the first year after traumatic brain injury: a prospective study. Psychol Med 41:2099–2109. https://doi.org/10.1017/S003329171100033X
Gupta A, Wang Y, Markram H (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287:273–278. https://doi.org/10.1126/science.287.5451.273
Hausrat TJ, Muhia M, Gerrow K, Thomas P, Hirdes W, Tsukita S, Heisler FF, Herich L, Dubroqua S, Breiden P, Feldon J, Schwarz JR, Yee BK, Smart TG, Triller A, Kneussel M (2015) Radixin regulates synaptic GABAA receptor density and is essential for reversal learning and short-term memory. Nat Commun 6:6872. https://doi.org/10.1038/ncomms7872
Heilig M (1995) Antisense inhibition of neuropeptide Y (NPY)-Y1 receptor expression blocks the anxiolytic –like action of NPY in amygdala and paradoxically increases feeding. Regul Pept 59:201–205. https://doi.org/10.1016/0167-0115(95)00103-i
Heilig M, McLeod S, Brot M, Heinrichs SC, Menzaghi F, Koob GF, Britton KT (1993) Anxiolytic-like action of neuropeptide Y: mediation by Y1 receptors in amygdala, and dissociation from food intake effects. Neuropsychopharmacology 8:357–363. https://doi.org/10.1038/npp.1993.35
Heldt SA, Ressler KJ (2010) Amygdala-specific reduction of alpha1-GABAA receptors disrupts the anticonvulsant, locomotor and sedative, but not anxiolytic effects of benzodiazepines. J Neurosci 26:7139–7151
Heldt SA, Mou L, Ressler KJ (2012) In vivo knowckdown of GAD67 in the amygdala disrupts fear extinction and the anxiolytic-like effect of diazepam in mice. Transl Psychiatry 2(2):e181. https://doi.org/10.1038/tp.2012.101
Henry-Feugeas MC, Azouvi P, Fontaine A, Denys P, Bussel B, Maaz F, Samson Y, Schouman-Claeys E (2000) MRI analysis of brain atrophy after severe closed-head injury: relation to clinical status. Brain Inj 14:597–604. https://doi.org/10.1080/02699050050043962
Hines RM, Maric HM, Hines DJ, Modgil A, Panzanelli P, Nakamura Y, Nathanson AJ, Cross A, Deeb T, Brandon NJ, Davies P, Fritschy JM, Schindelin H, Moss SJ (2018) Developmental seizures and mortality result from reducing GABAA receptor α2-subunit interaction with collybistin. Nat Commun 9(1):3130. https://doi.org/10.1038/s41467-018-05481-1
Hoffman AN, Paode PR, May HG, Ortiz JB, Kemmou S, Lifshitz J, Conrad CD, Currier Thomas T (2017) Early and persistent dendritic hypertrophy in the basolateral amygdala following experimental diffuse traumatic brain injury. J Neurotrauma 34:213–219. https://doi.org/10.1089/neu.2015.4339
Hoge CW, McGurk D, Thomas JL, Cox AL, Engel CC, Castro CA (2008) Mild traumatic brain injury in U.S. Soldiers returning from Iraq. N Engl J Med 358:453–463. https://doi.org/10.1056/NEJMoa072972
Holzschneider K, Mulert C (2011) Neuroimaging in anxiety disorders. Dialogues Clin Neurosci 13:453–461. https://doi.org/10.31887/DCNS.2011.13.4/kholzschneider
Janak PH, Tye KM (2015) From circuits to behavior in the amygdala. Nature 517:284–292. https://doi.org/10.1038/nature14188
Jarrahi A, Braun M, Ahluwalia M, Gupta RV, Wilson M, Munie S, Ahluwalia P, Vender JR, Vale FL, Dhandapani KM, Vaibhav K (2020) Revisiting traumatic brain injury: from molecular mechanisms to therapeutic interventions. Biomedicines 8:389. https://doi.org/10.3390/biomedicines8100389
Je HS, Yang F, Ji Y, Nagappan G, Hempstead BL, Lu B (2012) Role of pro-brain-derived neurotrophic factor (proBDNF) to mature BDNF conversion in activity-dependent competition at developing neuromuscular synapses. Proc Natl Acad Sci U S A 109:15924–15929. https://doi.org/10.1073/pnas.1207767109
Jiang X, Tian F, Mearow K, Okagaki P, Lipsky RH, Marini AM (2005) The excitoprotective effect of N-methyl-D-aspartate receptors is mediated by a brain-derived neurotrophic factor autocrine loop in cultured hippocampal neurons. J Neurochem 94:713–722. https://doi.org/10.1111/j.1471-4159.2005.03200.x
Juranek J, Johnson CP, Prasad MR, Kramer LA, Saunders A, Filipek PA, Swank PR, Cox CS Jr, Ewing-Cobbs L (2012) Mean diffusivity in the amygdala correlates with anxiety in pediatric TBI. Brain Imaging Behav 6:36–48. https://doi.org/10.1007/s11682-011-9140-5
Jüttner R, Meier J, Grantyn R (2001) Slow IPSC kinetics, low levels of α1 subunit expression and paired-pulse depression are distinct properties of neonatal inhibitory GABAergic synaptic connections in the mouse superior colliculus. Eur J Neurosci 13:2088–2098. https://doi.org/10.1046/j.0953-816x.2001.01587.x
Kaplan DR, Miller FD (2000) Neurotrophin signal transduction in the nervous system. Curr Opinion Neurobiol 10:381–391. https://doi.org/10.1016/s0959-4388(00)00092-1
Kaufmann WA, Humpel C, Alheid GF, Marksteiner J (2003) Compartmentation of alpha 1 and alpha 2 GABA(A) receptor subunits within rat extended amygdala: implications for benzodiazepine action. Brain Res 964:91–99. https://doi.org/10.1016/s0006-8993(02)04082-9
Keightley MI, Sinopoli KJ, Davis KD, Mikulis DJ, Wennberg R, Tartaglia MC, Chen J-K, Tator CH (2014) Is there evidence for neurodegenerative change following traumatic brain injury in children and youth? A scoping review. Front Hum Neurosci 8:139. https://doi.org/10.3389/fnhum.2014.00139
Kennedy JE, Jaffee MS, Leskin GA, Stokes JW, Leal FO, Fitzpatrick PJ (2007) Posttraumatic stress disorder and posttraumatic stress disorder-like symptoms and mild traumatic brain injury. J Rehabil Res Dev 44:895–920. https://doi.org/10.1682/jrrd.2006.12.0166
Kittler JT, Chen G, Honing S, Bogdanov Y, McAinsh K, Arancibia-Carcamo IL, Jovanovic JN, Pangalos MN, Haucke V, Yan Z, Moss SJ (2005) Phospho-dependent binding of the clathrin AP2 adaptor complex to GABAA receptors regulates the efficacy of inhibitory synaptic transmission. Proc Natl Acad Sci U S A 102:14871–14876. https://doi.org/10.1073/pnas.0506653102
Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321:53–57. https://doi.org/10.1126/science.1149381
Klein RC, Yakel JL (2006) Functional somato-dendritic alpha7-containing nicotinic acetylcholine receptors in the rat basolateral amygdala complex. J Physiol 576:865–872. https://doi.org/10.1113/jphysiol.2006.118232
Koenigs M, Grafman J (2009) Posttraumatic stress disorder: the role of medial prefrontal cortex and amygdala. Neuroscientist 15:540–548. https://doi.org/10.1177/1073858409333072
Kosari-Nasab M, Shokouhi G, Ghorbanihaghjo A, Abbasi MM, Salari AA (2018) Anxiolytic- and antidepressant-like effects of Silymarin compared to diazepam and fluoxetine in a mouse model of mild traumatic brain injury. Toxicol Appl Pharmacol 338:159–173. https://doi.org/10.1016/j.taap.2017.11.012
Kristman VL, Borg J, Godbolt AK, Salmi LR, Cancelliere C, Carroll LJ, Holm LW, Nygren-de Boussard C, Hartvigsen J, Abara U, Donovan J, Cassidy JD (2014) Methodological issues and research recommendations for prognosis after mild traumatic brain injury: results of the International Collaboration on Mild Traumatic Brain Injury Prognosis. Arch Phys Med Rehabil 95:S265–S277. https://doi.org/10.1016/j.apmr.2013.04.026
Lanteaume L, Khalfa S, Regis J, Marquis P, Chauvel P, Bartolomei F (2007) Emotion induction after direct intracerebral stimulatios of human amygdala. Cereb Cortex 17:1307–1313. https://doi.org/10.1093/cercor/bhl041
Lawrence TP, Steel A, Ezra M, Speirs M, Pretorius PM, Douaud G, Sotiropoulos S, Cadoux-Hudson T, Emir U, Voets NL (2019) MRS and DTI evidence of progressive posterior cingulate cortex and corpus callosum injury in the hyper-acute phase after Traumatic Brain Injury. Brain Inj 33:854–868. https://doi.org/10.1080/02699052.2019.1584332
Ledig C, Kamnitsas K, Koikkalainen J, Posti JP, Takala RSK, Katila A, Frantzén J, Ala-Seppälä H, Kyllönen A, Maanpää H-R, Tallus J, Lötjönen J, Glocker B, Tenovuo O, Rueckert D (2017) Regional brain morphometry in patients with traumatic brain injury based on acute- and chronic-phase magnetic resonance imaging. PLoS ONE 12(11):e0188152. https://doi.org/10.1371/journal.pone.0188152
Lee JJ, Segar DJ, Morrison JF, Mangham WM, Lee S, Asaad WF (2018) Subdural hematoma as a major determinant of short-term outcomes in traumatic brain injury. J Neurosurg 128:236–249. https://doi.org/10.3171/2016.5.JNS16255
Leigh R, Oishi K, Hsu J, Lindquist M, Gottesman RF, Jarso S, Crainiceanu C, Mori S, Hillis AE (2013) Acute lesions that impair affective empathy. Brain 136:2539–2549. https://doi.org/10.1093/brain/awt177
Levin HS, Meyers CA, Grossman RG, Sarwar M (1981) Ventricular enlargement after closed head injury. Arch Neurol 38:623–629. https://doi.org/10.1001/archneur.1981.00510100051007
Levin HS, Benavidez D, Verger-Maestre K, Perachio N, Song J, Mendelsohn DR, Fletcher JM (2000) Reduction of corpus callosum growth after severe traumatic brain injury in children. Neurology 54:647–653. https://doi.org/10.1212/wnl.54.3.647
Levine B, Kovacevic N, Nica EI, Cheung G, Gao F, Schwartz ML, Black SE (2008) The Toronto traumatic brain injury study: injury severity and quantified MRI. Neurology 70:771–778. https://doi.org/10.1212/01.wnl.0000304108.32283.aa
Liberzon SF, Taylor R, Amdur TD, Jung KR, Chamberlain SM, Koeppe RA, Fig LM (1999) Brain activation in PTSD in response to trauma-related stimuli. Biol Psychiatry 45:817–826. https://doi.org/10.1016/s0006-3223(98)00246-7
Loane DJ, Faden AI (2010) Neuroprotection for traumatic brain injury: translational challenges and emerging therapeutic strategies. Trends Pharmacol Sci 31:596–604. https://doi.org/10.1016/j.tips.2010.09.005
Loane DJ, Stoica BA, Faden AI (2012) Metabotropic glutamate receptor-mediated signaling in neuroglia. Wiley Interdisciplinary Reviews Membr Transp Signal 1:136–150. https://doi.org/10.1002/wmts.30
Long JB, Bentley TL, Wessner KA, Cerone C, Sweeney S, Bauman RA (2009) Blast overpressure in rats: recreating a battlefield injury in the laboratory. J Neurotrauma 26(6):827–840. https://doi.org/10.1089/neu.2008.0748
Löw K, Crestani F, Keist R, Benke D, Brünig I, Benson JA, Fritschy JM, Rülicke T, Bluethmann H, Möhler H, Rudolph U (2000) Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290(5489):131–134. https://doi.org/10.1126/science.290.5489.131
Lydiard RB (2003) The role of GABA in anxiety disorders. J Clin Psychiatry 64(suppl 3):21–27
Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory systems. Nat Rev Neurosci 5:793–807. https://doi.org/10.1038/nrn1519
Marowsky A, Rudolph U, Fritschy JM, Arand M (2012) Tonic inhibition in principal cells of the amygdala: a central role for α3 subunit-containing GABAA receptors. J Neurosci 32:8611–8619. https://doi.org/10.1523/JNEUROSCI.4404-11.2012
Martina M, Schultz JH, Ehmke H, Monyer H, Jonas P (1998) Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. J Neurosci 18:1811–1825. https://doi.org/10.1523/JNEUROSCI.18-20-08111.1998
Matthews SC, Strigo IA, Simmons AN, O’Connell RM, Reinhardt LE, Moseley SA (2011) A multimodal imaging study in U.S. veterans of Operations Iraqi and Enduring Freedom with and without major depression after blast-related concussion. Neuroimage 54(Suppl 1):S69-75. https://doi.org/10.1016/j.neuroimage.2010.04.269
Max J, Keatley E, Wilde EA, Bigler ED, Levin HS, Schachar RJ, Saunders A, Ewing-Cobbs L, Chapman SB, Dennis M, Yang TT (2011) Anxiety disorders in children and adolescents in the first six months after traumatic brain injury. J Neuropsychiatry Clin Neurosci 23:29–39. https://doi.org/10.1176/jnp.23.1.jnp29
Mayer AR, Hanlon FM, Ling JM (2015) Gray matter abnormalities in pediatric mild traumatic brain injury. J Neurotrauma 32:723–730. https://doi.org/10.1089/neu.2014.3534
McBain CJ, Fisahn A (2001) Interneurons unbound. Nat Rev Neurosci 2:11–23. https://doi.org/10.1038/35049047
McCorkle TA, Barson JR, Raghupathi R (2021) A role for the amygdala in impairments of affective behaviors following mild traumatic brain injury. Front Behav Neurosci 15:601275. https://doi.org/10.3389/fnbeh.2021.601275
McDonald BJ, Amato A, Connolly CN, Benke D, Moss SJ, Smart TG (1998) Adjacent phosphorylation sites on GABAA receptor β subunits determine regulation by cAMP-dependent protein kinase. Nat Neurosci 1:23–28. https://doi.org/10.1038/223
McDonald S, Dalton KI, Rushby JA, Landin-Romero R (2019) Loss of white matter connections after severe traumatic brain injury (TBI) and its relationship to social cognition. Brain Imaging Behav 13:819–829. https://doi.org/10.1007/s11682-018-9906-0
McKee AC, Daneshvar DH (2015) The neuropathology of traumatic brain injury. Handb Clin Neurol 127:45–66. https://doi.org/10.1016/B978-0-444-52892-6.00004-0
McKee AC, Cantu RC, Nowinski CJ, Hedley-Whyte ET, Gavett BE, Budson AE, Santini VE, Lee H-S, Kubilus CA, Stern RA (2009) Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 68:709–735. https://doi.org/10.1097/NEN.0b013e3181a9d503
Meis S, Endres T, Lessmann V (2012) Postsynaptic BDNF signaling regulates long-term potentiation at thalamo-amygdala afferents. J Physiol 590:193–208. https://doi.org/10.1113/jphysiol.2011.220434
Mele M, Leal G, Duarte CB (2016) Role of GABAA R trafficking in the plasticity of inhibitory synapses. J Neurochem 139:997–1018. https://doi.org/10.1111/jnc.13742
Metha MR, Lee AK, Wilson MA (2002) Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417:741–746. https://doi.org/10.1038/nature00807
Meyer DL, Davies DR, Barr JL, Manzerra P, Forster GL (2012) Mild traumatic brain injury in the rat alters neuronal number in the limbic system and increases conditioned fear and anxiety-like behaviors. Exp Neurol 235:574–587. https://doi.org/10.1016/j.expneurol.2012.03.012
Miller H (1966) Mental after-effects of head injury. Proc R Soc Med 59:257–261
Miller PS, Aricescu AR (2014) Crystal structure of a human GABAA receptor. Nature 512(7514):270–275. https://doi.org/10.1038/nature13293
Mody I, Pearce RA (2004) Diversity of inhibitory neurotransmission through GABA(A) and glycine receptors. Trends Neurosci 27:569–575. https://doi.org/10.1016/j.tins.2004.07.002
Möhler H (2006) GABA(A) receptor diversity and pharmacology. Cell Tissue Res 326:505–516. https://doi.org/10.1007/s00441-006-0284-3
Möhler H (2007) Molecular regulation of cognitive functions and developmental plasticity: impact of GABAA receptors. J Neurochem 102:1–12. https://doi.org/10.1111/j.1471-4159.2007.04454.x
Molosh AI, Sajdyk TJ, Truitt WA, Zhu W, Oxford GS, Shekhar A (2013) NPY Y1 receptors differentially modulate GABAA and NMDA receptors via divergent signal transduction pathways to reduce excitability in amygdala neurons. Neuropsychopharmacology 38:1352–1364. https://doi.org/10.1038/npp.2013.33
Murugan M, Ling EA, Kaur C (2013) Glutamate receptors in microglia. CNS Neurol Disord Drug Targets 12:773–784. https://doi.org/10.2174/18715273113126660174
Nakamura Y, Morrow DH, Nathanson AJ, Henley JM, Wilkinson KA, Moss SJ (2020) Phosphorylation on Ser-359 of the α2 subunit in GABA type A receptors down-regulates their density at inhibitory synapses. J Biol Chem 295:12330–12342. https://doi.org/10.1074/jbc.RA120.014303
Ng K, Mikulis DJ, Glazer J, Kabani N, Till C, Greenberg G, Thompson A, Lazinski D, Agid R, Colella B, Green RE (2008) Magnetic resonance imaging evidence of progression of subacute brain atrophy in moderate to severe traumatic brain injury. Arch Phys Med Rehabil 89:S35–S44. https://doi.org/10.1016/j.apmr.2008.07.006
Numakawa T, Kumamaru E, Adachi N, Yagasaki Y, Izumi A, Kunugi H (2009) Glucocorticoid receptor interaction with TrkB promotes BDNF-triggered PLC-gamma signaling for glutamate release via a glutamate transporter. Proc Natl Acad Sci USA 106:647–652. https://doi.org/10.1073/pnas.0800888106
Nuss P (2015) Anxiety disorders and GABA neurotransmission: a disturbance of modulation. Neuropsychiatr Dis Treat 11:165–175. https://doi.org/10.2147/NDT.S58841
Nwokafor C, Serova LI, Nahvi RJ, McCloskey J, Sabban EL (2020) Activation of NPY receptor subtype 1 by [D-His26]NPY is sufficient to prevent development of anxiety and depressive like effects in the single prolonged stress rodent model of PTSD. Neuropeptides 80:102001. https://doi.org/10.1016/j.npep.2019.102001
Pal B (2018) Involvement of extrasynaptic glutamate in physiological and pathophysiological changes of neuronal excitability. Cell Mol Life Sci 75:2917–2949. https://doi.org/10.1007/s00018-018-2837-5
Pandey DK, Yadav SK, Mahesh R, Rajkumar R (2009) Depression-like and anxiety-like behavioural aftermaths of impact accelerated traumatic brain injury in rats: a model of comorbid depression and anxiety? Behav Brain Res 205:436–442
Pandya AA, Yakel JL (2013) Effects of neuronal nicotinic acetylcholine receptor allosteric modulators in animal behavior studies. Biochem Pharmacol 86(8):1054–1062. https://doi.org/10.1016/j.bcp.2013.05.018
Papasergi-Scott MM, Robertson MJ, Seven AB, Panova O, Mathiesen JM, Skiniotis G (2020) Structures of metabotropic GABAB receptor. Nature 584:310–314. https://doi.org/10.1038/s41586-020-2469-4
Paulus MP, Feinstein JS, Castillo G, Simmons AN, Stein MB (2005) Dose-dependent decrease of activation in bilateral amygdala and insula by lorazepam during emotion processing. Arch Gen Psychiatry 62:282–288. https://doi.org/10.1001/archpsyc.62.3.282
Perez-Garcia G et al (2018) PTSD-related behavioral traits in a rat model of blast-induced mTBI are reversed by the mGluR2/3 receptor antagonist BCI-838. eNeuro. https://doi.org/10.1523/ENEURO.0357-17.2018
Phan KL, Fitzgerald DA, Nathan PJ, Tancer ME (2006) Association between amygdala hyperactivity to harsh faces and severity of social anxiety in generalized social phobia. Biol Psychiatry 59:424–429. https://doi.org/10.1016/j.biopsych.2005.08.012
Pidoplichko VI, Prager EM, Aroniadou-Anderjaska V, Braga MF (2013) Alpha7-Containing nicotinic acetylcholine receptors on interneurons of the basolateral amygdala and their role in the regulation of the network excitability. J Neurophysiol 110:2358–2369. https://doi.org/10.1152/jn.01030.2012
Pieper J, Chang DC, Mahasin SZ, Swan AR, Quinto AA, Nichols SL, Diwakar M, Huang C, Swan J, Lee RR, Baker DG, Huang M (2020) Brain amygdala volume increases in veterans and active-duty military personnel with combat-related posttraumatic stress disorder and mild traumatic brain injury. J Head Trauma Rehabil 35:E1–E9. https://doi.org/10.1097/HTR.0000000000000492
Pinard A, Seddik R, Bettler B (2010) GABAB receptors: physiological functions and mechanisms of diversity. Adv Pharmacol 58:231–255. https://doi.org/10.1016/S1054-3589(10)58010-4
Pollack MH, Roy-Burne PP, VanAmeringen M, Snyder H, Brown C, Ondrasik J, Richels K (2005) The selective GABA reuptake inhibitor tiagabine for the treatment of generalized anxiety disorder: results of a placebo-controlled study. J Clin Psychiatry 66:1401–1408. https://doi.org/10.4088/jcp.v66n1109
Porcher C, Hatchett C, Longbottom RE, McAinch K, Sihra TS, Moss SJ, Thomson AM, Jovanovic JN (2011) Positive feedback regulation between gamma-aminobutyric acid type A (GABA(A)) receptor signaling and brain-derived neurotrophic factor (BDNF) release in developing neurons. J Biol Chem 286:21667–21677. https://doi.org/10.1074/jbc.M110.201582
Porto I, Jurcoane A, Margerkurth J, Althaus J, Zanella F, Hattingen E, Kieslich M (2011) Morphometry and diffusion MR imaging years after childhood traumatic brain injury. Eur J Pediatr Neurol 15:493–501. https://doi.org/10.1016/j.ejpn.2011.06.004
Prins M, Greco T, Alexander D, Giza CC (2013) The pathophysiology of traumatic brain injury at a glance. Dis Model Mech 6:1307–1315. https://doi.org/10.1242/dmm.011585
Rankin KP, Gorno-Tempini ML, Allison SC, Stanley CM, Glenn S, Weiner MW, Miller BI (2006) Structural anatomy of empathy in frontolobar disease. Brain 129:2945–2956. https://doi.org/10.1093/brain/awl254
Ratliff WA, Mervis RF, Citron BA, Schwartz B, Rubovitch V, Schreiber S, Pick CG (2019) Mild blast-related TBI in a mouse model alters amygdalar neurostructure and circuitry. Exp Neurol 315:9–14. https://doi.org/10.1016/j.expneurol.2019.01.020
Rauch SL, van der Kolk BA, Fisler RE, Alpert NM, Orr SP, Savage CR, Fischman AJ, Jenike MA, Pitman RK (1996) A symptom provocation study of posttraumatic stress disorder using positron emission tomography and script-driven imagery. Arch Gen Psychiatry 53(5):380–387. https://doi.org/10.1001/archpsyc.1996.01830050014003
Rauch SL, Whalen PJ, Shin LM, McInerney SC, Macklin ML, Lasko NB, Orr SP, Pitman RK (2000) Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol Psychiatry 47:769–776. https://doi.org/10.1016/s0006-3223(00)00828-3
Ray S, Dixon CE, Banik NL (2002) Molecular mechanisms in the pathogenesis of traumatic brain injury. Histol Histopathol 17:1137–1152. https://doi.org/10.14670/HH-17.1137
Riffault B, Medina I, Dumon C, Thalman C, Ferrand N, Friedel P, Gaiarsa J-L, Porcher C (2014) Pro-brain-derived neurotrophic factor inhibits GABAergic neurotransmission by activating endocytosis and repression of GABAA receptors. J Neurosci 34:13516–13534. https://doi.org/10.1523/JNEUROSCI.2069-14.2014
Robinson OJ, Pike AC, Cornwell B, Grillon C (2019) The translational neural circuitry of anxiety. J Neurol Neurosurg Psychiatry 90:1353–1360. https://doi.org/10.1136/jnnp-2019-321400
Roozenbeek B, Maas AI, Menon DK (2013) Changing patterns in the epidemiology of traumatic brain injury. Nat Rev Neurol 9:231–236. https://doi.org/10.1038/nrneurol.2013.22
Rostami E, Davidsson J, Ng KC, Lu J, Gyorgy A, Walker J, Wingo D, Plantman S, Bellander BM, Agoston DV, Risling M (2012) A model for mild traumatic brain injury that induces limited transient memory impairment and increased levels of axon related serum biomarkers. Front Neurol 3:115. https://doi.org/10.3389/fneur.2012.00115
Rostkowski AB, Teppen TL, Peterson DA, Urban JH (2009) Cell-specific expression of neuropeptide Y Y1 receptor immunoreactivity in the rat basolateral amygdala. J Comp Neurol 517(2):166–176. https://doi.org/10.1002/cne.22143
Roy-Byrne P, Wingerson DK, Radant A, Greenblatt DJ, Cowley DS (1996) Reduced benzodiazepine sensitivity in patients with panic disorder: comparison with patients with obsessive-compulsive disorder and normal subjects. Am J Psychiatry 153:1444–1449. https://doi.org/10.1176/ajp.153.11.1444
Rushby JA, McDonald S, Fisher AC, Kornfeld EJ, De Blasio FM, Parks N, Piguet O (2016) Brain volume loss contributes to arousal and empathy dysregulation following severe traumatic brain injury. Neuroimage Clin 12:607–614. https://doi.org/10.1016/j.nicl.2016.09.017
Russell ER, McCabe T, Mackay DF, Stewart K, MacLean JA, Pell JP, Stewart W (2020) Mental health and suicide in former professional soccer players. J Neurol Neurosurg Psychiatry 91(12):1256–1260. https://doi.org/10.1136/jnnp-2020-323315
Sanders SK, Shekhar A (1995) Regulation of anxiety by GABAA receptors in the rat amygdala. Pharmacol Biochem Behav 52:701–706. https://doi.org/10.1016/0091-3057(95)00153-n
Scholten AC, Haagsma JA, Cnossen MC, Olff M, van Beeck EF, Polinder S (2016) Prevalence of and risk factors for anxiety and depressive disorders after traumatic brain injury: a systematic review. J Neurotrauma 33:1969–1994. https://doi.org/10.1089/neu.2015.4252
Semple BD, Zamani A, Rayner G, Shultz SR, Jones NC (2019) Affective, neurocognitive and psychosocial disorders associated with traumatic brain injury and post-traumatic epilepsy. Neurobiol Dis 123:27–41. https://doi.org/10.1016/j.nbd.2018.07.018
Serra-Grabulosa JM, Junqué C, Verger K, Salgado-Pineda P, Mañeru C, Mercader JM (2005) Cerebral correlates of declarative memory dysfunctions in early traumatic brain injury. J Neurol Neurosurg Psychiatry 76:129–131. https://doi.org/10.1136/jnnp.2004.027631
Shin LM, Kosslyn SM, McNally RJ, Alpert NM, Thompson WL, Rauch SL, Macklin ML, Pitman RK (1997) Visual imagery and perception in posttraumatic stress disorder. A positron emission tomographic investigation. Arch Gen Psychiatry 54:233–241. https://doi.org/10.1001/archpsyc.1997.01830150057010 (PMID: 9075464)
Shin LM, Orr SP, Carson MA, Rauch SL, Macklin ML, Lasko NB, Peters PM, Metzger LJ, Dougherty DD, Cannistraro PA, Alpert NM, Fischman AJ, Pitman RK (2004) 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 61:168–176. https://doi.org/10.1001/archpsyc.61.2.168
Sigel E, Buhr A (1997) The benzodiazepine binding site of GABAA receptors. Trends Pharmacol Sci 18:425–429. https://doi.org/10.1016/s0165-6147(97)01118-8
Sigel E, Steinmann ME (2012) Structure, function, and modulation of GABA(A) receptors. J Biol Chem 287:40224–40231. https://doi.org/10.1074/jbc.R112.386664
Simon D, Kaufmann C, Musch K, Kischkel E, Kathmann N (2010) Fronto–striato–limbic hyperactivation in obsessive–compulsive disorder during individually tailored symptom provocation. Psychophysiology 47:728–738. https://doi.org/10.1111/j.1469-8986.2010.00980.x
Smith Y, Pare D (1994) Intra-amygdaloid projections of the lateral nucleus in the cat: PHA-L anterograde labeling combined with postembedding GABA and glutamate immunocytochemistry. J Comp Neurol 342:232–248. https://doi.org/10.1002/cne.903420207
Smith KR, McAinsh K, Chen G, Arancibia-Carcamo IL, Haucke V, Yan Z, Moss SJ, Kittler JT (2008) Regulation of inhibitory synaptic transmission by a conserved atypical interaction of GABA(A) receptor beta- and gamma-subunits with the clathrin AP2 adaptor. Neuropharmacology 55:844–850. https://doi.org/10.1016/j.neuropharm.2008.06.072
Smith KS, Engin E, Meloni EG, Rudolph U (2012) Benzodiazepine-induced anxiolysis and reduction of conditioned fear are mediated by distinct GABAA receptor subtypes in mice. Neuropharmacology 63(2):250–258. https://doi.org/10.1016/j.neuropharm.2012.03.001
Stanić D, Mulder J, Watanabe M, Hökfelt T (2011) Characterization of NPY Y2 receptor protein expression in the mouse brain. II. Coexistence with NPY, the Y1 receptor, and other neurotransmitter-related molecules. J Comp Neurol 519:1219–1257. https://doi.org/10.1002/cne.22608
Straube T, Lipka J, Sauer A, Mothes-Lasch M, Miltner WH (2011) Amygdala activation to threat under attentional load in individuals with anxiety disorder. Biol Mood Anxiety Disord 1:12. https://doi.org/10.1186/2045-5380-1-12
Sweis BM, Bachour SP, Brekke JA, Gewirtz JC, Sadeghi-Bazargani H, Hevesi M, Divani AA (2016) A modified beam-walking apparatus for assessment of anxiety in a rodent model of blast traumatic brain injury. Behav Brain Res 296:149–156. https://doi.org/10.1016/j.bbr.2015.09.015
Tasker RC, Salmond CH, Westland AG, Pena A, Gillard JF, Sahakian BJ, Gillard JH, Sahakian BJ, Pickard JD (2005) Head circumference and brain and hippocampal volume after severe traumatic brain injury in childhood. Pediatr Res 58:302–308. https://doi.org/10.1203/01.PDR.0000169965.08854.25
Tate DF, Wade BSC, Velez CS, Drennon AM, Bolzenius J, Gutman BA, Thompson PM, Lewis JD, Wilde EA, Bigler ED, Shenton ME, Ritter JL, York GE (2016) Volumetric and shape analyses of subcortical structures in United States service members with mild traumatic brain injury. J Neurol 263:2065–2079. https://doi.org/10.1007/s00415-016-8236-7
Tator CH (2014) Chronic traumatic encephalopathy: how serious a sports problem is it? Br J Sports Med 48:81–83. https://doi.org/10.1136/bjsports-2013-093040
Thorsell A (2010) Brain neuropeptide Y and coricotropin-releasing hormone in mediating stress and anxiety. Exp Biol Med (maywood) 235:1163–1167. https://doi.org/10.1258/ebm.2010.009331
Tiihonen J, Kuikka J, Räsänen P, Lepola U, Koponen H, Liuska A, Lehmusvaara A, Vainio P, Könönen M, Bergström K, Yu M, Kinnunen I, Akerman K, Karhu J (1997) Cerebral benzodiazepine receptor binding and distribution in generalized anxiety disorder: a fractal analysis. Mol Psychiatry 2:463–471. https://doi.org/10.1038/sj.mp.4000329
Tillfors M, Furmark T, Marteinsdottir I, Fischer H, Pissiota A, Långstrom B, Fredrikson M (2001) Cerebral blood flow in subjects with social phobia during stressful speaking tasks: a PET study. Am J Psychiatry 158:1220–1226. https://doi.org/10.1176/appi.ajp.158.8.1220
Tillfors M, Furmark T, Marteinsdottir I, Fredrikson M (2002) Cerebral blood flow during anticipation of public speaking in social phobia: a PET study. Biol Psychiatry 52:1113–1119. https://doi.org/10.1016/s0006-3223(02)01396-3
Truitt WA, Johnson PL, Dietrich AD, Fitz SD, Shekhar A (2009) Anxiety-like behavior is modulated by a discrete subpopulation of interneurons in the basolateral amygdala. Neuroscience 160:284–294. https://doi.org/10.1016/j.neuroscience.2009.01.083
Tye KM, Prakash R, Kim SY, Fenno LE, Grosenick L, Zarabi H, Thompson KR, Gradinaru V, Ramakrishnan C, Deisseroth K (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471:358–362. https://doi.org/10.1038/nature09820
Umile EM, Sandel ME, Alavi A, Terry CM, Plotkin RC (2002) Dynamic imaging in mild traumatic brain injury: support for the theory of medial temporal vulnerability. Arch Phys Med Rehabil 83:1506–1513. https://doi.org/10.1053/apmr.2002.35092
Vascak M, Jin X, Jacobs KM, Povlishock JT (2018) Mild traumatic brain injury induces structural and functional disconnection of local neocortical inhibitory networks via parvalbumin interneuron diffuse axonal injury. Cereb Cortex 28(5):1625–1644. https://doi.org/10.1093/cercor/bhx058
Verger K, Junqué C, Levin HS, Jurado MA, Pérez-Gómez M, Bartrés-Faz D, Barrios M, Alvarez A, Bartumeus F, Mercader JM (2001) Correlation of atrophy measures on MRI with neuropsychological sequelae in children and adolescents with traumatic brain injury. Brain Inj 15:211–221. https://doi.org/10.1080/02699050010004059
Vicini S, Ferguson C, Prybylowski K, Kralic J, Morrow AL, Homanics GE (2001) GABAA receptor α1 subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons. J Neurosci 21:3009–3016. https://doi.org/10.1523/JNEUROSCI.21-09-03009.2001
Wilde EA, Hunter JV, Newsome MR, Scheibel RS, Bigler ED, Johnson JL, Fearing MA, Cleavinger HB, Li X, Swank PR, Pedroza C, Roberson GS, Bachevalier J, Levin HS (2005) Frontal and temporal morphometric findings on MRI in children after moderate to severe traumatic brain injury. J Neurotrauma 22:333–344. https://doi.org/10.1089/neu.2005.22.333
Wilde EA, Bigler ED, Hunter JV, Fearing MA, Scheibel RS, Newsome MR, Johnson JL, Bachevalier J, Li X, Levin HS (2007) Hippocampus, amygdala, and basal ganglia morphometrics in children after moderate-to-severe traumatic brain injury. Dev Med Child Neurol 49:294–299. https://doi.org/10.1111/j.1469-8749.2007.00294.x
Wilde EA, Merkley TL, Bigler ED, Max JE, Schmidt AT, Ayoub KW, McCauley SR, Hunter JV, Hanten G, Li X, Chu ZD, Levin HS (2012) Longitudinal changes in cortical thickness in children after traumatic brain injury and their relation to behavioral regulation and emotional control. Int J Dev Neurosci 30:267–276. https://doi.org/10.1016/j.ijdevneu.2012.01.003
Willer B, Leddy JJ (2006) Management of concussion and post-concussion syndrome. Curr Treat Options Neurol 8:415–426. https://doi.org/10.1007/s11940-006-0031-9
Williams DH, Levin HS, Eisenberg HM (1990) Mild head injury classification. Neurosurgery 27:422–428
Witcher KG, Eiferman DS, Godbout JP (2015) Priming the inflammatory pump of the CNS after traumatic brain injury. Trends Neurosci 38:609–620. https://doi.org/10.1016/j.tins.2015.08.002
Wojtowicz M, Gardner AJ, Stanwell P, Zafonte R, Dickerson BC, Iverson GL (2018) Cortical thickness and subcortical brain volumes in professional rugby league players. Neuroimage Clin 18:377–381. https://doi.org/10.1016/j.nicl.2018.01.005
Xiong Y, Mahmood A, Chopp M (2013) Animal models of traumatic brain injury. Nat Rev Neurosci 14:128–142. https://doi.org/10.1038/nrn3407
Yiannakkaras C, Konstantinou N, Constantinidou F, Pettemeridou E, Eracieous E, Papacostas SS, Seimenis I (2019) Whole brain and corpus callosum diffusion tensor metrics: how do they correlate with visual and verbal memory performance in chronic traumatic brain injury. J Integr NeurOsci 18(2):95–105. https://doi.org/10.31083/j.jin.2019.02.144
Yin B, Li D-D, Huang H, Gu C-H, Bai G-H, Hu L-X, Zhuang J-F, Xhang M (2019) Longitudinal changes in diffusion tensor imaging following mild traumatic brain injury and correlation with outcome. Front Neural CiRcuits 13:28. https://doi.org/10.3389/fncir.2019.00028
Zagorchev L, Meyer C, Stehle T, Wenzel F, Young S, Peters J, Weese J, Paulsen K, Garlinghouse M, Ford J, Roth R, Flashman L, McAllister T (2016) Differences in regional brain volumes two months and one year after mild traumatic brain injury. J Neurotrauma 33:29–34. https://doi.org/10.1089/neu.2014.3831
Zhu S, Noviello CM, Teng J, Walsh RM Jr, Kim JJ, Hibbs RE (2018) Structure of a human synaptic GABAA receptor. Nature 559:67–72. https://doi.org/10.1038/s41586-018-0255-3
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This research was supported by the CounterACT Program, National Institutes of Health, Office of the Director and the National Institute of Neurological Disorders and Stroke [Grant numbers 5R21NS094131-02 and 1U01NS102135-01A1 to MFMB].
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Braga, M.F.M., Juranek, J., Eiden, L.E. et al. GABAergic circuits of the basolateral amygdala and generation of anxiety after traumatic brain injury. Amino Acids 54, 1229–1249 (2022). https://doi.org/10.1007/s00726-022-03184-y
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DOI: https://doi.org/10.1007/s00726-022-03184-y