Old dog, new tricks: The attentional set-shifting test as a novel cognitive behavioral task after controlled cortical impact injury

Journal of Neurotrauma

Volumn 31, Issue 10, 2014, Pages 926-937

  Bondi, Corina O ^a,b   Cheng, Jeffrey P ^a   Tennant, Heather M ^a   Monaco, Christina M ^a   Kline, Anthony E ^a,b,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

attentional set shifting; behavior; controlled cortical impact; executive function; traumatic brain injury

Indexed keywords

ISOFLURANE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATTENTIONAL SET SHIFTING TEST; BRAIN CORTEX LESION; COGNITIVE DEFECT; COGNITIVE REHABILITATION; CONTROLLED CORTICAL IMPACT INJURY; CONTROLLED STUDY; DIET RESTRICTION; DISCRIMINATIVE STIMULUS; EXECUTIVE FUNCTION; INJURY SEVERITY; MALE; NAMED INVENTORIES, QUESTIONNAIRES AND RATING SCALES; NERVOUS SYSTEM INJURY; NONHUMAN; RAT; TASK PERFORMANCE; TRAUMATIC BRAIN INJURY; WEIGHT REDUCTION; ANIMAL; ATTENTION; BRAIN INJURY; COMPLICATION; DISEASE MODEL; NEUROPSYCHOLOGICAL TEST; SPRAGUE DAWLEY RAT;

ANIMALS; ATTENTION; BRAIN INJURIES; DISEASE MODELS, ANIMAL; EXECUTIVE FUNCTION; MALE; NEUROPSYCHOLOGICAL TESTS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84900300946     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2013.3295     Document Type: Article

References (93)

1. Summers, C. R., Ivins, B., and Schwab, K. A. (2009). Traumatic brain injury in the United States: an epidemiologic overview. Mt. Sinai J. Med. 76, 105-110.
2. Selassie, A. W., Zaloshnja, E., Langlois, J. A., Miller, T., Jones, P., and Steiner, C. (2008). Incidence of long-term disability following traumatic brain injury hospitalization, United States, 2003. J. Head Trauma Rehabil. 23, 123-131.
3. Corrigan, J. D., Selassie, A. W., and Orman, J. A. (2010). The epidemiology of traumatic brain injury. J. Head Trauma Rehabil. 25, 72-80.
4. Truelle, J. L., Koskinen, S., Hawthorne, G., Sarajuuri, J., Formisano, R., Von Wild, K., Neugebauer, E., Wilson, L., Gibbons, H., Powell, J., Bullinger, M., Hofer, S., Maas, A., Zitnay, G., Von Steinbuechel, N., and Qolibri Task, F. (2010). Quality of life after traumatic brain injury: the clinical use of the QOLIBRI, a novel disease-specific instrument. Brain Inj. 24, 1272-1291.
5. Finkelstein E. A., Corso, P. S., Miller, T. R., and Associates. (2006). The Incidence and Economic Burden of Injuries in the United States. Oxford University Press: New York.
6. Mateer, C. A., and Sira, C. S. (2006). Cognitive and emotional consequences of TBI: intervention strategies for vocational rehabilitation. NeuroRehabilitation 21, 315-326.
7. Horneman, G., and Emanuelson, I. (2009). Cognitive outcome in children and young adults who sustained severe and moderate traumatic brain injury 10 years earlier. Brain Inj. 23, 907-914.
8. Gioia, G. A., and Isquith, P. K. (2004). Ecological assessment of executive function in traumatic brain injury. Dev. Neuropsychol. 25, 135-158.
9. Hamm, R. J., Temple, M. D., O'Dell, D. M., Pike, B. R. and Lyeth, B. G. (1996). Exposure to environmental complexity promotes recovery of cognitive function after traumatic brain injury. J. Neurotrauma 13, 41-47.
10. Kline, A. E., Wagner, A. K., Westergom, B. P., Malena, R. R., Zafonte, R. D., Olsen, A. S., Sozda, C. N., Luthra, P., Panda, M., Cheng, J. P., and Aslam, H. A. (2007). Acute treatment with the 5-HT(1A) receptor agonist 8-OH-DPAT and chronic environmental enrichment confer neurobehavioral benefit after experimental brain trauma. Behav. Brain Res. 177, 186-194.
11. Kline, A. E., McAloon, R. L., Henderson, K. A., Bansal, U. K., Ganti, B. M., Ahmed, R. H., Gibbs, R. B., and Sozda, C. N. (2010). Evaluation of a combined therapeutic regimen of 8-OH-DPAT and environmental enrichment after experimental traumatic brain injury. J. Neurotrauma 27, 2021-2032.
12. Passineau, M. J., Green, E. J., and Dietrich, W. D. (2001). Therapeutic effects of environmental enrichment on cognitive function and tissue integrity following severe traumatic brain injury in rats. Exp. Neurol. 168, 373-384.
13. Shaw, K. E., Bondi, C. O., Light, S. H., Massimino, L. A., McAloon, R. L., Monaco, C. M., and Kline, A. E. (2013). Donepezil is ineffective in promoting motor and cognitive benefits after controlled cortical impact injury in male rats. J. Neurotrauma 30, 557-564.
14. Maegele, M., Lippert-Gruener, M., Ester-Bode, T., Sauerland, S., Schafer, U., Molcanyi, M., Lefering, R., Bouillon, B., Neiss, W. F., Angelov, D. N., Klug, N., McIntosh, T. K., and Neugebauer, E. A. (2005). Reversal of neuromotor and cognitive dysfunction in an enriched environment combined with multimodal early onset stimulation after traumatic brain injury in rats. J. Neurotrauma 22, 772-782.
15. Kovesdi, E., Kamnaksh, A., Wingo, D., Ahmed, F., Grunberg, N. E., Long, J. B., Kasper, C. E., and Agoston, D. V. (2012). Acute minocycline treatment mitigates the symptoms of mild blast-induced traumatic brain injury. Front. Neurol. 3, 111.
16. Hallam, T. M., Floyd, C. L., Folkerts, M. M., Lee, L. L., Gong, Q. Z., Lyeth, B. G., Muizelaar, J. P., and Berman, R. F. (2004). Comparison of behavioral deficits and acute neuronal degeneration in rat lateral fluid percussion and weight-drop brain injury models. J. Neurotrauma 21, 521-539.
17. Sebastian, V., Diallo, A., Ling, D. S., and Serrano, P. A. (2013). Robust training attenuates TBI-induced deficits in reference and working memory on the radial 8-arm maze. Front. Behav. Neurosci. 7, 38.
18. Zhao, Z., Loane, D. J., Murray, M. G. 2nd, Stoica, B. A. and Faden, A. I. (2012). Comparing the predictive value of multiple cognitive, affective, and motor tasks after rodent traumatic brain injury. J. Neurotrauma 29, 2475-2489.
19. Tong, J., Liu, W., Wang, X., Han, X., Hyrien, O., Samadani, U., Smith, D. H., and Huang, J. H. (2013). Inhibition of Nogo-66 receptor 1 enhances recovery of cognitive function after traumatic brain injury in mice. J. Neurotrauma 30, 247-258.
20. Bondi, C. O., Rodriguez, G., Gould, G. G., Frazer, A., and Morilak, D. A. (2008). Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology. 33. pag 320-331
21. Greve, K. W., Love, J. M., Sherwin, E., Mathias, C. W., Ramzinski, P., and Levy, J. (2002). Wisconsin Card Sorting Test in chronic severe traumatic brain injury: factor structure and performance subgroups. Brain Inj. 16, 29-40.
22. Benge, J. F., Caroselli, J. S., and Temple, R. O. (2007). Wisconsin Card Sorting Test: factor structure and relationship to productivity and supervision needs following severe traumatic brain injury. Brain Inj. 21, 395-400.
23. Ord, J. S., Greve, K. W., Bianchini, K. J., and Aguerrevere, L. E. (2010). Executive dysfunction in traumatic brain injury: the effects of injury severity and effort on the Wisconsin Card Sorting Test. J. Clin. Exp. Neuropsychol. 32, 132-140.
24. Hang, R. H., Xu, Y. J., Xie, H. F., and Zhu, X. Y. (2011). Evaluating on recognition impairment after traumatic brain injury with WCST. [Article in Chinese]. Fa Yi Xue Za Zhi 27, 346-349.
25. Merriam, E. P., Thase, M. E., Haas, G. L., Keshavan, M. S., and Sweeney, J. A. (1999). Prefrontal cortical dysfunction in depression determined by Wisconsin Card Sorting Test performance. Am. J. Psychiatry 156, 780-782.
26. Stuss, D. T., Levine, B., Alexander, M. P., Hong, J., Palumbo, C., Hamer, L., Murphy, K. J., and Izukawa, D. (2000). Wisconsin Card Sorting Test performance in patients with focal frontal and posterior brain damage: effects of lesion location and test structure on separable cognitive processes. Neuropsychologia. 38. pag 388-402
27. Tollefson, G. D. (1996). Cognitive function in schizophrenic patients. J. Clin. Psychiatry 57, Suppl. 11, 31-39.
28. Birrell, J. M., and Brown, V. J. (2000). Medial frontal cortex mediates perceptual attentional set shifting in the rat. J. Neurosci. 20, 4320-4324.
29. McAlonan, K., and Brown, V. J. (2003). Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behav. Brain Res. 146, 97-103.
30. Lapiz, M. D., and Morilak, D. A. (2006). Noradrenergic modulation of cognitive function in rat medial prefrontal cortex as measured by attentional set shifting capability. Neuroscience. 137. pag 1039-1049
31. Cao, A. H., Yu, L., Wang, Y. W., Wang, J. M., Yang, L. J., and Lei, G. F. (2012). Effects of methylphenidate on attentional set-shifting in a genetic model of attention-deficit/hyperactivity disorder. Behav. Brain Funct. 8, 10.
32. Brooks, J. M., Pershing, M. L., Thomsen, M. S., Mikkelsen, J. D., Sarter, M., and Bruno, J. P. (2012). Transient inactivation of the neonatal ventral hippocampus impairs attentional set-shifting behavior: reversal with an alpha7 nicotinic agonist. Neuropsychopharmacology. 37. pag 2476-2486
33. Tait, D. S., Brown, V. J., Farovik, A., Theobald, D. E., Dalley, J. W., and Robbins, T. W. (2007). Lesions of the dorsal noradrenergic bundle impair attentional set-shifting in the rat. Eur. J. Neurosci. 25, 3719-3724.
34. Broberg, B. V., Glenthoj, B. Y., Dias, R., Larsen, D. B., and Olsen, C. K. (2009). Reversal of cognitive deficits by an ampakine (CX516) and sertindole in two animal models of schizophreniasub-chronic and early postnatal PCP treatment in attentional set-shifting. Psychopharmacology (Berl. ). 206. pag 631-640
35. Goetghebeur, P. J., Lerdrup, L., Sylvest, A., and Dias, R. (2010). Erythropoietin reverses the attentional set-shifting impairment in a rodent schizophrenia disease-like model. Psychopharmacology (Berl. ). 212. pag 635-642
36. Kos, T., Nikiforuk, A., Rafa, D., and Popik, P. (2011). The effects of NMDA receptor antagonists on attentional set-shifting task performance in mice. Psychopharmacology (Berl. ). 214. pag 911-921
37. entional-set-shifting task: a method for assaying successful cognitive aging? Cogn. Affect. Behav. Neurosci. 10, 243-251.
38. Bondi, C. O., Jett, J. D., and Morilak, D. A. (2010). Beneficial effects of desipramine on cognitive function of chronically stressed rats are mediated by alpha1-adrenergic receptors in medial prefrontal cortex. Prog. Neuropsychopharmacol. Biol. Psychiatry 34, 913-923.
39. Liston, C., Miller, M. M., Goldwater, D. S., Radley, J. J., Rocher, A. B., Hof, P. R., Morrison, J. H., and McEwen, B. S. (2006). Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J. Neurosci. 26, 7870-7874.
40. Cheng, J. P., Aslam, H. A., Hoffman, A. N., Zafonte, R. D., and Kline, A. E. (2007). The neurobehavioral benefit conferred by a single systemic administration of 8-OH-DPAT after brain trauma is confined to a narrow therapeutic window. Neurosci. Lett. 416, 165-168.
41. Cheng, J. P., Hoffman, A. N., Zafonte, R. D., and Kline, A. E. (2008). A delayed and chronic treatment regimen with the 5-HT1A receptor agonist 8-OH-DPAT after cortical impact injury facilitates motor recovery and acquisition of spatial learning. Behav. Brain Res. 194, 79-85.
42. Cheng, J. P., Shaw, K. E., Monaco, C. M., Hoffman, A. N., Sozda, C. N., Olsen, A. S., and Kline, A. E. (2012). A relatively brief exposure to environmental enrichment after experimental traumatic brain injury confers long-term cognitive benefits. J. Neurotrauma 29, 2684-2688.
43. Kline, A. E., Yu, J., Massucci, J. L., Zafonte, R. D., and Dixon, C. E. (2002). Protective effects of the 5-HT1A receptor agonist 8-hydroxy- 2-(di-n-propylamino)tetralin against traumatic brain injury-induced cognitive deficits and neuropathology in adult male rats. Neurosci. Lett. 333, 179-182.
44. Yelleswarapu, N. K., Tay, J. K., Fryer, W. M., Shah, M. A., Garcia, A. N., Cheng, J. P., and Kline, A. E. (2012). Elucidating the role of 5- HT(1A) and 5-HT(7) receptors on 8-OH-DPAT-induced behavioral recovery after experimental traumatic brain injury. Neurosci. Lett. 515, 153-156.
45. Kline, A. E., Massucci, J. L., Dixon, C. E., Zafonte, R. D., and Bolinger, B. D. (2004). The therapeutic efficacy conferred by the 5- HT(1A) receptor agonist 8-Hydroxy-2-(di-n-propylamino)tetralin (8-OH-DPAT) after experimental traumatic brain injury is not mediated by concomitant hypothermia. J. Neurotrauma 21, 175-185.
46. Hoffman, A. N., Cheng, J. P., Zafonte, R. D., and Kline, A. E. (2008). Administration of haloperidol and risperidone after neurobehavioral testing hinders the recovery of traumatic brain injury-induced deficits. Life Sci. 83, 602-607.
47. Sozda, C. N., Hoffman, A. N., Olsen, A. S., Cheng, J. P., Zafonte, R. D., and Kline, A. E. (2010). Empirical comparison of typical and atypical environmental enrichment paradigms on functional and histological outcome after experimental traumatic brain injury. J. Neurotrauma 27, 1047-1057.
48. Olsen, A. S., Sozda, C. N., Cheng, J. P., Hoffman, A. N., and Kline, A. E. (2012). Traumatic brain injury-induced cognitive and histological deficits are attenuated by delayed and chronic treatment with the 5- HT(1A)-receptor agonist buspirone. J. Neurotrauma 29, 1898-1907.
49. Dias, R., Robbins, T. W., and Roberts, A. C. (1996). Primate analogue of the Wisconsin Card Sorting Test: effects of excitotoxic lesions of the prefrontal cortex in the marmoset. Behav. Neurosci. 110, 872-886.
50. Nyhus, E., and Barcelo, F. (2009). The Wisconsin Card Sorting Test and the cognitive assessment of prefrontal executive functions: a critical update. Brain Cogn. 71, 437-451.
51. McAllister, T. W. (2008). Neurobehavioral sequelae of traumatic brain injury: evaluation and management. World Psychiatry. 7. pag 3-10
52. McAllister, T. W. (2011). Neurobiological consequences of traumatic brain injury. Dialogues Clin. Neurosci. 13, 287-300.
53. Schwarzbold, M., Diaz, A., Martins, E. T., Rufino, A., Amante, L. N., Thais, M. E., Quevedo, J., Hohl, A., Linhares, M. N., and Walz, R. (2008). Psychiatric disorders and traumatic brain injury. Neuropsychiatr. Dis. Treat. 4, 797-816.
54. Sorg, S. F., Delano-Wood, L., Luc, N., Schiehser, D. M., Hanson, K. L., Nation, D. A., Lanni, E., Jak, A. J., Lu, K., Meloy, M. J., Frank, L. R., Lohr, J. B., and Bondi, M. W. (2014). White matter integrity in veterans with mild traumatic brain injury: associations with executive function and loss of consciousness. J. Head Trauma Rehabil. 29, 21-32.
55. Finnanger, T. G., Skandsen, T., Andersson, S., Lydersen, S., Vik, A., and Indredavik, M. (2013). Differentiated patterns of cognitive impairment 12 months after severe and moderate traumatic brain injury. Brain Inj. 27, 1606-1616.
56. Slomine, B. S., Gerring, J. P., Grados, M. A., Vasa, R., Brady, K. D., Christensen, J. R., and Denckla, M. B. (2002). Performance on measures of executive function following pediatric traumatic brain injury. Brain Inj. 16, 759-772.
57. Hashimoto, K., Uruma, G., and Abo, M. (2008). Activation of the prefrontal cortex during the Wisconsin Card Sorting Test (Keio Version) as measured by two-channel near-infrared spectroscopy in patients with traumatic brain injury. Eur. Neurol. 59, 24-30.
58. Lombardi, W. J., Andreason, P. J., Sirocco, K. Y., Rio, D. E., Gross, R. E., Umhau, J. C., and Hommer, D. W. (1999). Wisconsin Card Sorting Test performance following head injury: dorsolateral frontostriatal circuit activity predicts perseveration. J. Clin. Exp. Neuropsychol. 21, 2-16.
59. Millis, S. R., Rosenthal, M., Novack, T. A., Sherer, M., Nick, T. G., Kreutzer, J. S., High, W. M., Jr., and Ricker, J. H. (2001). Long-term neuropsychological outcome after traumatic brain injury. J. Head Trauma Rehabil. 16, 343-355.
60. Taylor, A. N., Rahman, S. U., Sanders, N. C., Tio, D. L., Prolo, P., and Sutton, R. L. (2008). Injury severity differentially affects short- and long-term neuroendocrine outcomes of traumatic brain injury. J. Neurotrauma 25, 311-323.
61. Binder, L. M., Kelly, M. P., Villanueva, M. R., and Winslow, M. M. (2003). Motivation and neuropsychological test performance following mild head injury. J. Clin. Exp. Neuropsychol. 25, 420-430.
62. Andreollo, N. A., Santos, E. F., Araujo, M. R., and Lopes, L. R. (2012). Rat's age versus human's age: what is the relationship? Arq. Bras. Cir. Dig. 25, 49-51.
63. Quinn, R. sti (2005). Comparing rat's to human's age: how old is my rat in people years? Nutrition. 21. pag 775-777
64. Chiarello, C., and Maxfield, L. (1996). Varieties of interhemispheric inhibition, or how to keep a good hemisphere down. Brain Cogn. 30, 81-108.
65. Cabeza, R., Nyberg, L., and Park, D. C. (2004). Cognitive Neuroscience of Aging: Linking Cognitive and Cerebral Aging. Oxford University Press: New York.
66. Callahan, C. D., and Hinkebein, J. (1999). Neuropsychological significance of anosmia following traumatic brain injury. J. Head Trauma Rehabil. 14, 581-587.
67. Ikeda, K., Sakurada, T., Takasaka, T., Okitsu, T., and Yoshida, S. (1995). Anosmia following head trauma: preliminary study of steroid treatment. Tohoku J. Exp. Med. 177, 343-351.
68. Kobayashi, M., and Costanzo, R. M. (2009). Olfactory nerve recovery following mild and severe injury and the efficacy of dexamethasone treatment. Chem. Senses 34, 573-580.
69. Bakker, K., Catroppa, C., and Anderson, V. (2014). Olfactory dysfunction in pediatric traumatic brain injury: a systematic review. J Neurotrauma. 31. pag 308-314
70. Callahan, C. D., and Hinkebein, J. H. (2002). Assessment of anosmia after traumatic brain injury: performance characteristics of the University of Pennsylvania Smell Identification Test. J. Head Trauma Rehabil. 17, 251-256.
71. Rajan, R., Clement, J. P., and Bhalla, U. S. (2006). Rats smell in stereo. Science. 311. pag 666-670
72. Lopez-Mascaraque, L., and de Castro, F. (2002). The olfactory bulb as an independent developmental domain. Cell Death Differ. 9, 1279-1286.
73. Lu, X. C., and Slotnick, B. M. (1998). Olfaction in rats with extensive lesions of the olfactory bulbs: implications for odor coding. Neuroscience. 84. pag 849-866
74. Li, H., Matsumoto, K., and Watanabe, H. (1999). Different effects of unilateral and bilateral hippocampal lesions in rats on the performance of radial maze and odor-paired associate tasks. Brain Res. Bull 48, 113-119.
75. Martens, K. M., Vonder Haar, C., Hutsell, B. A., and Hoane, M. R. (2012). A discrimination task used as a novel method of testing decision- making behavior following traumatic brain injury. J. Neurotrauma 29, 2505-2512.
76. Vertes, R. P. (2004). Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse. 51. pag 32-58
77. Godsil, B. P., Kiss, J. P., Spedding, M., and Jay, T. M. (2013). The hippocampal-prefrontal pathway: the weak link in psychiatric disorders? Eur. Neuropsychopharmacol. 23, 1165-1181.
78. Aston-Jones, G., and Cohen, J. D. (2005). An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu. Rev. Neurosci. 28, 403-450.
79. Chudasama, Y., and Robbins, T. W. (2006). Functions of frontostriatal systems in cognition: comparative neuropsychopharmacological studies in rats, monkeys and humans. Biol. Psychol. 73, 19-38.
80. Robbins, T. W., and Arnsten, A. F. (2009). The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. Annu. Rev. Neurosci. 32, 267-287.
81. McGaughy, J., Ross, R. S., and Eichenbaum, H. (2008). Noradrenergic. pag but not cholinergic, deafferentation of prefrontal cortex impairs attentional set-shifting. Neuroscience 153, 63-71
82. Crofts, H. S., Dalley, J. W., Collins, P., Van Denderen, J. C., Everitt, B. J., Robbins, T. W., and Roberts, A. C. (2001). Differential effects of 6-OHDA lesions of the frontal cortex and caudate nucleus on the ability to acquire an attentional set. Cereb. Cortex 11, 1015-1026.
83. Tunbridge, E. M., Bannerman, D. M., Sharp, T., and Harrison, P. J. (2004). Catechol-o-methyltransferase inhibition improves set-shifting performance and elevates stimulated dopamine release in the rat prefrontal cortex. J. Neurosci. 24, 5331-5335.
84. Marek, G. J., and Aghajanian, G. K. (1999). 5-HT2A receptor or alpha1- adrenoceptor activation induces excitatory postsynaptic currents in layer V pyramidal cells of the medial prefrontal cortex. Eur. J. Pharmacol. 367, 197-206.
85. Clarke, H. F., Walker, S. C., Dalley, J. W., Robbins, T. W., and Roberts, A. C. (2007). Cognitive inflexibility after prefrontal serotonin depletion is behaviorally and neurochemically specific. Cereb. Cortex 17, 18-27.
86. Wagner, A. K., Drewencki, L. L., Chen, X., Santos, F. R., Khan, A. S., Harun, R., Torres, G. E., Michael, A. C., and Dixon, C. E. (2009). Chronic methylphenidate treatment enhances striatal dopamine neurotransmission after experimental traumatic brain injury. J. Neurochem. 108, 986-997.
87. Wang, T., Huang, X. J., Van, K. C., Went, G. T., Nguyen, J. T., and Lyeth, B. G. (2014). Amantadine improves cognitive outcome and increases neuronal survival after fluid percussion traumatic brain injury in rats. J. Neurotrauma 31, 370-377.
88. Prasad, M. R., Tzigaret, C. M., Smith, D., Soares, H., and McIntosh, T. K. (1992). Decreased alpha 1-adrenergic receptors after experimental brain injury. J. Neurotrauma 9, 269-279.
89. Prasad, M. R., Ramaiah, C., McIntosh, T. K., Dempsey, R. J., Hipkens, S., and Yurek, D. (1994). Regional levels of lactate and norepinephrine after experimental brain injury. J. Neurochem. 63, 1086-1094.
90. Reid, W. M., and Hamm, R. J. (2008). Post-injury atomoxetine treatment improves cognition following experimental traumatic brain injury. J. Neurotrauma 25, 248-256.
91. Dixon, C. E., Kochanek, P. M., Yan, H. Q., Schiding, J. K., Griffith, R. G., Baum, E., Marion, D. W., and DeKosky, S. T. (1999). One-year study of spatial memory performance, brain morphology, and cholinergic markers after moderate controlled cortical impact in rats. J. Neurotrauma 16, 109-122.
92. Donat, C. K., Schuhmann, M. U., Voigt, C., Nieber, K., Deuther-Conrad, W., and Brust, P. (2008). Time-dependent alterations of cholinergic markers after experimental traumatic brain injury. Brain Res. 1246, 167-177.
93. Shin, S. S., Bray, E. R., Zhang, C. Q., and Dixon, C. E. (2011). Traumatic brain injury reduces striatal tyrosine hydroxylase activity and potassium-evoked dopamine release in rats. Brain Res. 1369, 208-215.