Differential effects of systemic and intraseptal administration of the acetylcholinesterase inhibitor tacrine on the recovery of spatial behavior in an animal model of diencephalic amnesia

European Journal of Pharmacology

Volumn 629, Issue 1-3, 2010, Pages 31-39

  Roland, Jessica J ^a   Levinson, Michelle ^a   Vetreno, Ryan P ^a   Savage, Lisa M ^a  

^a BINGHAMTON UNIVERSITY   (United States)

Author keywords

(Rat); Acetylcholine; Diencephalic amnesia; Septohippocampal pathway; Tacrine

Indexed keywords

ACETYLCHOLINE; CHOLINERGIC RECEPTOR; CHOLINESTERASE INHIBITOR; PYRITHIAMINE; SODIUM CHLORIDE; TACRINE; THIAMINE;

ACETYLCHOLINE BRAIN LEVEL; AMNESIA; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CELL LOSS; CHOLINERGIC ACTIVITY; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DIENCEPHALON; DOSE RESPONSE; DRUG ADMINISTRATION ROUTE; DRUG DOSE COMPARISON; DRUG MECHANISM; FOREBRAIN; HIPPOCAMPUS; INTRASEPTAL DRUG ADMINISTRATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SCORING SYSTEM; SYSTEMIC THERAPY; TASK PERFORMANCE; THIAMINE DEFICIENCY;

ACETYLCHOLINE; AMNESIA; ANIMALS; BEHAVIOR, ANIMAL; CHOLINESTERASE INHIBITORS; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION ROUTES; HIPPOCAMPUS; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SEPTUM OF BRAIN; SPATIAL BEHAVIOR; TACRINE;

EID: 74149084129     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2009.12.005     Document Type: Article

References (59)

1. 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
2. Beninger R.J., Wirsching B.A., Mallet P.E., Jhamandas K., and Boegman R.J. Physostigmine, but not 3, 4-diaminopyridine, improves radial maze performance in memory-impaired rats. Pharmacol. Biochem. Behav. 51 (1995) 739-746
3. Bunce J.G., Sabolek H.R., and Chrobak J.J. Intraseptal infusion of oxotremorine impairs memory in a delayed-non-match-to-sample radial maze task. Neuroscience 121 (2003) 259-267
4. Bunce J.G., Sabolek H.R., and Chrobak J.J. Intraseptal infusion of the cholinergic agonist carbachol impairs delayed-non-match-to-sample radial arm maze performance in the rat. Hippocampus 14 (2004) 450-459
5. Carvalho F.M., Pereira S.R.C., Pires R.G.W., Ferraz V.P., Romano-Silva M.A., Oliveria-Silva I.F., and Ribeiro A.M. Thiamine deficiency decreases glutamate uptake in the prefrontal cortex and impairs spatial memory performance in a water maze test. Pharmacol. Biochem. Behav. 83 (2006) 481-489
6. Chang Q., and Gold P.E. Intra-hippocampal lidocaine injections impair acquisition of a place task and facilitate acquisition of a response task in rats. Behav. Brain Res. 144 (2003) 19-24
7. 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
8. Chang Q., and Gold P.E. Age-related changes in memory and in acetylcholine functions in the hippocampus in the Ts65Dn mouse, a model of Down syndrome. Neurobiol. Learn. Mem. 89 (2008) 167-177
9. Degroot A., and Parent M.B. Increasing acetylcholine levels in the hippocampus or entorhinal cortex reverses the impairing effects of septal GABA receptor activation on spontaneous alternation. Learn. Memory 7 (2000) 293-302
10. Degroot A., and Parent M.B. Infusions of physostigmine into the hippocampus or the entorhinal cortex attenuate avoidance retention deficits produced by intra-septal infusions of the GABA agonist muscimol. Brain Res. 920 (2001) 10-18
11. Freund T.F., and Buzsaki G. Interneurons of the hippocampus. Hippocampus 6 (1996) 347-470
12. Frick K.M., Gorman L.K., and Markowska A.L. Oxotremorine infusions into the medial septal area of middle-aged rats affect spatial reference memory and ChAT activity. Behav. Brain Res. 80 (1996) 99-109
13. Frotscher M., and Leranth C. Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J. Comp. Neurol. 239 (1985) 237-246
14. Gao B., Hornung J.P., and Fritschy J.M. Identification of distinct GABA-a receptor subtypes in cholinergic and parvalbumin-positive neurons of the rat and marmoset medial septum diagonal band complex. Neuroscience 65 (1995) 101-117
15. Givens B.S., and Olton D.S. Cholinergic and GABAergic modulation of medial septal area: effect on working memory. Behav. Neurosci. 104 (1990) 849-855
16. Givens B.S., and Olton D.S. Bidirectional modulation of scopolamine-induced working memory impairments by muscarinic activation of the medial septal area. Neurobiol. Learn. Mem. 63 (1995) 269-276
17. Gold P.E. The many faces of amnesia. Learn. Memory 13 (2006) 506-514
18. Hasselmo M.E. The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 16 (2006) 1-6
19. Henck J. Developmental neurotoxicity: testing and interpretation. In: Massaro E.J. (Ed). Handbook of Neurotoxicology (2002), Humana Press, New York, NY 3-56
20. Imperato A., Puglisi-Allegra S., Casolini P., and Angelucci L. Changes in brain dopamine and acetylcholine release during and following stress are independent of the pituitary-adrenocortical axis. Brain Res. 538 (1991) 111-117
21. Kaplan D.R., and Miller F.D. Neurotrophin signal transdunction in the nervous system. Curr. Opin. Neurobiol. 10 (2000) 381-391
22. Langlais P.J., and Savage L.M. Thiamine deficiency in rats produces cognitive and memory deficits on spatial tasks that correlate with tissue loss in diencephalon, cortex and white matter. Behav. Brain Res. 68 (1995) 75-89
23. 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
24. Levey A.I., Edmunds S.M., Koliatsos V., Wiley R.G., and Heilman C.J. Expression of ml-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J. Neurosci. 15 (1995) 4077-4092
25. Mair R.G. On the role of thalamic pathology in diencephalic amnesia. Rev. Neurosci. 5 (1994) 105-140
26. Mair R.G., Otto T.A., Knoth R.L., Rabchenuk S.A., and Langlais P.J. Analysis of aversively conditioned learning and memory in rats recovered from pyrithiamine-induced thiamine deficiency. Behav. Neurosci. 105 (1991) 351-359
27. Manseau F., Danik M., and Williams S. A functional glutamatergic neurone network in the medial septum and diagonal band area. J. Physiol. 566 (2005) 865-884
28. Markowska A.L., Olton D.S., and Givens B.S. Cholinergic manipulations in the medial septal area: age-related effects on working memory and hippocampal electrophysiology. J. Neurosci. 15 (1995) 2063-2073
29. Matsuoka N., Maeda N., Ohkubo Y., and Yamaguchi I. Differential effects of physostigmine and pilocarpine on the spatial memory deficits produced by two septo-hippocampal deafferentations in rats. Brain Res. 559 (1991) 233-240
30. McKinney M. Brain cholinergic vulnerability: relevance to behavior and disease. Biochem. Pharmacol. 70 (2005) 1115-1124
31. Mulder J., Harkany T., Czollner K., Cremers T.I.F.H., Keijser J.N., Nyakas C., and Luiten P.G.M. Galantamine-induced behavioral recovery after sublethal excitotoxic lesions to the rat medial septum. Behav. Brain Res. 163 (2005) 33-41
32. Nakagawasai O., Tadano T., Hozumi S., Taniguchi R., Yamadera F., Tan-No K., Niijima F., Arai H., Yasuhara H., Kinemuchi H., and Kisara K. Involvement of muscarinic receptor on the impairment of avoidance learning in mice fed a thiamine-deficient diet. Biogenic Amines 16 (2001) 199-210
33. Nilsson O.G., Kalen P., Rosengren E., and Bjorklund A. Acetylcholine release in the rat hippocampus as studied by microdialysis is dependent on axonal impulse flow and increases during behavioural activation. Neuroscience 36 (1990) 325-338
34. Pang K.C.H., and Nocera R. Interactions between 192-IgG saporin and intraseptal cholinergic and GABAergic drugs: role of cholinergic medial septal neurons in spatial working memory. Behav. Neurosci. 113 (1999) 265-275
35. Parent M.B., and Baxter M.G. Septohippocampal acetylcholine: involved in but not necessary for learning and memory?. Learn. Memory 11 (2004) 9-20
36. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, San Diego, CA
37. Ragozzino M.E., Unick K.E., and Gold P.E. Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 4693-4698
38. Roland J.J., and Savage L.M. Blunted hippocampal, but not striatal, acetylcholine efflux parallels learning impairment in diencephalic-lesioned rats. Neurobiol. Learn. Mem. 87 (2007) 123-132
39. Roland J.J., and Savage L.M. The role of cholinergic and GABAergic medial septal/diagonal band cell populations in the emergence of diencephalic amnesia. Neuroscience 160 (2009) 32-41
40. Roland J.J., and Savage L.M. Blocking GABA-A receptors in the medial septum enhances hippocampal acetylcholine release and behavior in a rat model of diencephalic amnesia. Pharmacol. Biochem. Behav. 92 (2009) 480-487
41. Roland J.J., Mark K., Vetreno R.P., and Savage L.M. Increasing hippocampal acetylcholine levels enhances behavioral performance in an animal model of diencephalic amnesia. Brain Res. 1234 (2008) 116-127
42. Rowntree C.I., and Bland B.H. An analysis of cholinoceptive neurons in the hippocampal formation by direct microinfusion. Brain Res. 362 (1986) 98-113
43. Sabolek H.R., Bunce J.G., and Chrobak J.J. Intraseptal tacrine can enhance memory in cognitively impaired young rats. NeuroReport 15 (2004) 181-183
44. Sabolek H.R., Bunce J.G., Giuliana D., and Chrobak J.J. Within-subject memory decline in middle-aged rats: effects of intraseptal tacrine. Neurobiol. Aging 25 (2004) 1221-1229
45. Sabolek H.R., Bunce J.G., and Chrobak J.J. Intraseptal tacrine-induced disruptions of spatial memory performance. Behav. Brain Res. 158 (2005) 1-7
46. Savage L.M., Chang Q., and Gold P.E. Diencephalic damage decreases hippocampal acetylcholine release during spontaneous alternation testing. Learn. Memory 10 (2003) 242-246
47. Savage L.M., Roland J.J., and Klintsova A.Y. Selective septohippocampal - but not forebrain amygdalar - cholinergic dysfunction in diencephalic amnesia. Brain Res. 1139 (2007) 210-219
48. Smythe J.W., Colom L.V., and Bland B.H. The extrinsic modulation of hippocampal theta depends on the coactivation of cholinergic and GABA-ergic medial septal inputs. Neurosci. Biobehav. Rev. 16 (1992) 289-308
49. Szutowicz A., Bielarczyk H., Gul S., Ronowska A., Pawelczyk T., and Jankowska-Kulawy A. Phenotype-dependent susceptibility of cholinergic neuroblastoma cells to neurotoxic inputs. Metab. Brain Dis. 21 (2007) 149-161
50. Telting-Diaz M., and Lunte C.E. Distribution of tacrin across the blood-brain barrier in awake, freely moving rats using in vivo microdialysis sampling. Pharm. Res. 10 (1993) 44-48
51. Todd K.G., and Butterworth R.F. Mechanisms of selective neuronal cell death due to thiamine deficiency. Ann. N. Y. Acad. Sci. 893 (1999) 404-411
52. Todd K.G., and Butterworth R.F. In vivo microdialysis in an animal model of neurological disease: thiamine deficiency (Wernicke) encephalopathy. Methods 23 (2001) 55-61
53. Van der Zee E.A., and Luiten P.G.M. Cholinergic and GABAergic neurons in the rat medial septum express muscarinic acetylcholine receptors. Brain Res. 652 (1994) 263-272
54. Vetreno R.P., Anzalone S.J., and Savage L.M. Impaired, spared, and enhanced acetylcholine efflux across the hippocampus and striatum in diencephalic amnesia is dependent on task demands. Neurobiol. Learn. Mem. (2008)
55. Wallenstein G.V., and Hasselmo M.E. Functional transitions between epileptiform-like activity and associative memory in hippocampal region CA3. Brain Res. Bull. 43 (1997) 485-493
56. Wu M., Shanabrough M., Leranth C., and Alreja M. Cholinergic excitation of septohippocampal GABA but not cholinergic neurons: implications for learning and memory. J. Neurosci. 20 (2000) 3900-3908
57. Wu M., Newton S.S., Atkins J.B., Xu C., Dunman 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
58. Wu H., Hajszan T., Xu C., Leranth C., and Alreja M. Group I metabotropic glutamate receptor activation produces a direct excitation of identified septohippocampal cholinergic neurons. J. Neurophysiol. 92 (2004) 1216-1225
59. Zarrindast M.R., Bakhsha A., Rostami P., and Shafaghi B. Effects of intrahippocampal injection of GABAergic drugs on memory retention of passive avoidance learning in rats. J. Psychopharm. 16 (2002) 313-319