Selective septohippocampal - but not forebrain amygdalar - cholinergic dysfunction in diencephalic amnesia

Brain Research

Volumn 1139, Issue 1, 2007, Pages 210-219

  Savage, Lisa M ^a   Roland, Jessica ^a   Klintsova, Anna ^b  

^a BINGHAMTON UNIVERSITY   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

Acetylcholine; Amygdala; Diencephalon; Hippocampus; Microdialysis; Stereology

Indexed keywords

ACETYLCHOLINE; CHOLINE ACETYLTRANSFERASE; PYRITHIAMINE; THIAMINE;

AMNESIA; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; DIENCEPHALIC AMNESIA; FOREBRAIN; HIPPOCAMPUS; LIMBIC CORTEX; MALE; MEDIAL SEPTAL DIAGONAL BAND; MEYNERT BASAL NUCLEUS; NONHUMAN; PRIORITY JOURNAL; RAT; STEREOLOGY; THIAMINE DEFICIENCY;

ACETYLCHOLINE; AMNESIA; AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC FIBERS; DISCRIMINATION LEARNING; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; MALE; NEURAL PATHWAYS; PYRITHIAMINE; RATS; RATS, SPRAGUE-DAWLEY; SEPTUM OF BRAIN; THIAMINE DEFICIENCY;

ANIMALIA; RATTUS; RODENTIA;

EID: 33847295123     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2006.12.083     Document Type: Article

References (60)

1. Aggleton J.P., and Brown M.W. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav. Brain Sci. 22 (1999) 425-489
2. Alreja M., Wu M., Liu W., Atkins J.B., Leranth C., and Shanabrough M. Muscarinic tone sustains impulse flow in the septohippocampal GABA but not cholinergic pathway: implications for learning and memory. J. Neurosci. 20 (2000) 8103-8110
3. Angunawela I., and Barker A. Anticholinesterase drugs for alcoholic Korsakoff syndrome. Int. J. Geriatr. Psychiatry 16 (2001) 338-339
4. Bentivoglio M., Aggleton J.P., and Mishkin M. The thalamus and memory formation. In: Steriade M., Jones E.J., and McCormick D.A. (Eds). Thalamus (1997), Elsevier, Amsterdam 689-720
5. Berger-Sweeney J., Heckers S., Mesulam M.M., Wiley R.G., Lappi D.A., and Sharma M. Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis. J. Neurosci. 14 (1994) 4507-4519
6. Blundell P., Hall G., and Killcross S. Lesions of the basolateral amygdala disrupt selective aspects of reinforcer representation in rats. J. Neurosci. 21 (2001) 9018-9026
7. Chang, Q., Gold, P.E., 2003. Switching memory systems during learning: changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats.
8. Chang Q., and Gold P.E. Impaired and spared cholinergic functions in the hippocampus after lesions of the medial septum/vertical limb of the diagonal band with 192 IgG-saporin. Hippocampus 14 (2004) 170-179
9. Cochrane M., Cochrane A., Jauhar P., and Ashton E. Acetylcholinesterase inhibitors for the treatment of Wernicke-Korsakoff Syndrome-Three further cases show response to donepezil. Alcohol Alcohol. 40 (2005) 151-154
10. Cohen J., and Squire L.R. Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. Science 210 (1980) 207-210
11. Colgin L.L., Kubota D., and Lynch G. Cholinergic plasticity in the hippocampus. Proc. Natl. Acad. Sci. 100 (2003) 2872-2877
12. Desjardins P., and Butterworth R.F. Role of mitochondrial dysfunction and oxidative stress in the pathogenesis of selective neuronal loss in Wernicke's encephalopathy. Mol. Neurobiol. 31 (2005) 17-25
13. Elvander E., Schött P.A., Sandin J., Bjelke B., Kehr J., Yoshitake T., and Ogren S.O. Intraseptal muscarinic ligands and galanin: influence on hippocampal acetylcholine and cognition. Neuroscience 126 (2004) 541-557
14. Gold P.E. Acetylcholine modulation of neural systems involved in learning and memory. Neurobiol. Learn. Mem. 80 (2003) 194-210
15. Gold P.E. Coordination of multiple memory systems. Neurobiol. Learn. Mem. 82 (2004) 230-242
16. Harding A., Halliday G., Caine D., and Kril J. Degeneration of anterior thalamic nuclei differentiates alcoholics with amnesia. Brain 123 (2000) 141-154
17. Hasselmo M.E. The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 16 (2006) 1-6
18. Heckers S., Ohtake T., Wiley R.G., Lappi D.A., Geula C., and Mesulam M.M. Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. J. Neurosci. 14 (1994) 1271-1289
19. Jacobson R.R., and Lishman W.A. Selective memory loss and global intellectual deficits in alcoholic Korsakoff's syndrome. Psychol. Med. 17 (1997) 649-655
20. Jenkins T.A., Dias R., Amin E., Brown M.W., and Aggleton J.P. Fos imaging reveals that lesions of the anterior thalamic nuclei produce widespread limbic hypoactivity in rats. Neuroscience 22 (2002) 5230-5238
21. Kirk I.J., and Mackay J.C. The role of theta-range oscillations in synchronizing and integrating activity in distributed mnemonic networks. Cortex 39 (2003) 993-1008
22. Kolmac C., and Mitrofanis J. Organization of the basal forebrain projection to the thalamus in rats. Neurosci. Lett. 272 (1999) 151-154
23. Kopelman M.D. The Korsakoff syndrome. Br. J. Psychiatry 166 (1995) 154-173
24. Langlais P.J., and Savage L.M. Thiamine deficiency in rats produces cognitive and memory deficits on spatial tasks which correlate with tissue loss in diencephalon, cortex and white matter. Behav. Brain Res. 68 (1995) 75-89
25. Langlais P.J., and Zhang S.X. Extracellular glutamate is increased in the thalamus during thiamine deficiency-induced lesions and is blocked by MK-801. J. Neurochem. 61 (1993) 2175-2182
26. Langlais P.J., and Zhang S.X. Cortical and subcortical white matter damage without Wernicke's encephalopathy after recovery from thiamine deficiency in the rat. Alcohol., Clin. Exp. Res. 68 (1997) 75-89
27. Langlais P.J., Zhang S.X., and Savage L.M. Neuropathology of thiamine deficiency: an update on the comparative analysis of human disorders and experimental models. Metab. Brain Dis. 11 (1996) 19-37
28. Mair R.G. On the role of thalamic pathology in diencephalic amnesia. Rev. Neurosci. 5 (1994) 105-140
29. Mair R.G., Anderson C.D., Langlais P.J., and McEntee W.J. Behavioral impairments, brain lesions, and monoaminergic activity in the rat following recovery from a bout of thiamine deficiency. Behav. Brain Res. 27 (1988) 223-239
30. Markowitsch H.J., and Pritzel M. The neuropathology of amnesia. Prog. Neurobiol. 25 (1985) 189-287
31. McIntyre C.K., Pal S.N., Marriott L.K., and Gold P.E. Competition between memory systems: acetylcholine release in the hippocampus correlates negatively with good performance on an amygdala-dependent task. J. Neurosci. 22 (2002) 1171-1176
32. McIntyre C.K., Marriott L.K., and Gold P.E. Cooperation between memory systems: acetylcholine release in the amygdala correlates positively with performance on a hippocampus-dependent task. Behav. Neurosci. 117 (2003) 320-326
33. McIntyre C.K., Marriott L.K., and Gold P.E. Patterns of brain acetylcholine release predict individual differences in preferred learning strategies in rats. Neurobiol. Learn. Mem. 79 (2003) 177-183
34. McKinney M., and Jacksonville M.C. Brain cholinergic vulnerability: relevance to behavior and disease. Biochem. Pharmacol. 70 (2005) 1115-1124
35. Miettinen R.A., Kalesnykas G., and Koivisto E.H. Estimations of the total number of cholinergic neurons containing estrogen receptors-α in the rat basal forebrain. J. Histochem. Cytochem. 50 (2002) 891-902
36. Nakagawasai O. Behavioral and neurochemical alterations following thiamine deficiency in rodents: relationship to functions of cholinergic neurons. Pharm. Soc. Japan 125 (2005) 549-554
37. Nakagawasai O., Tadano T., Hozumi S., Tan-No K., Niijima F., and Kisara K. Immunohistochemical estimation of brain choline acetyltransferase and somatostatin related to the impairment of avoidance learning induced by thiamine deficiency. Brain Res. Bull. 52 (2000) 189-196
38. Nakagawasai O., Yamadera F., Iwasaki K., Arai H., Taniguchi R., Tan-No K., Sasaki H., and Tadano T. Effect of Kamiuntan-to on impairment of learning and memory induced by thiamine-deficient feeding in mice. Neuroscience 125 (2004) 233-241
39. Parent M.B., and Baxter M.G. Septohippocampal acetylcholine: involved in but not necessary for learning and memory?. Learn. Mem. 11 (2004) 9-20
40. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, San Diego, CA
41. Pires R.G., Pereira S.R.C., Pittella E.J.H., Franco G.C., Ferreira C.L.M., Fernandes P.A., and Ribeiro A.M. The contribution of mild thiamine deficiency and ethanol consumption to central cholinergic parameter dysfunction and rats' open-field performance impairment. Pharmacol. Biochem. Behav. 70 (2001) 227-235
42. Pires R.G., Pereira S.R.C., Oliveira-Silva I.F., Franco G.C., and Ribeiro A.M. Cholinergic parameters and the retrieval of learned and re-learned spatial information: a study using a model of Wernicke-Korsakoff syndrome. Behav. Brain Res. 162 (2005) 11-21
43. Pitkin S.R., and Savage L.M. Aging potentiates acute neurological symptoms and brain pathology in pyrithiamine-induced thiamine deficient rats. Behav. Brain Res. 119 (2001) 167-177
44. Pitkin S.R., and Savage L.M. Age-related vulnerability to diencephalic amnesia produced by thiamine deficiency: the role of time of insult. Behav. Brain Res. 148 (2004) 93-105
45. Reed L.J., Lasserson D., Marsden P., Stanhope N., Stevens T., Bello F., Kingsley D., Colchester A., and Kopelman M.D. FDG-PET findings in the Wernicke-Korsakoff syndrome. Cortex 39 (2003) 1027-1045
46. Roland J.J., and Savage L.M. Hippocampal and striatal acetylcholine efflux during learning in diencephalic-lesioned rats. Neurobiol. Learn. Mem. 87 (2007) 123-132
47. Savage L. In search of the neurobiological correlates of the differential outcomes effect. Int. Physiol. Behav. Sci. 36 (2001) 182-195
48. Savage L.M., and Langlais P.J. Differential outcomes attenuates spatial memory impairments seen in pyrithiamine-induced thiamine deficiency in rats. Psychobiology 23 (1995) 153-160
49. Savage L.M., Chang Q., and Gold P.E. Diencephalic-lesions impair spontaneous alternation behavior and reduce behaviorally-activated acetylcholine release in the hippocampus. Learn. Mem. 10 (2003) 242-246
50. Sotty F., Danik M., Manseau F., Laplante F., Quirion R., and Williams S. Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicity. J. Physiol. 551 (2003) 927-943
51. Squire L.R. The neuropsychology of human memory. Annu. Rev. Neurosci. 5 (1982) 241-273
52. Todd K., and Butterworth R.F. Mechanisms of selective neuronal cell death due to thiamine deficiency. Ann. N. Y. Acad. Sci. 893 (1999) 404-411
53. Vann S.D., and Aggleton J.P. Evidence of a spatial encoding deficit in rats with lesions of the mammillary bodies or mammillothalamic tract. J. Neurosci. 23 (2003) 3506-3514
54. Vann S.D., and Aggleton J.P. The mammillary bodies: two memory systems in one?. Nat. Rev. 5 (2004) 35-44
55. Vertes R.P., Hoover W.B., and Di Prisco G.V. Theta rhythm of the hippocampus: subcortical control and functional significance. Behav. Cogn. Neurosci. Rev. 3 (2004) 173-200
56. Yoder R.M., and Pang C.H. Involvement of GABAergic and cholinergic medial septal neurons in hippocampal theta rhythm. Hippocampus 15 (2005) 381-392
57. Wainer B.H., and Mesulam M.M. Ascending cholinergic pathways in the rat brain. In: Steriade M., and Biesold D. (Eds). Brain Cholinergic Systems (1990), Oxford Science Publications, Oxford 65-119
58. Warburton E.C., Baird A., Morgan A., Muir J.L., and Aggleton J.P. The conjoint importance of the hippocampus and anterior thalamic nuclei for allocentric spatial learning: evidence from a disconnection study in the rat. J. Neurosci. 21 (2001) 7323-7330
59. Warrington E.K., and Weiskrantz L. Amnesia: a disconnection syndrome?. Neuropsychologia 20 (1982) 233-248
60. Wu M., Newton S.S., Atkins J.B., Xu C., Duman R.S., and Alreja M. Acetylcholinesterase inhibitors activate septohippocampal GABAergic neurons via muscarinic but not nicotinic receptors. J. Pharmacol. Exp. Ther. 307 (2003) 535-543