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Potentiation of amphetamine-induced locomotor activity following NMDA-induced retrohippocampal neuronal loss in the rat

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Abstract

The present experiment assessed the locomotor response to a low dose (1 mg/kg) of systemic gemd-amphetamine in rats with cytotoxic lesions of the retrohippocampus (entorhinal and extra-subicular cortices), compared with vehicle-operated shams and unoperated controls. Under spontaneous and saline conditions, both the sham and the lesioned animals were more active than unoperated controls, and they did not differ from each other. Systemic gemd-amphetamine produced increased locomotion in all groups, but this effect was potentiated in animals with retrohippocampal lesions; two control groups did not differ from each other in their response to the drug. The present results are consistent with the suggestion that cell loss within the retrohippocampal region could affect the functional response of nucleus accumbens to amphetamine. The results are discussed in terms of the interaction between the retrohippocampus and nucleus accumbens in the control of mesolimbic dopamine release and the possible implications for schizophrenia.

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References

  • Brog JS, Salyapongse A, Deutch AY, Zahm DS (1993) The patterns of afferent innervation of the core and shell in the “accumbens” part of the rat ventral striatum: immunohistochemical detection of retrograde transported fluoro-gold. J Comp Neurol 338:255–278

    CAS  PubMed  Google Scholar 

  • Burns L, Robbins TW, Everitt BJ (1993) Differential effects of excitotoxic lesions of the basolateral amygdala, ventral subiculum and medial prefrontal cortex on responding with conditioned reinforcement and locomotory activity potentiated by intra-accumbens infusion of gemd-amphetamine. Behav Brain Res 55:167–183

    Google Scholar 

  • Creese I, Iversen SD (1975) The pharmacological and anatomical substrates of the amphetamine response in the rat. Brain Res 83:419–436

    Google Scholar 

  • Csernansky JG, Murphy GM, Faustman WO (1991) Limbic/mesolimbic connections and the pathogenesis of schizophrenia. Biol Psychiatr 30:383–400

    Google Scholar 

  • Danscher G (1981) Histochemical demonstration of heavy metals: a revised version of the sulphide silver method suitable for both light and electromicroscopy. Histochemistry 71:1–16

    Google Scholar 

  • DeFrance JF, Marhand JF, Stanley J, Sikes RW, Chronister RB (1980) Convergence of excitatory amygdaloid and hippocampal input in the nucleus accumbens septi. Brain Res 185:183–186

    Google Scholar 

  • DiChiara G, Tanda G, Fray R, Carboni E (1993) On the preferential release of dopamine in the nucleus accumbens by amphetamine: further evidence obtained by vertically implanted concentric dialysis probes. Psychopharmacology 112:398–402

    Google Scholar 

  • Donzanti BA, Uretsky NJ (1983) Effects of excitatory amino acids on locomotor activity after bilateral microinjection into the rat nucleus accumbens: possible dependence on dopaminergic mechanism. Neuropharmacology 22:971–981

    Google Scholar 

  • Essam WD, McGonigle P, Lucki I (1993) Anatomical differentiation within the nucleus accumbens of the locomotor stimulatory actions of selective dopamine agonists and gemd-amphetamine. Psychopharmacology 112:233–241

    Google Scholar 

  • Fass B (1983) Temporal changes in open-field activity following progressive lesions of entorhinal cortex: evidence for enhanced recovery. Behav Neural Biol 37:108–124

    Google Scholar 

  • Frederickson CJ, Danscher G (1989) Zinc-containing neurons in the hippocampus and related structures. Progr Brain Res 83:71–84

    Google Scholar 

  • Frederickson CJ, Klitenick MA, Manton WI, Kirkpatrick JB (1983) Cytoarchitectonic distribution of zinc in the hippocampus of man and the rat. Brain Res 273:335–339

    Google Scholar 

  • Friston KJ, Liddle PF, Frith CD, Hirsch SR, Frackowiak RSJ (1993) The left medial temporal region and schizophrenia. Brain 115:367–382

    Google Scholar 

  • Frotscher M, Zimmer J (1983) Lesion-induced mossy fibres to the molecular layer of the fascia dentata: identification of postsynaptic granule cells by the Golgi-EM technique. J Comp Neurol 215:299–311

    Google Scholar 

  • Geneser FA, Haug FMS, Danscher G (1974) Distribution of heavy metals in the hippocampal region of the guinea pig. A light microscopic study with the Timm's sulphide silver method. Z Zellforch 147:441–478

    Google Scholar 

  • Gray JA, Feldon J, Rawlins JNP, Hemsley DR, Smith AD (1991) The neuropsychology of schizophrenia. Behav Brain Sci 14:1–84

    Google Scholar 

  • Groenewegen HJ, Room P, Witter MP, Lohman AMH (1982) Cortical afferents of the nucleus accumbens in the cat studied with anterograde and retrograde transport techniques. Neuroscience 7:977–996

    Google Scholar 

  • Groenewegen HJ, Vermeulen-Van der Zee E, Te Kortschot A, Witter MP (1987) Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of PHA-L. Neuroscience 23:103–120

    Google Scholar 

  • Hagan JJ, Verheijck EE, Spigt MH, Ruigt GSF (1992) Behavioural and electrophysiological studies of entorhinal cortex lesions in the rat. Physiol Behav 51:255–266

    Google Scholar 

  • Hannigan JH, Springer JE, Isaacson RE (1984) Differentiation of basal ganglia dopaminergic involvement in behaviour after hippocampectomy. Brain Res 291:83–91

    Google Scholar 

  • Haug FMS (1974) Light microscopic mapping of the hippocampal region, the piriform cortex and the corticomedial amygdaloid nuclei of the rat with Timm's sulphide silver method. Z Anat Entwickl Gesch 145:1–27

    Google Scholar 

  • Hedreen JC, Bacon SJ, Price DL (1985) A modified histochemical technique to visualize acetylcholinesterase-containing axons. J Histochem Cytochem 33:134–140

    Google Scholar 

  • Isaacson RL (1984) Hippocampal damage: effects on dopaminergic systems of the basal ganglia. Int Rev Neurobiol 25:339–359

    Google Scholar 

  • Jarrard LE (1968) Behaviour of hippocampal lesioned rats in home cage and novel situations. Physiol Behav 3:65–70

    Google Scholar 

  • Kelly AE, Domesick VB (1982) The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde and retrograde-HRP study. Neuroscience 7:2321–2335

    Google Scholar 

  • Killcross AS, Robbins TW (1993) Differential effects of intra-accumbens and systemic amphetamine on latent inhibition using an on-baseline, within-subject conditioned suppression paradigm. Psychopharmacology 110:479–489

    Google Scholar 

  • Köhler C (1985) Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex. J Comp Neurol 236:504–522

    Google Scholar 

  • Köhler C, Sundberg H (1977) Locomotor activity and exploratory behaviour after medial entorhinal cortex lesions in the albino rat. Behav Biol 20:419–432

    Google Scholar 

  • Lasher SS, Steward O (1981) The time course of changes in open ield activity following bilateral entorhinal lesions in rats and cats. Behav Neural Biol 32:1–20

    Google Scholar 

  • Laurberg S, Zimmer J (1981) Lesion-induced sprouting of hippocampal mossy fibre collaterals to the fascia dentata in adult rats. J Comp Neurol 200:433–459

    Google Scholar 

  • Liddle PF, Friston KJ, Frith CD, Jones T, Hirsch SR, Frackowiak RSJ (1992) Patterns of cerebral blood flow in schizophrenia. Br J Psychiatr 160:179–186

    Google Scholar 

  • Lynch G, Matthews DA, Mosko S, Parks T, Cotman CW (1972) Induced acetylcholinesterase-rich layer in rat dentate gyrus following entorhinal lesions. Brain Res 42:311–318

    Google Scholar 

  • Mittleman G, LeDuc PA, Whishaw IQ (1993) The role of D1 and D2 receptors in the heightened locomotion induced by direct and indirect dopamine agonists in rats with hippocampal damage: an animal analogue of schizophrenia. Behav Brain Res 55:253–267

    Google Scholar 

  • Newman R, Winans SS (1980) An experimental study of the ventral striatum of the golden hamster. I. Neuronal connections of the nucleus accumbens. J Comp Neurol 191:167–192

    Google Scholar 

  • Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, New York

    Google Scholar 

  • Pennartz CMA, Groenewegen HJ, Lopes da Silva FH (1994) The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog Neurobiol 42:719–761

    Google Scholar 

  • Pennartz CMA, Kitai ST (1991) Hippocampal inputs to identified neurons in an in vivo slice preparation of the rat nucleus accumbens: evidence for feed-forward inhibition. J Neurosci 11:2838–2847

    Google Scholar 

  • Pijnenburg AJJ, Honig WMM, Van der Heyden JAM, van Rossum JM (1976) Effects of chemical stimulation of the mesolimbic dopamine system upon locomotor activity. Eur J Pharmacol 35:45–58

    Google Scholar 

  • Roberts GW (1991) Schizophrenia: a neuropathological perspective. Br J Psychiatr 158:8–17

    Google Scholar 

  • Roberts GW, Horton K (1992) Neuropathology of psychoses: towards a common biology. In: Trimble MR, Bolwig TG (eds) The temporal lobes and the limbic system. Wrightson Biomedical, Petersfield, UK, pp 213–238

    Google Scholar 

  • Robinson TE, Becker JB (1986) Enduring changes in brain and behaviour produced by chronic amphetamine administration: a review and evaluation of animal models of amphetamine psychosis. Brain Res Rev 11:157–198

    Google Scholar 

  • Ross JF, Walsh LL, Grossman SP (1973) Some behavioural effects of entorhinal cortex lesions in albino rats. J Comp Physiol Psychol 85:70–81

    Google Scholar 

  • Sesack SR, Pickel VM (1990) In the rat medial nucleus accumbens, hippocampal and catecholaminergic terminals converge on spiny neurons and are in opposition to each other. Brain Res 527:266–279

    Google Scholar 

  • Shreve PE, Uretsky NJ (1988) Role of quisqualic acid receptors in the hypermotility response produced by the injection of AMPA into the nucleus accumbens. Pharmacol Biochem Behav 30:379–384

    Google Scholar 

  • Solomon PR, Staton DM (1982) Differential effects of microinjections of gemd-amphetamine into the nucleus accumbens or the caudate putamen on the rat's ability to ignore an irrelevant stimulus. Biol Psychiatr 17:743–756

    Google Scholar 

  • Sørensen KE, Witter MP (1983) Entorhinal efferents reach the caudato-putamen. Neurosci Lett 35:259–264

    Google Scholar 

  • Springer HE, Isaacson RL (1982) Catecholamine alterations in basal ganglia after hippocampal lesions. Brain Res 252:185–188

    Google Scholar 

  • Stanfield BB, Cowan WM (1982) The sprouting of septal afferents to the dentate gyrus after lesions of the entorhinal cortex in adult rats. Brain Res 232:162–170

    Google Scholar 

  • Steward O, Loesche J, Horton WC (1977) Behavioral correlates of denervation and reinnervation of the hippocampal formation of the rat: open field activity and cue utilization following bilateral entorhinal cortex lesions. Brain Res Bull 2:41–48

    Google Scholar 

  • Teitelbaum H, Milner P (1963) Activity changes following partial hippocampal lesions in rats. J Comp Physiol Psychol 56:284–289

    Google Scholar 

  • Totterdell S, Smith AD (1989) Convergence of hippocampal and dopaminergic input onto identified neurons in the nucleus accumbens of the rat. J Chem Neuroanat 2:285–298

    Google Scholar 

  • Weiner I, Lubow RE, Feldon J (1988) Disruption of latent inhibition by acute administration of low doses of amphetamine. Pharmacol Biochem Behav 30:871–878

    Google Scholar 

  • West JR, Dewey SL (1984) Mossy fibre sprouting in the fascia dentata after unilateral entorhinal lesions: quantitative analysis using computer-assisted image processing. Neuroscience 13:377–384

    Google Scholar 

  • Whishaw IQ, Mittleman G (1991) Hippocampal modulation of nucleus accumbens: behavioural evidence from amphetamine-induced activity profile. Behav Neural Biol 55:289–306

    Google Scholar 

  • Wilkinson LS, Mittleman G, Torres E, Humby T, Hall FS, Robbins TW (1993) Enhancement of amphetamine-induced locomotor activity and dopamine release in nucleus accumbens following excitotoxic lesion of the hippocampus. Behav Brain Res 55:143–150

    Google Scholar 

  • Witter MP (1989) Connectivity of the rat hippocampus. In: Chan-Palay V, Köhler C (eds) The hippocampus: new vista. (Neurology and neurobiology, vol 52) Liss, New York, pp 53–69

    Google Scholar 

  • Witter MP, Groenewegen HJ (1992) Organization principles of hippocampal connections. In: Trimble MR, Bolwig TG (eds) The temporal lobes and the limbic system. Wrightson Biomedical, Petersfield, UK, pp 37–60

    Google Scholar 

  • Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AHM (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33:161–253

    Article  CAS  PubMed  Google Scholar 

  • Yang CR, Mogenson GJ (1987) Hippocampal signal transmission to the pedunculopontine nucleus and its regulation by dopamine D2 receptors in the nucleus accumbens: an electrophysiological and behavioural study. Neuroscience 23:1041–1055

    Google Scholar 

  • Yee BK, Feldon J, Rawlins JNP (1995) Latent inhibition in rats is abolished by NMDA-induced retrohippocampal cell loss but this lesion effect can be prevented by systemic haloperidol treatment. Behav Neurosci 109:227–240

    Google Scholar 

  • Yung KKL, Bolam JP, Smith AD, Ciliax BJ, Levey AI (1995) Immunocytochemical localisation of D1 and D2 dopamine receptors in the basal ganglia of the rat: light and electron microscopy. Neuroscience 65:709–730

    Google Scholar 

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Yee, B.K., Feldon, J. & Rawlins, J.N.P. Potentiation of amphetamine-induced locomotor activity following NMDA-induced retrohippocampal neuronal loss in the rat. Exp Brain Res 106, 356–364 (1995). https://doi.org/10.1007/BF00241131

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