Long-term cognitive impairment, neuronal loss and reduced cortical cholinergic innervation after recovery from sepsis in a rodent model

Experimental Neurology

Volumn 204, Issue 2, 2007, Pages 733-740

  Semmler, Alexander ^a   Frisch, Christian ^b   Debeir, Thomas ^c   Ramanathan, Mutiah ^a   Okulla, Thorsten ^a   Klockgether, Thomas ^a   Heneka, Michael T ^d  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^d UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Behavior; Cholinergic innervation; Cortex; Hippocampus; Lipopolysaccharides; Memory disorders; Rat; Sepsis

Indexed keywords

ESCHERICHIA COLI LIPOPOLYSACCHARIDE; VESICULAR ACETYLCHOLINE TRANSPORTER;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BACTERIAL INFECTION; BRAIN TISSUE; CHOLINERGIC SYSTEM; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; CONVALESCENCE; ESCHERICHIA COLI; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LEARNING; MALE; MAZE TEST; MEMORY; MEMORY DISORDER; NONHUMAN; OPEN FIELD BEHAVIOR; PARASYMPATHETIC INNERVATION; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SEPSIS; TASK PERFORMANCE;

ANIMALS; CEREBRAL CORTEX; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; MALE; MAZE LEARNING; NEURONS; PHOSPHOPYRUVATE HYDRATASE; POLYSACCHARIDES; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; SEPSIS; TIME FACTORS; VESICULAR TRANSPORT PROTEINS;

EID: 33947690200     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2007.01.003     Document Type: Article

References (47)

1. Angus D.C., Linde-Zwirble W.T., Lidicker J., Clermont G., Carcillo J., and Pinsky M.R. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29 (2001) 1303-1310
2. Arvidsson U., Riedl M., Elde R., and Meister B. Vesicular acetylcholine transporter (VAChT) protein: a novel and unique marker for cholinergic neurons in the central and peripheral nervous systems. J. Comp. Neurol. 378 (1997) 454-467
3. Barichello T., Martins M.R., Reinke A., Feier G., Ritter C., Quevedo J., and Dal Pizzol F. Cognitive impairment in sepsis survivors from cecal ligation and perforation. Crit. Care Med. 33 (2005) 221-223
4. Barichello T., Martins M.R., Reinke A., Feier G., Ritter C., Quevedo J., and Dal Pizzol F. Long-term cognitive impairment in sepsis survivors. Crit. Care Med. 33 (2005) 1671
5. Barichello T., Fortunato J.J., Vitali A.M., Feier G., Reinke A., Moreira J.C., Quevedo J., and Dal Pizzol F. Oxidative variables in the rat brain after sepsis induced by cecal ligation and perforation. Crit. Care Med. 34 (2006) 886-889
6. Buras J.A., Holzmann B., and Sitkovsky M. Animal models of sepsis: setting the stage. Nat. Rev., Drug Discov. 4 (2005) 854-865
7. Chao C.C., Hu S., and Peterson P.K. Glia, cytokines, and neurotoxicity. Crit. Rev. Neurobiol. 9 (1995) 189-205
8. Ching S., Zhang H., Lai W., and Quan N. Peripheral injection of lipopolysaccharide prevents brain recruitment of leukocytes induced by central injection of interleukin-1. Neuroscience 137 (2006) 717-726
9. Debeir T., Saragovi H.U., and Cuello A.C. A nerve growth factor mimetic TrkA antagonist causes withdrawal of cortical cholinergic boutons in the adult rat. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 4067-4072
10. Dixon C.E., Kochanek P.M., Yan H.Q., Schiding J.K., Griffith R.G., Baum E., Marion D.W., and DeKosky S.T. One-year study of spatial memory performance, brain morphology, and cholinergic markers after moderate controlled cortical impact in rats. J. Neurotrauma 16 (1999) 109-122
11. Eckenstein F.P., Baughman R.W., and Quinn J. An anatomical study of cholinergic innervation in rat cerebral cortex. Neuroscience 25 (1988) 457-474
12. Gage F.H., Bjorklund A., and Stenevi U. Reinnervation of the partially deafferented hippocampus by compensatory collateral sprouting from spared cholinergic and noradrenergic afferents. Brain Res. 268 (1983) 27-37
13. Gilmor M.L., Nash N.R., Roghani A., Edwards R.H., Yi H., Hersch S.M., and Levey A.I. Expression of the putative vesicular acetylcholine transporter in rat brain and localization in cholinergic synaptic vesicles. J. Neurosci. 16 (1996) 2179-2190
14. Granja C., Dias C., Costa-Pereira A., and Sarmento A. Quality of life of survivors from severe sepsis and septic shock may be similar to that of others who survive critical illness. Crit. Care 8 (2004) R91-R98
15. Hauss-Wegrzyniak B., Vraniak P.D., and Wenk G.L. LPS-induced neuroinflammatory effects do not recover with time. NeuroReport 11 (2000) 1759-1763
16. Heidbreder C.A., and Groenewegen H.J. The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci. Biobehav. Rev. 27 (2003) 555-579
17. Heyland D.K., Hopman W., Coo H., Tranmer J., and McColl M.A. Long-term health-related quality of life in survivors of sepsis. Short Form 36: a valid and reliable measure of health-related quality of life. Crit. Care Med. 28 (2000) 3599-3605
18. Hu S., Peterson P.K., and Chao C.C. Cytokine-mediated neuronal apoptosis. Neurochem. Int. 30 (1997) 427-431
19. Jarrard L.E. What does the hippocampus really do?. Behav. Brain Res. 71 (1995) 1-10
20. Kolb B., and Walkey J. Behavioural and anatomical studies of the posterior parietal cortex in the rat. Behav. Brain Res. 23 (1987) 127-145
21. Liu B., Gao H.M., Wang J.Y., Jeohn G.H., Cooper C.L., and Hong J.S. Role of nitric oxide in inflammation-mediated neurodegeneration. Ann. N. Y. Acad. Sci. 962 (2002) 318-331
22. Luhmann H.J., Huston J.P., and Hasenohrl R.U. Contralateral increase in thigmotactic scanning following unilateral barrel-cortex lesion in mice. Behav. Brain Res. 157 (2005) 39-43
23. Mello E.S., Vianna M.R., Rodrigues C., Quevedo J., Moleta B.A., and Izquierdo I. Involvement of the medial precentral prefrontal cortex in memory consolidation for inhibitory avoidance learning in rats. Pharmacol. Biochem. Behav. 66 (2000) 615-622
24. Messaris E., Memos N., Chatzigianni E., Konstadoulakis M.M., Menenakos E., Katsaragakis S., Voumvourakis C., and Androulakis G. Time-dependent mitochondrial-mediated programmed neuronal cell death prolongs survival in sepsis. Crit. Care Med. 32 (2004) 1764-1770
25. Mesulam M.M., Mufson E.J., Wainer B.H., and Levey A.I. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10 (1983) 1185-1201
26. Mesulam M., Shaw P., Mash D., and Weintraub S. Cholinergic nucleus basalis tauopathy emerges early in the aging-MCI-AD continuum. Ann. Neurol. 55 (2004) 815-828
27. Mogensen J., Moustgaard A., Khan U., Wortwein G., and Nielsen K.S. Egocentric spatial orientation in a water maze by rats subjected to transection of the fimbria-fornix and/or ablation of the prefrontal cortex. Brain Res. Bull. 65 (2005) 41-58
28. Nelson C.L., Sarter M., and Bruno J.P. Prefrontal cortical modulation of acetylcholine release in posterior parietal cortex. Neuroscience 132 (2005) 347-359
29. Paxinos G., Watson C., Pennisi M., and Topple A. Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight. J. Neurosci. Methods 13 (1985) 139-143
30. Perl T.M., Dvorak L., Hwang T., and Wenzel R.P. Long-term survival and function after suspected gram-negative sepsis. JAMA 274 (1995) 338-345
31. Perry E., Walker M., Grace J., and Perry R. Acetylcholine in mind: a neurotransmitter correlate of consciousness?. Trends Neurosci. 22 (1999) 273-280
32. Pine R.W., Wertz M.J., Lennard E.S., Dellinger E.P., Carrico C.J., and Minshew B.H. Determinants of organ malfunction or death in patients with intra-abdominal sepsis. A discriminant analysis. Arch. Surg. 118 (1983) 242-249
33. Reimann-Philipp U., Ovase R., Weigel P.H., and Grammas P. Mechanisms of cell death in primary cortical neurons and PC12 cells. J. Neurosci. Res. 64 (2001) 654-660
34. Ricceri L., Minghetti L., Moles A., Popoli P., Confaloni A., De Simone R., Piscopo P., Scattoni M.L., di Luca M., and Calamandrei G. Cognitive and neurological deficits induced by early and prolonged basal forebrain cholinergic hypofunction in rats. Exp. Neurol. 189 (2004) 162-172
35. Rietschel E.T., Brade H., Holst O., Brade L., Muller-Loennies S., Mamat U., Zahringer U., Beckmann F., Seydel U., Brandenburg K., Ulmer A.J., Mattern T., Heine H., Schletter J., Loppnow H., Schonbeck U., Flad H.D., Hauschildt S., Schade U.F., Di Padova F., Kusumoto S., and Schumann R.R. Bacterial endotoxin: chemical constitution, biological recognition, host response, and immunological detoxification. Curr. Top. Microbiol. Immunol. 216 (1996) 39-81
36. Ringman J.M., and Cummings J.L. Current and emerging pharmacological treatment options for dementia. Behav. Neurol. 17 (2006) 5-16
37. Save E., and Poucet B. Hippocampal-parietal cortical interactions in spatial cognition. Hippocampus 10 (2000) 491-499
38. Schmitz C., and Hof P.R. Design-based stereology in neuroscience. Neuroscience 130 (2005) 813-831
39. Semmler A., Okulla T., Sastre M., Dumitrescu-Ozimek L., and Heneka M.T. Systemic inflammation induces apoptosis with variable vulnerability of different brain regions. J. Chem. Neuroanat. 30 (2005) 144-157
40. Sharshar T., Annane D., de la Grandmaison G.L., Brouland J.P., Hopkinson N.S., and Francoise G. The neuropathology of septic shock. Brain Pathol. 14 (2004) 21-33
41. Shulz D.E., Ego-Stengel V., and Ahissar E. Acetylcholine-dependent potentiation of temporal frequency representation in the barrel cortex does not depend on response magnitude during conditioning. J. Physiol. Paris 97 (2003) 431-439
42. Sprung C.L., Peduzzi P.N., Shatney C.H., Schein R.M., Wilson M.F., Sheagren J.N., and Hinshaw L.B. Impact of encephalopathy on mortality in the sepsis syndrome. The Veterans Administration Systemic Sepsis Cooperative Study Group. Crit. Care Med. 18 (1990) 801-806
43. Squire L.R., and Zola-Morgan S. The medial temporal lobe memory system. Science 253 (1991) 1380-1386
44. Stork O., Welzl H., Wolfer D., Schuster T., Mantei N., Stork S., Hoyer D., Lipp H., Obata K., and Schachner M. Recovery of emotional behaviour in neural cell adhesion molecule (NCAM) null mutant mice through transgenic expression of NCAM180. Eur. J. Neurosci. 12 (2000) 3291-3306
45. Willard L.B., Hauss-Wegrzyniak B., and Wenk G.L. Pathological and biochemical consequences of acute and chronic neuroinflammation within the basal forebrain cholinergic system of rats. Neuroscience 88 (1999) 193-200
46. Young G.B., Bolton C.F., Austin T.W., Archibald Y.M., Gonder J., and Wells G.A. The encephalopathy associated with septic illness. Clin. Invest. Med. 13 (1990) 297-304
47. Zhao X., Bausano B., Pike B.R., Newcomb-Fernandez J.K., Wang K.K., Shohami E., Ringger N.C., DeFord S.M., Anderson D.K., and Hayes R.L. TNF-alpha stimulates caspase-3 activation and apoptotic cell death in primary septo-hippocampal cultures. J. Neurosci. Res. 64 (2001) 121-131