Effects of damage to the basal forebrain on brain glucose utilization: A reevaluation using positron emission tomography in baboons with extensive unilateral excitotoxic lesion

Journal of Cerebral Blood Flow and Metabolism

Volumn 18, Issue 5, 1998, Pages 476-490

  Le Mestric, Claude ^a   Chavoix, Chantal ^a   Chapon, Françoise ^b   Mézenge, Florence ^a   Epelbaum, Jacques ^c   Baron, Jean Claude ^a,d  

^a UNIVERSITÉ DE CAEN   (France)

^b CAEN UNIVERSITY HOSPITAL   (France)

^c INSERM   (France)

^d GIP CYCERON   (France)

Author keywords

18F fluoro 2 deoxy D glucose; Acetylcholine; Alzheimer's disease; Nonhuman primate; Nucleus of Meynert

Indexed keywords

CHOLINE ACETYLTRANSFERASE; EXCITOTOXIN; FLUORODEOXYGLUCOSE F 18; GLUCOSE; IBOTENIC ACID;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BABOON; BRAIN INJURY; BRAIN METABOLISM; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DEAFFERENTATION; FOREBRAIN; GLUCOSE BRAIN LEVEL; GLUCOSE UTILIZATION; INTRACEREBRAL DRUG ADMINISTRATION; INTRAVENOUS DRUG ADMINISTRATION; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OLIVARY NUCLEUS; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL;

EID: 0031925513     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1097/00004647-199805000-00003     Document Type: Article

References (56)

1. Aigner TG, Mitchell SJ, Aggleton JP, DeLong MR, Struble RG, Price DL, Wenk GL, Pettigrew KD, Mishkin M (1991) Transient impairment of recognition memory following ibotenic-acid lesions of the basal forebrain in macaques. Exp Brain Res 86:18-26
2. Aigner T, Saunders R, Chavoix C, Frank J (1990) Application of magnetic resonance imaging to a primate model of the cholinergic deficit of Alzheimer's disease. In: Basic, Clinical, and Therapeutic Aspects of Alzheimer's and Parkinson's Diseases, vol 2 (Nagatsu T, et al., eds), New York, Plenum Press, pp 63-66
3. Baron JC (1989) Depression of energy metabolism in distant brain structures: studies with positron emission tomography in stroke patients. Semin Neurol 9:281-285
4. Bassant MH, Poindessous-Jazat F (1997) Consommation cérébrale de glucose dans un modèle de dénervation cholinergique chez le rat. Proceedings of the 4th Réunion Francophone sur la Maladie d'Alzheimer et les Syndromes apparentés, Montpellier, October 2-4, p 57
5. Benson DF, Kuhl DE, Hawkins RA, Phelps ME, Cummings JL, Tsai SY (1983) The fluorodeoxyglucose 18F scan in Alzheimer's disease and multi-infarct dementia. Arch Neurol 40:711-714
6. glc) and declarative memory in baboons. J Cereb Blood Flow Metab 17(suppl 1):S639
7. Blin J, Ray CA, Piercey MF, Bartko JJ, Mouradian MM and Chase TN (1994) Comparison of cholinergic drug effects on regional brain glucose consumption in rats and humans by means of autoradiography and positron emission tomography. Brain Res 635:196-202
8. Braak H, Braak E, Yilmazer D, de Vos RAI, Jansen ENH, Bohl J (1996) Pattern of brain destruction in Parkinson's and Alzheimer's diseases. J Neural Transm 103:455-490
9. Cutler NR. Haxby JV, Duara R, Grady CL, Kay AD, Kessler RM, Sundaram M, Rapoport SI (1985) Clinical history, brain metabolism, and neuropsychological function in Alzheimer's disease. Ann Neurol 18:298-309
10. Davies P, Maloney AJF (1976) Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 2:1403-1404
11. DeCarli C, Atack JR, Ball MJ, Kay JA, Grady CL, Fewster P, Pettigrew KD, Rapoport SI, Schapiro MB (1992) Post-mortem regional neurofibrillary tangle densities but not senile plaque densities are related to regional cerebral metabolic rates for glucose during life in Alzheimer's disease patients. Neurodegeneration 1:113-121
12. Dunnett SB, Everitt BJ and Robbins TW, (1991) The basal forebrain-cortical cholinergic system: interpreting the functional consequences of excitotoxic lesions. Trends Neurosci 14:494-501
13. Fitch W, McGeorge AP, MacKenzie ET (1978) Anaesthesia for studies of cerebral circulation: a comparison of phencyclidine and althesin in the baboon. Br J Anaesth 50:985-991
14. Fonnum F (1975) A rapid radiochemical method for the determination of choline acetyltransferase. J Neurochem 24:407-409
15. Frackowiak RJS, Pozzilli C, Legg N, Du Boulay GH, Marshall J, Lenzi GL, Jones T (1981) Regional cerebral oxygen supply and utilization in dementia: a clinical and physiological study with oxygen-15 and positron tomography. Brain 104:753-758
16. Frey KA, Agranoff BW (1983) Barbiturate-enhanced detection of brain lesions by carbon- 14-labeled 2-deoxyglucose autoradiography. Science 219:879-881
17. Gamzu ER, Thal LJ, Davis KL (1990) Therapeutic trials using tacrine and other cholinesterase inhibitors. In: Advances in Neurology: Alzheimer's Disease, vol 51 (Wurtman RJ, et al., eds), New York, Raven Press, pp 241-245
18. Geaney DP, Soper N, Shepstone BJ, Cowen PJ (1990) Effect of central cholinergic stimulation on regional cerebral blood flow in Alzheimer disease. Lancet 335:1484-1487
19. Geula C, Mesulam MM (1994) Cholinergic systems and related neuropathological predilection patterns in Alzheimer disease. In: Alzheimer Disease (Terry RD, Katzman R, Bick KL, eds), New York, Raven Press, pp 263-291
20. 18F-fluoro-2-deoxy-D-glucose using aminopolyether supported nucleophilic substitution. J Nucl Med 27:235-238
21. Haxby JV (1990) Cognitive deficits and local metabolic changes in dementia of the Alzheimer type. In: Imaging, Cerebral Topography and Alzheimer's Disease (Rapoport SR, Petit H, Leys D, Christen Y, eds), Berlin, Springer-Verlag, pp 109-119
22. Huang SC, Phelps ME, Hoffman EJ, Sideris K, Selin CJ, Kuhl DE (1980) Non-invasive determination of local cerebral metabolic rate of glucose in man. Am J Physiol 238:569-582
23. Kása P (1986) The cholinergic systems in brain and spinal cord. Prog Neurobiol 26:211-272
24. Kennedy AM, Frackowiak RSJ, Newman SK, Bloomfield PM, Seaward J. Roques P, Lewington G, Cunningham VJ, Rossor MN (1995) Deficits in cerebral glucose metabolism demonstrated by positron emission tomography in individuals at risk of familial Alzheimer's disease. Neurosci Lett 186:17-20
25. Kiyosawa M, Baron JC, Hamel E, Pappata S, Duverger D, Riche D, Mazoyer B, Naquet R, MacKenzie ET (1989) Time course of effects of unilateral lesions of the nucleus basalis of Meynert on glucose utilization by the cerebral cortex. Brain 112:435-455
26. Kuhl DE, Minoshima S, Fessler JA, Frey KA, Foster NL, Ficaro EP, Wieland DM, Koeppe RA (1996) In vivo mapping of cholinergic terminals in normal aging, Alzheimer's disease, and Parkinson's disease. Ann Neurol 40:399-410
27. Lamarca MV and Fibiger HC (1984) Deoxyglucose uptake and choline acetyltransferase activity in cerebral cortex following lesions of the nucleus basalis magnocellularis. Brain Res 307:366-369
28. Lehéricy S, Hirsch ÉC. Cervera-Piérot P, Hersh LB, Bakchine S, Piette F. Duyckaerts C, Hauw J-J, Javoy-Agid F, Agid Y (1993) Heterogeneity and selectivity of the degeneration of the cholinergic neurons in the basal forebrain of patients with Alzheimer's disease. J Comp Neurol 330:15-31
29. Le Mestric C, Chavoix C, Miyazawa H, Tillet I, Allain P, Luet D, Gourand F, Travère J, MacKenzie ET, Baron JC (1993) Lesional models in the non-human primate brain: advances with magnetic resonance imaging (MRI) and coronal positron emission tomography (PET). In: Quantification of Brain Function: Tracer Kinetics and Image Analysis in Brain PET (Uemura K et al., eds), Amsterdam, Elsevier Science, pp 475-485
30. London ED, McKinney M, Dam M, Ellis A, Coyle JT (1984) Decreased cortical glucose utilization after ibotenate lesion of the rat ventromedial globus pallidus. J Cereb Blood Flow Metab 4:381-390
31. Markowska AL, Wenk GL, Olton DS (1990) Nucleus basalis magnocellularis and memory: differential effects of two neurotoxins. Behav Neural Biol 54:13-26
32. Mazoyer B, Trebossen R, Shoukroun C, Verrey B, Syrota A, Vacher J, Lemasson P, Monnet O, Bouvier A, Lecomte JL (1990) Physical characteristics of TTV03, a new high spatial resolution time-of-flight positron tomograph. IEEE Trans Nucl Sci 37:778-782
33. McGeer PL, Kamo H, Harrop R, McGeer EG, Martin WRW, Pate BD, Li DKB (1986) Comparison of PET, MRI, and CT with pathology in a proven case of Alzheimer's disease. Neurology 36:1569-1574
34. Mesulam M-M, Mufson EJ, Levey AI, Wainer BH (1983) Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections on the septal area, diagonal band nuclei, nucleus basalis (substantia innominata) and hypothalamus in the rhesus monkey. J Comp Neurol 214:170-197
35. Mielke R, Schröder R, Fink GR, Kessler J, Herholz K, Heiss WD (1996) Regional cerebral glucose metabolism and postmortem pathology in Alzheimer's disease. Acta Neuropathol 91:174-179
36. Miyazawa H, Osmont A, Petit-Taboué MC, Tillet I, Travère JM, Young AR, Barré L. MacKenzie ET, Baron JC (1993) Determination of 18F-fluoro-2-deoxy-D-glucose rate constants in the anesthetized baboon brain with dynamic positron tomography. J Neurosci Meth 50:263-272
37. Orzi F, Diana G, Casamenti F, Palombo E, Fieschi C (1988) Local cerebral glucose utilization following unilateral and bilateral lesions of the nucleus basalis magnocellularis in the rat. Brain Res 462:99-103
38. Ouchi Y, Fukuyama H, Ogawa M, Yamauchi H, Kimura J, Magata Y. Yonekura Y, Konishi J (1996) Cholinergic projection from the basal forebrain and cerebral glucose metabolism in rats: a dynamic PET study. J Cereb Blood Flow Metab 16:34-41
39. Palmer AM, Gary C, Stratmann GC, Procter AW, Bowen DM (1988) Possible neurotransmitter basis of behavorial changes in Alzheimer's disease. Ann Neurol 23:616-620
40. Perry EK, Tomlinson BE, Blessed G, Bergmann K, Gibson PH, Perry RH (1978) Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. Br Med J 2: 1457-1459
41. Phelps ME, Huang SC, Hoffman EJ, Selin C, Sokoloff L, Kuhl DE (1979) Tomographic measurement of local cerebral glucose metabolic rate in humans with (F-18)2-fluoro-2-deoxy-D-glucose: validation of method. Ann Neurol 6:371-388
42. Rasool CG, Svendsen CN, Selkoe DJ (1986) Neurofibrillary degeneration of cholinergic and noncholinergic neurons of the basal forebrain in Alzheimer's disease. Ann Neurol 20:482-488
43. Richardson PJ (1981) Quantitation of cholinergic synaptosomes from guinea pig brain. J Neurochem 37:258-260
44. Riche D. Christolomme A, Bert J, Naquet R (1968). Atlas Stéréotaxique du Cerveau de Babouin (Papio papio), Paris, Centre National de la Recherche Scientifique (ed), p 207
45. Ridley RM. Baker HF, Drewett B, Johnson JA (1985) Effects of ibotenic acid lesions of the basal forebrain on serial reversal learning in marmosets. Psychopharmacology 86:438-443
46. Robbins TW, Everitt BJ, Ryan CN, Marston HM, Jones GH, Page KJ (1989) Comparative effects of quisqualic and ibotenic acid-induced lesions of the substantia innominata and globus pallidus on the acquisition of a conditional visual discrimination: differential effects on cholinergic mechanisms. Neuroscience 28:337-352
47. Roberts AC, Robbins TW, Everitt BJ, Muir JL (1992) A specific form of cognition rigidity following excitotoxic lesions of the basal forebrain in marmosets. Neuroscience 47:251-264
48. Satoh K, Fibiger HC (1985) Distribution of central cholinergic neurons in the baboon (Papio papio). Part I. General morphology. J Comp Neurol 236:197-214
49. Soncrant TT, Holloway HW, Horwitz B, Rapoport SI, Lamour YA (1992) Effect of nucleus basalis magnocellularis ablation on local brain glucose utilization in the rat: functional brain reorganization. Eur J Neurosci 4:653-662
50. Struble RG, Lehmann J, Mitchell SJ, McKinney M, Price D, Coyle JT, DeLong MR (1986) Basal forebrain neurons provide major cholinergic innervation of primate neocortex. Neurosci Lett 66:215-220
51. Tsukada H, Kakiuchi T, Ando I, Shizuno H, Nakanishi S, Ouchi Y (1997) Regulation of cerebral blood flow response to somatosensory stimulation through the cholinergic system: a positron emission tomography study in unanesthetized monkeys. Brain Res 749: 10-17
52. Vaucher E, Borredon J, Bonvento G, Seylaz J, Lacombe P (1997) Autoradiographic evidence for flow-metabolism uncoupling during stimulation of the nucleus basalis of Meynert in the conscious rat. J Cereb Blood Flow Metab 17:686-694
53. Voytko ML, Olton DS, Richardson RT, Gorman LK, Tobin JR, Price DL (1994) Basal forebrain lesions in monkeys disrupt attention but not learning and memory. J Neurosci 14:167-186
54. Whitehouse PJ, Price DL, Struble RG, Clark AW, Coyle JT, DeLong MR (1982) Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 215:1237-1239
55. Wilcock GK, Esiri MM, Bowen DM, Smith CCT (1982) Alzheimer disease: correlation of cortical choline acetyltransferase activity with the severity of dementia and histological abnormalities. J Neurol Sci 57:407-417
56. Yamaguchi T, Kunimoto M, Pappata S, Chavoix C, Brouillet E, Riche D. Mazière M, Naquet R, MacKenzie ET, Baron JC (1990) Effects of unilateral lesion of the nucleus basalis of Meynert on brain glucose utilization in callosotomized baboons: a PET study. J Cereb Blood Flow Metab 10:618-623