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Local cerebral glucose utilization in the brain of old, learning impaired rats

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Summary

The local cerebral glucose utilization (LCGU) was measured in 63 different cortical areas and nuclei of the telencephalon, diencephalon and rhombencephalon of young adult (3 to 4-month-old) rats and of 27-month-old Wistar rats, in which learning impairments had been proven by a water maze test. The LCGU was determined by [14C]2-deoxyglucose autoradiography. In the old rats the mean LCGU of all brain regions was significantly reduced by about 10% compared with the young control group; the mean LCGU was 74.2 μmol glucose/(100 g × min) in the young and 66.7 in the old rats. Different degrees of LCGU decrease were found in the different regions. Most of the brain regions with significantly reduced LCGU values in the aged, learning impaired rats were associated with auditory and visual functions, the dopaminergic system, and structures known to be involved in learning and memory processes. Therefore, the regional pattern of LCGU reduction found in the aged, learning impaired rats did not resemble any known pattern found after lesions of a single transmitter system or systemic administration of transmitter agonists or antagonists.

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References

  • Algeri S, Calderini G, Toffano G, Ponzio F (1983) Neurotransmitter alterations in aging rats. In: Samuel D, Algeri S, Gershon S, Grimm VE, Toffano G (eds) Aging of the brain. Raven Press, New York, pp 227–243

    Google Scholar 

  • Astrup J, Møller Sørensen P, Rahbek Sørensen N (1981) Oxygen and glucose consumption related to Na+-K+-transport in canine brain. Stroke 12:726–730

    Google Scholar 

  • Banay-Schwartz M, Lajtha A, Palkovits M (1989) Changes with aging in the levels of the amino acids in rat CNS structural elements. I. Glutatamate and related amino acids. Neurochem Res 14:555–562

    Google Scholar 

  • Barnes CA (1979) Memory deficits associated with senescence: a neurophysiological and behavioral study. J Comp Physiol Psychol 93:74–104

    Google Scholar 

  • Bartus RT, Dean RL, Beer B, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408–417

    Google Scholar 

  • Bartus RT, Dean RL, Pontecorvo MJ, Flicker C (1985) The cholinergic hypothesis: a historical overview, current perspectives, and future directions. Ann NY Acad Sci 444:332–358

    Google Scholar 

  • Baskys A, Reynolds JN, Carlen PL (1990) NMDA depolarizations and long term potentiation are reduced in the aged rat neocortex. Brain Res 530:142–146

    Google Scholar 

  • Bauchweitz-Milton E, Weiss HR (1987a) Cerebral oxygen consumption and blood flow in Fischer-344 rats at different ages. Neurobiol Aging 8:55–60

    Google Scholar 

  • Bauchweitz-Milton E, Weiss HR (1987b) Perfused capillary morphometry in the senescent brain. Neurobiol Aging 8:271–278

    Google Scholar 

  • Bertoni-Freddari C, Meier-Ruge W, Ulrich J (1988) Quantitative morphology of synaptic plasticity in the aging brain. Scann Microsc 2:1027–1034

    Google Scholar 

  • Biegon A, Duvdevani R, Greenberger V, Segal M (1988) Aging and brain cholinergic muscarinic receptors: an autoradiographic study in the rat. J Neurochem 51:1381–1385

    Google Scholar 

  • Biegon A, Hanau M, Greenberger V, Segal M (1989) Aging and brain cholinergic muscarinic receptor subtypes: an autoradiographic study in the rat. Neurobiol Aging 10:305–310

    Google Scholar 

  • Birren JE, Botwinick J, Weiss AD, Morrison DF (1963) Interrelation of mental and perceptional tests given to healthy elderly men. In: Birren JE (ed) Human aging. A biological and behavioral study. Government Printing Office, Washington D.C., pp 143–156

    Google Scholar 

  • Björklund H, Eriksdotter-Nilsson M, Dahl D, Rose G, Hoffer B, Olson L (1985) Image analysis of GFA-positive astrocytes from adolescence to senescence. Exp Brain Res 58:163–170

    Google Scholar 

  • Brizzee KR, Ordy JM (1979) Age pigments, cell loss and hippocampal function. Mech Ageing Dev 9:143–162

    Google Scholar 

  • Buzsáki G, Bickford RG, Armstrong DM, Ponomareff G, Chen KS, Ruiz R, Thal LJ, Gage FH (1988) Electric activity in the neocortex of freely moving young and old rats. Neuroscience 26:735–744

    Google Scholar 

  • Burck HC (1988) Histologische Technik. Thieme, Stuttgart

    Google Scholar 

  • Casey MA, Feldman ML (1988) Age-related loss of synaptic terminals in the rat medial nucleus of the trapezoid body. Neuroscience 24:189–194

    Google Scholar 

  • Caspary DM, Raza A, Lawhorn-Armour BA, Pippin J, Arneric SP (1990) Immunocytochemical and neurochemical evidence for age-related loss of GABA in the inferior colliculus: implications for neural presbycusis. J Neurosci 10:2363–2372

    Google Scholar 

  • Cooper WA, Coleman RJ, Newton EH (1990) Auditory brainstem responses to tonal stimuli in young and aging rats. Hear Res 43:171–180

    Google Scholar 

  • Cotman CW, Holets VR (1985) Structural changes at synapses with age: plasticity and regeneration. In: Finch CE, Schneider EL (eds) Handbook of the biology of aging, 2nd edn. Van Nostrand-Reinhold, New York, pp 617–644

    Google Scholar 

  • Decker MW (1987) The effects of aging on hippocampal and cortical projections of the forebrain cholinergic system. Brain Res Rev 12:423–438

    Google Scholar 

  • Degrell I, Stock G, Hoyer S (1983) On the relationship between energy and neurotransmitter metabolism in rat brain cortex during aging. In: Samuel D, Algeri S, Gershon S, Grimm VE, Toffano G (eds) Aging of the brain. Raven Press, New York, pp 99–109

    Google Scholar 

  • Leon MJ de, Harris SH, George AE, Reisberg B, Christman DR, Kricheff II, Wolf AP (1983) Computed tomography and positron emission transaxial tomography evaluation of normal aging and Alzheimer's disease. J Cerebral Blood Flow Metab 3:391–394

    Google Scholar 

  • Duara R et al. (1983) Cerebral glucose utilization, as measured with positron emission topography in 21 resting healthy men between the ages of 21 and 83. Brain 106:761–775

    Google Scholar 

  • Duara R et al. (1984) Human brain glucose metabolism and cognitive functions in relation to age. Ann Neurol 16:702–713

    Google Scholar 

  • Feldman ML (1976) Aging changes in the morphology of cortical dendrites. In: Terry RD, Gershon S (eds) Neurobiology of aging (Aging, vol 3), Raven Press, New York, pp 211–227

    Google Scholar 

  • Finch CE, Schneider EL (1985) Handbook of the biology of aging, 2nd edn. Van Nostrand-Reinhold, New York

    Google Scholar 

  • Fischer W, Gage FH, Björklund A (1989) Degenerative changes in forebrain cholinergic system correlate with cognitive impairments in aged rats. Eur J Neurosci 1:34–45

    Google Scholar 

  • Franckowiak RSJ, Gibbs JM (1983) The pathophysiology of Alzheimer's disease studied with positron emission tomography. In: Katzman R (ed) Banbury Report 15: Biological aspects of Alzheimer's disease. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp 329–334

    Google Scholar 

  • Freilich JS, Weiss B (1983) Altered adaptive capacity of brain cate-cholaminergic receptors during aging. In: Samuel D, Algeri S, Gershon S, Grimm VE, Toffano G (eds) Aging of the brain. Raven Press, New York, pp 277–300

    Google Scholar 

  • Fujisawa K, Shiraki H (1978) Study on axonal dystrophy. I. Pathology of the neuropil of the gracile and the cuneate nuclei in aging and old rats: a stereological study. Neuropathol Appl Neurobiol 4:1–20

    Google Scholar 

  • Gage FH, Björklund A (1986) Cholinergic septal grafts into the hippocampal formation improve spatial learning and memory in aged rats by an atropine-sensitive mechanism. J Neurosci 6:2837–2847

    Google Scholar 

  • Gage FH, Dunnett SB, Björklund A (1984a) Spatial learning and motor deficits in aged rats. Neurobiol Aging 5:43–48

    Google Scholar 

  • Gage FH, Kelly PAT, Björklund A (1984b) Regional changes in brain glucose metabolism reflect cognitive impairments in aged rats. J Neurosci: 2856–2865

  • Geinisman Y, Toledo-Morell L de, Morell F (1986) Aged rats need a preserved complement of perforated axospinous synapses per neuron to maintain good spatial memory. Brain Res 398:266–275

    Google Scholar 

  • Giorgi O, Calderini G, Toffano G, Biggio G (1987) D-1 dopamine receptors labelled with 3H-SCH 23390: decrease in the striatum of aged rats. Neurobiol Aging 8:51–54

    Google Scholar 

  • Gomez-Pinilla F, Cotman CW, Nieto-Sampedro M (1989) NGF receptor immunoreactivity in aged rat brain. Brain Res 479:255–262

    Google Scholar 

  • Gozlan H, Daval G, Verge D, Spampinato U, Fattaccini CM, Gallissot MC, Mestikawy S el, Hamon M (1990) Aging associated changes in serotoninergic and dopaminergic pre- and postsynaptic neurochemical markers in the rat brain. Neurobiol Aging 11:437–449

    Google Scholar 

  • Guidobono F, Netti C, Bettica P, Sibilia V, Pagani F, Cazzamalli E (1989) Effects of age on binding sites for calcitonin gene-related peptide in the rat central nervous system. Neurosci Lett 102:20–26

    Google Scholar 

  • Gurwitz D, Egozi Y, Henis YI, Kloog Y, Sokolovsky M (1987) Agonist and antagonist binding to rat muscarinic receptors: influence of aging. Neurobiol Aging 8:115–122

    Google Scholar 

  • Heimer L, Alheid GF, Zaborszky L (1985) Basal ganglia. In: Paxinos G (ed) The rat nervous system, vol 1. Academic Press, Sydney New York London, pp 37–86

    Google Scholar 

  • Hoeffding V, Feldman ML (1988) Changes with age in the morphology of the cochlear nerve in rats: light microscopy. J Comp Neurol 276:537–546

    Google Scholar 

  • Issa AM, Rowe W, Gauthier S, Meaney J (1990) Hypothalamicpituitary-adrenal activity in aged, cognitively impaired and cognitively unimpaired rats. J Neurosci 10:3247–3254

    Google Scholar 

  • Joseph JA, Roth GS (1983) Age-related alterations in dopaminergic mechanisms. In: Samuel D, Algeri S, Gershon S, Grimm VE, Toffano G (eds) Aging of the brain. Raven Press, New York, pp 245–256

    Google Scholar 

  • Joseph JA, Berger RE, Engel BT, Roth GS (1978) Age-related changes in the nigrostriatum: a behavioural and biochemical analysis. J Gerontol 33:643–649

    Google Scholar 

  • Kadar T, Silbermann M, Brandeis R, Levy A (1990) Age-related structural changes in the rat hippocampus: correlation with working memory deficiency. Brain Res 512:113–120

    Google Scholar 

  • Karnowsky MJ, Roots L (1964) A “direct coloring” thiocholine method for choline esterase. J Histochem Cytochem 12:219–221

    Google Scholar 

  • Keithley EM, Feldman ML (1979) Spiral ganglion cell counts in an age-graded series of rat cochleas. J Comp Neurol 188:429–442

    Google Scholar 

  • Keithley EM, Feldman ML (1982) Hair cell counts in an age-graded series of rat cochleas. Hear Res 8:249–262

    Google Scholar 

  • Kennedy C, Des Rosiers MH, Jehle JW, Reivich M, Sharp F, Sokoloff L (1975) Mapping of functional neuronal pathways by autoradiographic survey of local metabolic rate with [14C]deoxyglucose. Science 187:850–853

    Google Scholar 

  • Kugler P, Vogel S, Gehm M (1988) Quantitative succinate dehydrogenase histochemistry in the hippocampus of aged rats. Histochemistry 88:299–307

    Google Scholar 

  • Lai YL, Jacoby RO, Jones AM (1978) Age-related and light associated retinal changes in Fischer rats. Invest Ophthalmol Visual Res 17:634–638

    Google Scholar 

  • La Manna JC, Doull G, McCracken K, Harik SI (1983) (Na+-K+)-ATP-ase activity and ouabain binding sites in the cerebral cortex of young and aged Fischer-344 rats. Gerontology 29:242–247

    Google Scholar 

  • Landfield PW, Rose S, Sandles L, Wohlstadter TC, Lynch G (1977) Patterns of astroglial hypertrophy and neuronal degeneration in the hippocampus of aged, memory-deficient rats. J Gerontol 32:3–12

    Google Scholar 

  • Lippa AS, Loullis CC, Rotrosen J, Cordasco DM, Joseph JA (1985) Conformational changes in muscarinic receptors may produce diminished cholinergic transmission and memory deficits in aged rats. Neurobiol Aging 6:317–323

    Google Scholar 

  • London ED, Nespor SM, Ohata M, Rapoport SI (1981) Local cerebral glucose utilization during development and aging of Fischer-344 rats. J Neurochem 37:217–221

    Google Scholar 

  • Luine V, Hearns M (1990) Spatial memory deficits in aged rats: contributions of the cholinergic system assessed by ChAT. Brain Res 523:321–324

    Google Scholar 

  • Marchi M, Paudice P, Raiteri M (1983) Choline uptake, acetylcholine synthesis, and regulation of acetylcholine release through autoreceptors in the aging cortex. In: Samuel D, Algeri S, Gershon S, Grimm VE, Toffano G (eds) Aging of the brain. Raven Press, New York, pp 165–170

    Google Scholar 

  • McCulloch J (1982) Mapping functional alterations in the CNS with (14C)deoxyglucose. In: Iversen LL, Iversen SD, Snyder SH (eds) Handbook of psychopharmacology, vol 15. Plenum Publishing Corp., New York, pp 321–410

    Google Scholar 

  • Miller JA, Zahniser NR (1988) Quantitative autoradiographic analysis of 125I-pindolol binding in Fischer-344 rat brain: changes in beta-adrenergic receptor density with aging. Neurobiol Aging 9:267–272

    Google Scholar 

  • Moretti A, Carfagna N, Trunzo F (1987) Effect of aging on monoamines and their metabolites in the rat brain. Neurochem Res 12:1935–1939

    Google Scholar 

  • Nowak G, Silberberg J (1988) Kinetics of (3H)-prazosin binding to the rat cortex during aging. Pharmacol Biochem Behav 31:505–507

    Google Scholar 

  • Ohata M, Sundaram U, Fredericks WR, London ED, Rapoport SI (1981) Regional cerebral blood flow during development and aging of the rat brain. Brain 104:319–332

    Google Scholar 

  • Olton DS, Becker JT, Handelmann GE (1979) Hippocampus, space, and memory. Behav Brain Res 2:313–365

    Google Scholar 

  • Ordy JM, Brizzee KR, Kaack B, Hansche J (1978) Age differences in short-term memory and cell loss in the cortex of the rat. Gerontology 24:276–285

    Google Scholar 

  • Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic Press, New York

    Google Scholar 

  • Perry EK et al. (1985) Cholinergic correlates of cognitive impairments in Parkinson's disease: comparisons with Alzheimer's disease. J Neurol Neurosurg Psychiat 4:413–421

    Google Scholar 

  • Pedigo NW, Minor LD, Krumrei TN (1984) Cholinergic drug effects and brain muscarinic receptor binding in aged rats. Neurobiol Aging 5:227–233

    Google Scholar 

  • Pradhan SH (1980) Central neurotransmitters and aging. Life Sci 26:1643–1656

    Google Scholar 

  • Rapoport SI (1983) Session 6: summary and discussion. In: Katzman R (ed) Banbury Report 15:Biological aspects of Alzheimer's disease. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp 329–334

    Google Scholar 

  • Rapoport SI, London ED, Takei H (1982) Brain metabolism and blood flow during development and aging of the Fischer-344 rat. Exp Brain Res 5[Suppl]:86–101

    Google Scholar 

  • Rapoport SI, Duara R, London ED, Margolin RA, Schwartz M, Cutler NR, Partanen M, Shinowara NL (1983) Glucose metabolism of the aging nervous system. In: Samuel D, Algeri S, Gershon S, Grimm VE, Toffano G (eds) Aging of the brain. Raven Press, New York, pp 111–121

    Google Scholar 

  • Sachs L (1978) Angewandte Statistik. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Savaki HE, Davidsen L, Smith C, Sokoloff L (1980) Measurement of free glucose turnover in the brain. J Neurochem 35:495–502

    Google Scholar 

  • Schardein JL, Lucas JA, Fitzgerald JE (1975) Retinal dystrophy in Sprague-Dawley rats. Lab Anim Sci 25:323–326

    Google Scholar 

  • Scheff SW, Anderson KJ, DeKosky ST (1985) Strain comparison of synaptic density in hippocampal CA1 of aged rats. Neurobiol Aging 6:29–34

    Google Scholar 

  • Schlicker E, Betz R, Gothert M (1989) Investigation into the age-dependence of release of serotonin and noradrenaline in the rat brain cortex and of autoreceptor-mediated modulation of release. Neuropharmacology 28:811–815

    Google Scholar 

  • Schuurman T, Horváth E, Spencer DG, Traber J (1986) Old rats: an animal model for senile dementia. In: Bes et al. (eds) Senile dementias: early detection. John Libby Eurotext, London Paris, pp 624–630

    Google Scholar 

  • Schwartz WJ, Sharp FR (1978) Autoradiographic maps of regional glucose consumption in resting, awake rats using (14C)2-deoxyglucose. J Comp Neurol 177:335–360

    Google Scholar 

  • Shinowara NL, London ED, Rapoport SI (1982) Changes in retinal morphology and glucose utilization in aging albino rats. Exp Eye Res 34:517–530

    Google Scholar 

  • Simpson GV, Knight RT, Brailowksy S, Prospero-Garcia O, Scabini D (1985) Altered peripheral and brainstem auditory functions in aged rats. Brain Res 348:28–35

    Google Scholar 

  • Sirvio J, Valjykka A, Jolkkonen J, Hervonen A, Riekkinen PJ (1988) Cholinergic enzym activities and muscarinic binding sites in the cerebral cortex of rats of different age and sex. Comp Biochem Physiol C 90:245–248

    Google Scholar 

  • Smith G (1988) Animal models of Alzheimer's disease: experimental cholinergic denervation. Brain Res Rev 13:103–118

    Google Scholar 

  • Smith CB, Sokoloff L (1982) Age-related changes in local glucose utilization in the brain. Exp Brain Res 5[Suppl]:76–85

    Google Scholar 

  • Smith CB, Goochee C, Rapoport SI, Sokoloff L (1980) Effects of ageing on the local rates of cerebral glucose utilization in the rat. Brain 103:351–363

    Google Scholar 

  • Sokoloff L (1977) Relation between physiological function and energy metabolism in the central nervous system. J Neurochem 29:13–26

    Google Scholar 

  • Sokoloff L (1982) The radioactive deoxyglucose method: theory, procedure, and applications for the measurement of local cerebral glucose utilization in the central nervous system. Adv Neurochem 4:1–82

    Google Scholar 

  • Sokoloff L (1983) Measurement of local cerebral glucose utilization in the central nervous system and its relationship to local functional activity. In: Lajtha A (ed) Handbook of neurochemistry, 2nd edn., vol 3. Plenum Press, New York, pp 225–257

    Google Scholar 

  • Sokoloff L, Reivich M, Kennedy C, Des Rosiers MH, Patlak CS, Pettigrew KD, Sakurada O, Shinohara M (1977) The (14C)deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J Neurochem 28:897–917

    Google Scholar 

  • Soncrant TT (1990) Age-associated functional impairments of specific neurotransmitter systems: detection by pharmacological brain metabolism studies and criteria for design of human investigations. Int J Clin Pharmacol Res 10:27–47

    Google Scholar 

  • Soncrant TT, Holloway HW, Greig NH, Rapoport SI (1989) Regional brain metabolic responsivity to the muscarinic cholinergic agonist arecoline is similar in young and aged Fischer-344 rats. Brain Res 487:255–266

    Google Scholar 

  • Springer JE, Tayrien MW, Loy R (1987) Regional analysis of age-related changes in the cholinergic system of the hippocampal formation and basal forebrain of the rat. Brain Res 407:180–184

    Google Scholar 

  • Stein DG, Mufson EJ (1979) Tumor induced brain damage in rats: implications for behavioral and anatomical studies with aging animals. Exp Aging Res 5:537–547

    Google Scholar 

  • Stephan H (1975) Allocortex. In: Bargmann W (ed) Handbuch der mikroskopischen Anatomic des Menschen, 4. Bd., Teil 9. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Strong R, Hicks P, Hsu L, Bartus RT, Enna SJ (1980) Age-related alterations in the rodent brain cholinergic system and behavior. Neurobiol Aging 1:59–63

    Google Scholar 

  • Tack W, Wree A, Schleicher A (1989) Local cerebral glucose utilization in the hippocampus of old rats. Histochemistry 92:413–419

    Google Scholar 

  • Takei H, Fredericks WR, London ED, Rapoport SI (1983) Cerebral blood flow and oxidative metabolism in conscious Fischer-344 rats of different ages. J Neurochem 40:801–805

    Google Scholar 

  • Takei H, Fredericks WR, Rapoport SI (1986) The lumped constant in the deoxyglucose procedure declines with age in Fischer-344 rats. J Neurochem 46:931–938

    Google Scholar 

  • Victoria J, Andrés A, Satrústegui J, Machado A (1981) Age-related changes in enzyme activities of rat brain. Neurochem Res 6:127–137

    Google Scholar 

  • Waller SB, London ED (1989) Choline acetyltransferase activity and muscarinic binding in brain regions of aging Fischer-344 rats. Neurochem Int 14:493–490

    Google Scholar 

  • Watanabe H (1987a) Substrain differences of age-related changes in in vivo dopamine synthesis in the striatum and nucleus accumbens of the rat brain. J Pharmacobiodyn 10:317–320

    Google Scholar 

  • Watanabe H (1987b) Differential decrease in the rate of dopamine synthesis in several dopaminergic neurons of aged rat brain. Exp Gerontol 22:17–25

    Google Scholar 

  • Weiland NG, Wise PM (1986) Effects of age on β1- and β2-adrenergic receptors in the brain assessed by quantitative autoradiography. Brain Res 398:305–312

    Google Scholar 

  • Whitehouse PJ, Price DL, Clark AW, Coyle JT, DeLong MR (1981) Alzheimer's disease: evidence for selective loss of cholinergic neurons in the nucleus basalis. Ann Neurol 10:12–126

    Google Scholar 

  • Wise PM, Walovitch RC, Cohen IR, Weiland NG, London ED (1987) Diurnal rhythmicity and hypothalamic deficits in glucose utilization in aged ovariectomized rats. J Neurosci 7:3469–3473

    Google Scholar 

  • Wree A (1990) Prinziples of the 2-deoxyglucose method for the determination of the local cerebral glucose utilization. Eur J Morphol 28:132–138

    Google Scholar 

  • Wree A, Schleicher A (1988) The determination of the local cerebral glucose utilization with the 2-deoxyglucose method. Histochemistry 90:109–121

    Google Scholar 

  • Wree A, Zilles K, Schleicher A, Horváth E, Traber J (1987) Effect of the 5-HT1A-receptor agonist ipsapirone on the local cerebral glucose utilization of the rat hippocampus. Brain Res 436:283–290

    Google Scholar 

  • Wree A, Schleicher A, Zilles K, Beck T (1988) Local cerebral glucose utilization in the Ammon's horn and dentate gyrus of the rat brain. Histochemistry 88:415–426

    Google Scholar 

  • Wree A, Zilles K, Schleicher A (1990) Local cerebral glucose utilization in the neocortical areas of the rat brain. Anat Embryol 181:603–614

    Google Scholar 

  • Zilles K (1985) The cerebral cortex of the rat. A stereotaxic atlas. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Zilles K (1990) Anatomy of the neocortex. Cytoarchitecture and myeloarchitecture. In: Kolb B, Tees RC (eds) The cerebral cortex of the rat. MIT Press, Cambridge, pp 77–112

    Google Scholar 

  • Zilles K, Wree A (1985) Cortex: Areal and luminar structure. In: Paxinos G (ed) The rat nervous system, vol 1. Academic Press, Sydney New York London, pp 375–416

    Google Scholar 

  • Zilles K, Wree A, Schleicher A, Divac I (1985) The monocular and binocular subfileds of the rat's primary visual cortex. A quantitative morphological approach. J Comp Neurol 226:391–402

    Google Scholar 

  • Zilles K, Schleicher A, Rath M, Glaser T, Traber J (1986) quantitative autoradiography of transmitter binding sites with an image analyzer. J Neurosci Methods 18:207–220

    Google Scholar 

  • Zilles K, Wree A, Dausch ND (1990) Anatomy of the neocortex: Neurochemical organization. In: Kolb B, Tees RC (eds) The cerebral cortex of the rat. MIT Press, Cambridge, pp 113–150

    Google Scholar 

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  1. Anatomisches Institut der Universität Würzburg, Koellikerstrasse 6, W-8700, Würzburg, Federal Republic of Germany

    A. Wree

  2. Anatomisches Institut der Universität Köln, Joseph-Stelzmann-Strasse 9, W-5000, Köln 41, Federal Republic of Germany

    C. Kaever, B. Birgel, A. Schleicher & K. Zilles

  3. Institut für Neurobiologie, Troponwerke, Berliner Strasse 156, W-5000, Köln 80, Federal Republic of Germany

    E. Horvath

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Wree, A., Kaever, C., Birgel, B. et al. Local cerebral glucose utilization in the brain of old, learning impaired rats. Histochemistry 95, 591–603 (1991). https://doi.org/10.1007/BF00266747

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