Advertisement

Mesolimbic dopaminergic supersensitivity following electrical kindling of the amygdala

  • John G. Csernansky
    Correspondence
    Address reprint requests to Dr. J.G. Csernansky, Psychiatry Service. VA Medical Center, Miranda Avenue 4B2 Palo Alto CA 98304.
    Affiliations
    Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, and the Palo Alto VA Medical Center, Palo Alto, CAUSA
    Search for articles by this author
  • Julia Mellentin
    Affiliations
    Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, and the Palo Alto VA Medical Center, Palo Alto, CAUSA
    Search for articles by this author
  • Linda Beauclair
    Affiliations
    Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, and the Palo Alto VA Medical Center, Palo Alto, CAUSA
    Search for articles by this author
  • Leon Lombrozo
    Affiliations
    Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, and the Palo Alto VA Medical Center, Palo Alto, CAUSA
    Search for articles by this author
      This paper is only available as a PDF. To read, Please Download here.

      Abstract

      Limbic seizures developed in rats following daily electrical stimulation of the basolateral nucleus of the amygdala. Animals were designated as “kindled” after five complete (stage 5) behavioral seizures were observed. A subgroup, designated as “superkindled,” received three additional weeks of electrical stimulations. Kindled rats were significantly subsensitive to the stereotypy-inducing effects of apomorphine, a direct dopamine agonist, compared to controls. Superkindled rats were supersensitive to the effects of apomorphine. However, both kindled and superkindled rats demonstrated an increase in 3H-spiperone βmax values, reflecting dopamine D2-receptor densities, in the nucleus accumbens ipsilateral to the stimulating electrode. The number of interictal spikes recorded from the stimulating amygdaloid electrode during the last week of kindling was correlated with changes in apomorphine sensitivity in individual animals.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Biological Psychiatry
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Ackerman RF
        • Finch DM
        • Bobb TL
        • Engel Jr, J
        Increased glucose metabolism during long-duration recurrent inhibition of hippocampal pyramidal cells.
        J Neurosci. 1984; 4: 251-264
        • Ackerman RF
        • Engel Jr, J
        • Phelps ME
        Identification of seizure-mediating brain structures with the deoxyglucose method: Studies of human epilepsy with positron emission tomography, and animal seizure models with contact autoradiography.
        Adv Neurol. 1986; 44: 921-934
        • Ashton D
        • Leysen JE
        • Wauquier A
        Neurotransmitters and receptor binding in amygdaloid kindled rats: Serotonergic and noradrenergic modulatory effects.
        Life Sci. 1980; 27: 1547-1556
        • Blackwood D
        The role of noradrenaline and dopamine in amygdaloid kindling.
        in: Morselli L Lloyd KG Loscher W Meldrom B Reynolds EN Neurotransmitters, Seizures, and Epilepsy. Raven Press, New York1981: 203-211
        • Burnham WM
        • Racine RJ
        • Okazaki MO
        Kindling mechanisms: II. Biochemical studies.
        in: Wada JA Kindling. Raven Press, New York1986: 283-299
        • Burt DR
        • Creese I
        • Snyder SH
        Properties of 3[H]-haloperidol and 3[H]-dopamine binding associated with dopamine receptors in calf brain membranes.
        Mol Pharmacol. 1976; 12: 800-812
        • Corcoran ME
        Catecholamines and kindling.
        in: Wada JA Kindling. Raven Press, New York1986: 87-104
        • Costall B
        • Naylor RJ
        The role of telencephalic dopaminergic systems in the mediation of apomorphine-stereotyped behaviour.
        Eur J Pharmacol. 1973; 24: 8-24
        • Csernansky JG
        • Holman CA
        • Hollister LE
        Variability and the dopamine hypothesis of schizophrenia.
        Schizophr Bull. 1983; 9: 325-328
        • Csernansky JG
        • Holman CA
        • Bonnet KA
        • Grabowsky K
        • King R
        • Hollister LE
        Dopa-minergic supersensitivity at distant sites following induced epileptic foci.
        Life Sci. 1983; 32: 385-390
        • Csernansky JG
        • Csernansky CA
        • Hollister LE
        Distinct effects of two stresses on the behavioral response to apomorphine.
        Life Sci. 1984; 35: 1513-1518
        • Csernansky JG
        • Csernansky CA
        • Bonnet KA
        • Hollister LE
        Dopaminergic supersensitivity follows ferric chloride-induced limbic seizures.
        Biol Psychiatry. 1985; 20: 723-733
        • Csernansky JG
        • Csernansky CA
        • Glick SA
        • Hollister LE
        Lidocaine kindling is accompanied by an increase in apomorphine stereotypy and mesolimbic dopamine D2 receptor density.
        Psychopharmacol Bull. 1985; 21: 707-711
        • Csernansky CA
        • Csernansky JG
        • Hollister LE
        A comparison between centrifugation and filtration as a means to separate bound and unbound ligand during 3[H]-spiroperidol binding.
        J Pharmacol Meth. 1985; 13: 187-191
        • Dashieff RM
        • Byrne MC
        • Patrone V
        • McNamara JO
        Biochemical evidence of decreased muscarinic cholinergic neuronal communication following amygdala kindled seizures.
        Brain Res. 1981; 206: 233-238
        • Engel J
        • Sharpless NS
        Long-lasting depletion of dopamine in the rat amygdala induced by kindling stimulation.
        Brain Res. 1977; 136: 381-386
        • Farjo IB
        • Blackwood DHR
        Reduction in tyrosine hydroxylase activity in rat amygdala induced by kindling stimulation.
        Brain Res. 1978; 153: 423-426
        • Gee KW
        • Hollinger MA
        • Bowyer JF
        • Killam EK
        Modification of dopaminergic receptor sensitivity in rat brain after amygdaloid kindling.
        Exp Neurol. 1979; 66: 771-777
        • Goddard GV
        • McIntyre DC
        • Leech CK
        A permanent change in brain function resulting from daily electrical stimulation.
        Exp Neurol. 1969; 25: 295-330
        • Konig J
        • Klippel R
        The Rat Brain. A Stereotactic Atlas.
        Robert E. Kreiger, New York1963
        • Lee T
        • Seeman P
        Elevation of brain neuroleptic/dopamine receptors in schizophrenia.
        Am J Psychiatry. 1980; 137: 191-197
        • Lowry OH
        • Rosenbrough NJ
        • Farr AL
        • Randell RJ
        Protein measurement with the folin phenol reagent.
        J Biol Chem. 1951; 193: 265-275
        • Mackay AVP
        • Iversen LL
        • Rossor M
        • Bird EB
        • Arregui A
        • Creese I
        • Snyder SH
        Increased brain dopamine and dopamine receptors in schizophrenia.
        Arch Gen Psychiatry. 1982; 39: 991-997
        • McNamara JO
        Role of neurotransmitters in seizure mechanisms in the kindling model of epilepsy.
        in: Fed Proc. 43. 1984: 2516-2520
        • McNamara JO
        • Peper AM
        • Patrone V
        Repeated seizures induce long-term increase in hippocampal benzodiazepine receptors.
        in: Proc Natl Acad Sci USA. 77. 1980: 3029-3032
        • Meltzer HY
        • Stahl SM
        The dopamine hypothesis of schizophrenia: A review.
        Schizophr Bull. 1976; 2: 19-76
        • Owen F
        • Cross AJ
        • Crow TJ
        • Longden A
        • Poulter M
        • Riley GJ
        Increased dopamine receptor sensitivity in schizophrenia.
        Lancet. 1978; ii: 223-224
        • Post RM
        • Kopanda RT
        Cocaine, kindling, and psychosis.
        Am J Psychiatry. 1976; 133: 627-634
        • Post RM
        • Squillace KM
        • Pert A
        • Sass W
        The effect of amygdala kindling on spontaneous and cocaine-induced motor activity and lidocaine seizures.
        Psychopharmacology. 1981; 72: 189-196
        • Prince DA
        • Wilder BJ
        Control mechanisms in cortical epileptogenic foci: “Surround” inhibition.
        Arch Neurol. 1967; 16: 194-202
        • Racine RJ
        Modification of seizure activity by electrical stimulation: II. Motor seizure.
        Electroencephalogr Clin Neurophysiol. 1972; 32: 281-294
        • Racine RJ
        • McIntyre DC
        • Burnham W
        The kindling model.
        in: Electrophysiology of Epilepsy. Academic, Orlando, FL1984: 153-171
        • Sato M
        • Nakashima T
        • Mitsunobu K
        • Otsuki S
        Correlation between seizure susceptibility and brain catecholamine levels: An experimental study using a kindling preparation.
        Brain Nerve (Tokyo). 1976; 28: 471-477
        • Seeman P
        Brain dopamine receptors.
        Pharmacol Rev. 1980; 32: 229-313
        • Seeman P
        • Ulpian C
        • Bergeron C
        • Riederer P
        • Jellinger K
        • Gabriel E
        • Reynolds GP
        • Tourtellotte WW
        Bimodal distribution of dopamine receptor densities in brains of schizophrenics.
        Science. 1984; 225: 728-731
        • Stevens JR
        An anatomy of schizophrenia?.
        Arch Gen Psychiatry. 1973; 29: 177-189
        • Stevens JR
        • Livermore A
        Kindling of the mesolimbic dopamine system: Animal model of psychosis.
        Neurology. 1978; 28: 36-46
        • Tepper JM
        • Nakamura S
        • Spanis CW
        • Squire LR
        • Young SJ
        • Groves PM
        Subsensitivity of catecholaminergic neurons to direct acting agonists after single or repeated electroconvulsive shock.
        Biol Psychiatry. 1982; 17: 1059-1070
        • Wong DF
        • Wagner HN
        • Tune LE
        • Dannals RF
        • Pearlson GD
        • Links JM
        • Tamminga CA
        • Broussolle P
        • Ravert HT
        • Wilson AA
        • Thomas Toung JK
        • Malat MJ
        • Williams JA
        • O'Tuama LA
        • Snyder SH
        • Kuhar MJ
        • Gjedde A
        Positron emission tomography reveals elevated D2 dopamine receptors in drug-naive schizophrenics.
        Science. 1986; 234: 1558-1563
        • Yim CY
        • Mogenson GJ
        Response of nucleus accumbens neurons to amygdala stimulation and its modification by dopamine.
        Brain Res. 1982; 239: 401-415
        • Yim CY
        • Mogenson GJ
        Mesolimbic dopamine projection modulates amygdala-evoked EPS? in nucleus accumbens neurons: An in vivo study.
        Brain Res. 1986; 369: 347-352