Advertisement
Original article| Volume 61, ISSUE 5, P640-652, March 01, 2007

Parvalbumin Neurons in the Entorhinal Cortex of Subjects Diagnosed With Bipolar Disorder or Schizophrenia

  • Harry Pantazopoulos
    Affiliations
    Translational Neuroscience Laboratory, McLean Hospital, Belmont, Massachusetts
    Search for articles by this author
  • Nicholas Lange
    Affiliations
    Neurostatistics Laboratory, McLean Hospital, Belmont, Massachusetts

    Department of Psychiatry, Harvard Medical School, Boston, Massachusetts

    Department of Biostatistics Harvard School of Public Health, Boston, Massachusetts.
    Search for articles by this author
  • Ross J. Baldessarini
    Affiliations
    Neuropharmacology Laboratory, McLean Hospital, Belmont, Massachusetts

    Department of Psychiatry, Harvard Medical School, Boston, Massachusetts

    Neuroscience Program, Harvard Medical School, Boston, Massachusetts
    Search for articles by this author
  • Sabina Berretta
    Correspondence
    Address reprint requests to Sabina Berretta, M.D., MRC 3 - McLean Hospital, 115 Mill Street, Belmont, MA 02478
    Affiliations
    Translational Neuroscience Laboratory, McLean Hospital, Belmont, Massachusetts

    Department of Psychiatry, Harvard Medical School, Boston, Massachusetts
    Search for articles by this author
Published:September 04, 2006DOI:https://doi.org/10.1016/j.biopsych.2006.04.026

      Background

      Growing evidence indicates that the entorhinal cortex (ECx) might be affected in schizophrenia (SZ) and bipolar disorder (BD). To test whether distinct interneuronal subpopulations might be altered, numbers of parvalbumin-immunoreactive (PVB-IR) neurons were measured in the ECx of BD and SZ subjects. These neurons play a pivotal role within ECx intrinsic circuits.

      Methods

      Numbers, numerical density, and soma size of PVB-IR neurons were measured in the ECx of normal control (n = 16), BD (n = 10), and SZ (n = 10) subjects. The volume of the ECx was measured in Nissl-stained sections.

      Results

      In BD, decreases of total numbers (p = .02) and numerical densities (p = .01) of PVB-IR neurons were detected in the ECx. Within distinct subregions, reductions were detected in the superficial layers of the lateral (p = .02), intermediate (p = .04), and caudal (p = .01) ECx. In SZ, total numbers and numerical densities were not altered. A reduction of soma size was present in the intermediate ECx (p = .01). Volume was unaffected in either disorder.

      Conclusions

      In BD, a decrease of PVB-IR neurons may alter intrinsic inhibitory networks within the superficial layers of the ECx. The likely consequence is a disruption of integration and transfer of information from the cerebral cortex to the hippocampus.

      Key Words

      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

        • Abercrombie M.
        Estimation of nuclear population from microtome sections.
        Anat Rec. 1946; 94: 239-247
        • Akbarian S.
        • Kim J.J.
        • Potkin S.G.
        • Hagman J.O.
        • Tafazzoli A.
        • Bunney Jr, W.E.
        • Jones E.G.
        Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics.
        Arch Gen Psychiatry. 1995; 52: 258-266
        • Akil M.
        • Lewis D.A.
        Cytoarchitecture of the entorhinal cortex in schizophrenia.
        Am J Psychiatry. 1997; 154: 1010-1012
        • Altshuler L.L.
        • Bartzokis G.
        • Grieder T.
        • Curran J.
        • Mintz J.
        Amygdala enlargement in bipolar disorder and hippocampal reduction in schizophrenia: an MRI study demonstrating neuroanatomic specificity.
        Arch Gen Psychiatry. 1998; 55: 663-664
        • Arnold S.E.
        The medial temporal lobe in schizophrenia.
        J Neuropsychiatry Clin Neurosci. 1997; 9: 460-470
        • Arnold S.E.
        • Franz B.R.
        • Gur R.C.
        • Gur R.E.
        • Shapiro R.M.
        • Moberg P.J.
        • Trojanowski J.Q.
        Smaller neuron size in schizophrenia in hippocampal subfields that mediate cortical-hippocampal interactions.
        Am J Psychiatry. 1995; 152: 738-748
        • Arnold S.E.
        • Hyman B.T.
        • Van Hoesen G.W.
        • Damasio A.R.
        Some cytoarchitectural abnormalities of the entorhinal cortex in schizophrenia.
        Arch Gen Psychiatry. 1991; 48: 625-632
        • Bachus S.E.
        • Hyde T.M.
        • Herman M.M.
        • Egan M.F.
        • Kleinman J.E.
        Abnormal cholecystokinin mRNA levels in entorhinal cortex of schizophrenics.
        J Psychiatr Res. 1997; 31: 233-256
        • Bakchine S.
        • Lacomblez L.
        • Benoit N.
        • Parisot D.
        • Chain F.
        • Lhermitte F.
        Manic-like state after bilateral orbitofrontal and right temporoparietal injury: Efficacy of clonidine.
        Neurology. 1989; 39: 777-781
        • Baker N.J.
        • Staunton M.
        • Adler L.E.
        • Gerhardt G.A.
        • Drebing C.
        • Waldo M.
        • et al.
        Sensory gating deficits in psychiatric inpatients: relation to catecholamine metabolites in different diagnostic groups.
        Biol Psychiatry. 1990; 27: 519-528
        • Baldessarini R.J.
        • Tarazi F.I.
        Pharmacotherapy of psychosis and mania.
        in: Brunton L.L. Lazo J.S. Parker K.L. Goodman and Gilman’s The Pharmacological Basis of Therapeutics. 11th ed. McGraw-Hill Press, New York1995: 461-500
        • Bartha R.
        • Williamson P.C.
        • Drost D.J.
        • Malla A.
        • Carr T.J.
        • Cortese L.
        • et al.
        Measurement of glutamate and glutamine in the medial prefrontal cortex of never-treated schizophrenic patients and healthy controls by proton magnetic resonance spectroscopy.
        Arch Gen Psychiatry. 1997; 54: 959-965
        • Beasley C.
        • Zhang Z.
        • Patten I.
        • Reynolds G.
        Selective deficits in prefrontal cortical GABAergic neurons in schizophrenia defined by the presence of calcium-binding proteins.
        Biol Psychiatry. 2002; 52: 708
        • Beasley C.L.
        • Reynolds G.P.
        Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics.
        Schizophr Res. 1997; 24: 349-355
        • Benes F.M.
        Altered glutamatergic and GABAergic mechanisms in the cingulate cortex of the schizophrenic brain.
        Arch Gen Psychiatry. 1995; 52: 1015-1018
        • Benes F.M.
        • Berretta S.
        Amygdalo-Entorhinal Inputs to the Hippocampal Formation in Relation to Schizophrenia.
        Ann N Y Acad Sci. 2000; 911: 293-304
        • Benes F.M.
        • Berretta S.
        Gabaergic interneurons.
        Neuropsychopharmacology. 2001; 25: 1-27
        • Benes F.M.
        • Kwok E.W.
        • Vincent S.L.
        • Todtenkopf M.S.
        A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressive.
        Biol Psychiatry. 1998; 44: 88-97
        • Benes F.M.
        • Lange N.
        Two-dimensional versus three-dimensional cell counting: A practical perspective.
        Trends Neurosci. 2001; 24: 11-17
        • Benes F.M.
        • McSparren J.
        • Bird E.D.
        • SanGiovanni J.P.
        • Vincent S.L.
        Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients.
        Arch Gen Psychiatry. 1991; 48: 996-1001
        • Benes F.M.
        • Todtenkopf M.S.
        • Logiotatos P.
        • Williams M.
        Glutamate decarboxylase(65)-immunoreactive terminals in cingulate and prefrontal cortices of schizophrenic and bipolar brain.
        J Chem Neuroanat. 2000; 20: 259-269
        • Benes F.M.
        • Vincent S.L.
        • Alsterberg G.
        • Bird E.D.
        • SanGiovanni J.P.
        Increased GABAA receptor binding in superficial layers of cingulate cortex in schizophrenics.
        J Neurosci. 1992; 12: 924-929
        • Benes F.M.
        • Vincent S.L.
        • Marie A.
        • Khan Y.
        Up-regulation of GABAA receptor binding on neurons of the prefrontal cortex in schizophrenic subjects.
        Neuroscience. 1996; 75: 1021-1031
        • Benes F.M.
        • Vincent S.L.
        • Todtenkopf M.
        The density of pyramidal and nonpyramidal neurons in anterior cingulate cortex of schizophrenic and bipolar subjects.
        Biol Psychiatry. 2001; 50: 395-406
        • Benes F.M.
        • Wickramasinghe R.
        • Vincent S.L.
        • Khan Y.
        • Todtenkopf M.
        Uncoupling of GABA-A and benzodiazepine receptor binding activity in the hippocampal formation of schizophrenic brain.
        Brain Res. 1997; 755: 121-129
        • Berdel B.
        • Morys J.
        Expression of calbindin-D28k and parvalbumin during development of rat’s basolateral amygdaloid complex.
        Int J Dev Neurosci. 2000; 18: 501-513
        • Blumberg H.P.
        • Charney D.S.
        • Krystal J.H.
        Frontotemporal neural systems in bipolar disorder.
        Semin Clin Neuropsychiatry. 2002; 7: 243-254
        • Blumberg H.P.
        • Kaufman J.
        • Martin A.
        • Whiteman R.
        • Zhang J.H.
        • Gore J.C.
        • et al.
        Amygdala and hippocampal volumes in adolescents and adults with bipolar disorder.
        Arch Gen Psychiatry. 2003; 60: 1201-1208
        • Blumberg H.P.
        • Stern E.
        • Ricketts S.
        • Martinez D.
        • de Asis J.
        • White T.
        • et al.
        Rostral and orbital prefrontal cortex dysfunction in the manic state of bipolar disorder.
        Am J Psychiatry. 1999; 156: 1986-1988
        • Bogerts B.
        [Neuropathology of schizophrenias].
        Fortschr Neurol Psychiatr. 1984; 52: 428-437
        • Bogerts B.
        • Meertz E.
        • Schonfeldt-Bausch R.
        Basal ganglia and limbic system pathology in schizophrenia.
        Arch Gen Psychiatry. 1985; 42: 784-791
        • Broadbelt K.
        • Byne W.
        • Jones L.B.
        Evidence for a decrease in basilar dendrites of pyramidal cells in schizophrenic medial prefrontal cortex.
        Schizophr Res. 2002; 58: 75-81
        • Burwell R.D.
        • Amaral D.G.
        Perirhinal and postrhinal cortices of the rat: Interconnectivity and connections with the entorhinal cortex.
        J Comp Neurol. 1998; 391: 293-321
        • Bussiere T.
        • Friend P.D.
        • Sadeghi N.
        • Wicinski B.
        • Lin G.I.
        • Bouras C.
        • et al.
        Stereologic assessment of the total cortical volume occupied by amyloid deposits and its relationship with cognitive status in aging and Alzheimer’s disease.
        Neuroscience. 2002; 112: 75-91
        • Caillard O.
        • Moreno H.
        • Schwaller B.
        • Llano I.
        • Celio M.R.
        • Marty A.
        Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity.
        Proc Natl Acad Sci U S A. 2000; 97: 13372-13377
        • Cavalieri B.
        Geometria degli Indivisibili, Unione Tipografico-Editrice Torinese. 1966 ([original work—Geometria Indivisilibus Continuorum. Torino: Bononi, Typis Clementis Feronji—published 1635].)
        • Chang K.
        • Adleman N.E.
        • Dienes K.
        • Simeonova D.I.
        • Menon V.
        • Reiss A.
        Anomalous prefrontal-subcortical activation in familial pediatric bipolar disorder: a functional magnetic resonance imaging investigation.
        Arch Gen Psychiatry. 2004; 61: 781-792
        • Chard P.S.
        • Bleakman D.
        • Christakos S.
        • Fullmer C.S.
        • Miller R.J.
        Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones.
        J Physiol. 1993; 472: 341-357
        • Cirillo M.A.
        • Seidman L.J.
        Verbal declarative memory dysfunction in schizophrenia: from clinical assessment to genetics and brain mechanisms.
        Neuropsychol Rev. 2003; 13: 43-77
        • Clark L.
        • Kempton M.J.
        • Scarna A.
        • Grasby P.M.
        • Goodwin G.M.
        Sustained attention-deficit confirmed in euthymic bipolar disorder but not in first-degree relatives of bipolar patients or euthymic unipolar depression.
        Biol Psychiatry. 2005; 57: 183-187
        • Coggeshall R.E.
        • Lekan H.A.
        Methods for determining number of cells and synapses: A case for more uniform standard of review.
        J Comp Neurol. 1996; 364: 6-15
        • Cotter D.
        • Hudson L.
        • Landau S.
        Evidence for orbitofrontal pathology in bipolar disorder and major depression, but not in schizophrenia.
        Bipolar Disord. 2005; 7: 358-369
        • Danos P.
        • Baumann B.
        • Bernstein H.G.
        • Franz M.
        • Stauch R.
        • Northoff G.
        • et al.
        Schizophrenia and anteroventral thalamic nucleus: Selective decrease of parvalbumin-immunoreactive thalamocortical projection neurons.
        Psychiatry Res. 1998; 82: 1-10
        • de Curtis M.
        • Pare D.
        The rhinal cortices: A wall of inhibition between the neocortex and the hippocampus.
        Prog Neurobiol. 2004; 74: 101-110
        • Drevets W.C.
        Prefrontal cortical-amygdalar metabolism in major depression.
        Ann N Y Acad Sci. 1999; 877: 614-637
        • Eastwood S.L.
        • Burnet P.W.
        • Harrison P.J.
        Altered synaptophysin expression as a marker of synaptic pathology in schizophrenia.
        Neuroscience. 1995; 66: 309-319
        • Eastwood S.L.
        • Harrison P.J.
        Synaptic pathology in the anterior cingulate cortex in schizophrenia and mood disorders.
        Brain Res Bull. 2001; 55: 569-578
        • Eastwood S.L.
        • Kerwin R.W.
        • Harrison P.J.
        Immunoautoradiographic evidence for a loss of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate-preferring non-N-methyl-D-aspartate glutamate receptors within the medial temporal lobe in schizophrenia.
        Biol Psychiatry. 1997; 41: 636-643
        • El-Badri S.M.
        • Ashton C.H.
        • Moore P.B.
        • Marsh V.R.
        • Ferrier I.N.
        Electrophysiological and cognitive function in young euthymic patients with bipolar affective disorder.
        Bipolar Disord. 2001; 3: 79-87
        • Eyles D.W.
        • McGrath J.J.
        • Reynolds G.P.
        Neuronal calcium-binding proteins and schizophrenia.
        Schizophr Res. 2002; 57: 27-34
        • Falkai P.
        • Bogerts B.
        • Rozumek M.
        Limbic pathology in schizophrenia: The entorhinal region- -a morphometric study.
        Biol Psychiatry. 1988; 24: 515-521
        • Falkai P.
        • Schneider-Axmann T.
        • Honer W.G.
        Entorhinal cortex pre-alpha cell clusters in schizophrenia: Quantitative evidence of a developmental abnormality.
        Biol Psychiatry. 2000; 47: 937-943
        • Feighner J.P.
        • Robins E.
        • Guze S.B.
        Diagnostic criteria for use in psychiatric research.
        Arch Gen Psychiatry. 1972; 26: 57-63
        • Goldsmith S.K.
        • Shapiro R.M.
        • Joyce J.N.
        Disrupted pattern of D2 dopamine receptors in the temporal lobe in schizophrenia.
        Arch Gen Psychiatry. 1997; 54: 649-658
        • Grateron L.
        • Cebada-Sanchez S.
        • Marcos P.
        • Mohedano-Moriano A.
        • Insausti A.M.
        • Munoz M.
        • et al.
        Postnatal development of calcium-binding proteins immunoreactivity (parvalbumin, calbindin, calretinin) in the human entorhinal cortex.
        J Chem Neuroanat. 2003; 26: 311-316
        • Grateron L.
        • Insausti A.M.
        • Garci-Bragado F.
        • et al.
        Postnatal development of the human entorhinal cortex.
        in: Witter M.P. Wouterlood F.G. The Parahippocampal Region Organization and role in cognitive function. Oxford University Press, New York2002
        • Guidotti A.
        • Pesold C.
        • Costa E.
        New neurochemical markers for psychosis: A working hypothesis of their operation.
        Neurochem Res. 2000; 25 ([In Process Citation]): 1207-1218
        • Guillery R.W.
        • Herrup K.
        Quantification without pontification: Choosing a method for counting objects in sectioned tissues.
        J Comp Neurol. 1997; 386: 2-7
        • Heckers S.
        • Rauch S.L.
        • Goff D.
        • Savage C.R.
        • Schacter D.L.
        • Fischman A.J.
        • Alpert N.M.
        Impaired recruitment of the hippocampus during conscious recollection in schizophrenia.
        Nature Neuroscience. 1998; 1: 318-323
        • Heckers S.
        • Weiss A.P.
        • Alpert N.M.
        • Schacter D.L.
        Hippocampal and brain stem activation during word retrieval after repeated and semantic encoding.
        Cereb Cortex. 2002; 12: 900-907
        • Hemby S.E.
        • Ginsberg S.D.
        • Brunk B.
        • Arnold S.E.
        • Trojanowski J.Q.
        • Eberwine J.H.
        Gene expression profile for schizophrenia: discrete neuron transcription patterns in the entorhinal cortex.
        Arch Gen Psychiatry. 2002; 59: 631-640
        • Insausti R.
        • Amaral D.G.
        • Cowan W.M.
        The entorhinal cortex of the monkey: II.
        J Comp Neurol. 1987; 264: 356-395
        • Insausti R.
        • Amaral D.G.
        • Cowan W.M.
        The entorhinal cortex of the monkey: III.
        J Comp Neurol. 1987; 264: 396-408
        • Insausti R.
        • Tunon T.
        • Sobreviela T.
        • Insausti A.M.
        • Gonzalo L.M.
        The human entorhinal cortex: A cytoarchitectonic analysis.
        J Comp Neurol. 1995; 355: 171-198
        • Ishikawa M.
        • Mizukami K.
        • Iwakiri M.
        • Asada T.
        Immunohistochemical and immunoblot analysis of gamma-aminobutyric acid B receptor in the prefrontal cortex of subjects with schizophrenia and bipolar disorder.
        Neurosci Lett. 2005; 383: 272-277
        • Ishikawa M.
        • Mizukami K.
        • Iwakiri M.
        • Hidaka S.
        • Asada T.
        GABAA receptor gamma subunits in the prefrontal cortex of patients with schizophrenia and bipolar disorder.
        Neuroreport. 2004; 15: 1809-1812
        • Ishikawa M.
        • Mizukami K.
        • Iwakiri M.
        • Hidaka S.
        • Asada T.
        Immunohistochemical and immunoblot study of GABA(A) alpha1 and beta2/3 subunits in the prefrontal cortex of subjects with schizophrenia and bipolar disorder.
        Neurosci Res. 2004; 50: 77-84
        • Jakob H.
        • Beckmann H.
        Prenatal developmental disturbances in the limbic allocortex in schizophrenics.
        J Neural Transm. 1986; 65: 303-326
        • Jakob H.
        • Beckmann H.
        Circumscribed malformation and nerve cell alterations in the entorhinal cortex of schizophrenics.
        J Neural Transm Gen Sect. 1994; 98: 83-106
        • Johansen F.F.
        • Zimmer J.
        • Baimbridge K.G.
        • Diemer N.H.
        Short-term changes of parvalbumin and calbindin immunoreactivity in the rat hippocampus following cerebral ischemia.
        Neurosci Lett. 1990; 120 (N. Tn): 171-174
        • Jones R.S.G.
        • Buhl E.H.
        Basket-like interneurones in layer II of the enthorinal cortex exhibit powerful NMDA-mediated synaptic excitation.
        Neurosci Lett. 1993; 149: 35-39
        • Joyal C.C.
        • Laakso M.P.
        • Tiihonen J.
        • et al.
        A volumetric MRI study of the entorhinal cortex in first episode neuroleptic-naive schizophrenia.
        Biol Psychiatry. 2002; 51: 1005-1007
        • Kieseppa T.
        • Tuulio-Henriksson A.
        • Haukka J.
        • Van Erp T.
        • Glahn D.
        • Cannon T.D.
        • et al.
        Memory and verbal learning functions in twins with bipolar-I disorder, and the role of information-processing speed.
        Psychol Med. 2005; 35: 205-215
        • Knable M.B.
        • Barci B.M.
        • Webster M.J.
        • Meador-Woodruff J.
        • Torrey E.F.
        Molecular abnormalities of the hippocampus in severe psychiatric illness: Postmortem findings from the Stanley Neuropathology Consortium.
        Mol Psychiatry. 2004; 9: 609-620
        • Kohler C.
        Intrinsic projections of the retrohippocampal region in the rat brain.
        J Comp Neurol. 1985; 236: 504-522
        • Konradi C.
        • Eaton M.
        • MacDonald M.L.
        • Walsh J.
        • Benes F.M.
        • Heckers S.
        Molecular evidence for mitochondrial dysfunction in bipolar disorder.
        Arch Gen Psychiatry. 2004; 61: 300-308
        • Kovalenko S.
        • Bergmann A.
        • Schneider-Axmann T.
        • Ovary I.
        • Majtenyi K.
        • Havas L.
        • et al.
        Regio entorhinalis in schizophrenia: More evidence for migrational disturbances and suggestions for a new biological hypothesis.
        Pharmacopsychiatry. 2003; 36: S158-S161
        • Krimer L.S.
        • Herman M.M.
        • Saunders R.C.
        • Boyd J.C.
        • Hyde T.M.
        • Carter J.M.
        • et al.
        A qualitative and quantitative analysis of the entorhinal cortex in schizophrenia.
        Cereb Cortex. 1997; 7: 732-739
        • Kurachi M.
        Pathogenesis of schizophrenia: Part I.
        Psychiatry Clin Neurosci. 2003; 57: 3-8
        • Lavenex P.
        • Amaral D.G.
        Hippocampal-neocortical interaction: A hierarchy of associativity.
        Hippocampus. 2000; 10: 420-430
        • Law A.J.
        • Weickert C.S.
        • Hyde T.M.
        • Kleinman J.E.
        • Harrison P.J.
        Reduced spinophilin but not microtubule-associated protein 2 expression in the hippocampal formation in schizophrenia and mood disorders: Molecular evidence for a pathology of dendritic spines.
        Am J Psychiatry. 2004; 161: 1848-1855
        • Lee S.H.
        • Rosenmund C.
        • Schwaller B.
        • Neher E.
        Differences in Ca2+ buffering properties between excitatory and inhibitory hippocampal neurons from the rat.
        J Physiol. 2000; 525: 405-418
        • Lewis D.A.
        • Cruz D.A.
        • Melchitzky D.S.
        • Pierri J.N.
        Lamina-specific deficits in parvalbumin-immunoreactive varicosities in the prefrontal cortex of subjects with schizophrenia: Evidence for fewer projections from the thalamus.
        Am J Psychiatry. 2001; 158: 1411-1422
        • Longson D.
        • Deakin J.F.
        • Benes F.M.
        Increased density of entorhinal glutamate-immunoreactive vertical fibers in schizophrenia.
        J Neural Transm. 1996; 103: 503-507
        • Lopez-Tellez J.F.
        • Vela J.
        • del Rio J.C.
        • Ramos B.
        • Baglietto-Vargas D.
        • et al.
        Postnatal development of the alpha1 containing GABAA receptor subunit in rat hippocampus.
        Brain Res Dev Brain Res. 2004; 148: 129-141
        • Magloczky Z.
        • Freund T.F.
        Delayed cell death in the contralateral hippocampus following kainate injection into the CA3 subfield.
        Neuroscience. 1995; 66: 847-860
        • Manaye K.F.
        • Lei D.L.
        • Tizabi Y.
        • Davila-Garcia M.I.
        • Mouton P.R.
        • Kelly P.H.
        Selective neuron loss in the paraventricular nucleus of hypothalamus in patients suffering from major depression and bipolar disorder.
        J Neuropathol Exp Neurol. 2005; 64: 224-249
        • McDonald B.
        • Highley J.R.
        • Walker M.A.
        • Herron B.M.
        • Cooper S.J.
        • Esiri M.M.
        • Crow T.J.
        Anomalous asymmetry of fusiform and parahippocampal gyrus gray matter in schizophrenia: A postmortem study.
        Am J Psychiatry. 2000; 157: 40-47
        • Miettinen M.
        • Koivisto E.
        • Riekkinen P.
        • Miettinen R.
        Coexistence of parvalbumin and GABA in nonpyramidal neurons of the rat entorhinal cortex.
        Brain Res. 1996; 706: 113-122
        • Mikkonen M.
        • Soininen H.
        • Pitkanen A.
        Distribution of parvalbumin-, calretinin-, and calbindin-D28k-immunoreactive neurons and fibers in the human entorhinal cortex.
        J Comp Neurol. 1997; 388: 64-88
        • Mizukami K.
        • Ishikawa M.
        • Hidaka S.
        • Iwakiri M.
        • Sasaki M.
        • Iritani S.
        Immunohistochemical localization of GABAB receptor in the entorhinal cortex and inferior temporal cortex of schizophrenic brain.
        Prog Neuropsychopharmacol Biol Psychiatry. 2002; 26: 393-396
        • Olincy A.
        • Martin L.
        Diminished suppression of the P50 auditory evoked potential in bipolar disorder subjects with a history of psychosis.
        Am J Psychiatry. 2005; 162: 43-49
        • Pantazopoulos H.
        • Stone D.
        • Walsh J.
        • Benes F.M.
        Differences in the cellular distribution of D1 receptor mRNA in the hippocampus of bipolars and schizophrenics.
        Synapse. 2004; 54: 147-155
        • Phillips M.L.
        • Drevets W.C.
        • Rauch S.L.
        • Lane R.
        Neurobiology of emotion perception II: Implications for major psychiatric disorders.
        Biol Psychiatry. 2003; 54: 515-528
        • Pierri J.N.
        • Volk C.L.
        • Auh S.
        • Sampson A.
        • Lewis D.A.
        Decreased somal size of deep layer 3 pyramidal neurons in the prefrontal cortex of subjects with schizophrenia.
        Arch Gen Psychiatry. 2001; 58: 466-473
        • Rajkowska G.
        Cell pathology in bipolar disorder.
        Bipolar Disord. 2002; 4: 105-116
        • Rajkowska G.
        • Halaris A.
        • Selemon L.D.
        Reductions in neuronal and glial density characterize the dorsolateral prefrontal cortex in bipolar disorder.
        Biol Psychiatry. 2001; 49: 741-752
        • Reynolds G.P.
        • Abdul-Monim Z.
        • Neill J.C.
        • Zhang Z.J.
        Calcium binding protein markers of GABA deficits in schizophrenia–postmortem studies and animal models.
        Neurotox Res. 2004; 6: 57-61
        • Reynolds G.P.
        • Beasley C.L.
        GABAergic neuronal subtypes in the human frontal cortex - development and deficits in schizophrenia.
        J Chem Neuroanat. 2001; 22: 95-100
        • Reynolds G.P.
        • Beasley C.L.
        • Zhang Z.J.
        Understanding the neurotransmitter pathology of schizophrenia: selective deficits of subtypes of cortical GABAergic neurons.
        J Neural Transm. 2002; 109: 881-889
        • Reynolds G.P.
        • Czudek C.
        • Andrews H.B.
        Deficit and hemispheric asymmetry of GABA uptake sites in the hippocampus in schizophrenia.
        Biol Psychiatry. 1990; 27: 1038-1044
        • Saccuzzo D.P.
        • Braff D.L.
        Information-processing abnormalities: Trait- and state-dependent components.
        Schizophr Bull. 1986; 12: 447-459
        • Saunders R.C.
        • Rosene D.L.
        A comparison of the efferents of the amygdala and the hippocampal formation in the rhesus monkey: I.
        J Comp Neurol. 1988; 271: 153-184
        • Schwaller B.
        • Meyer M.
        • Schiffmann S.
        ‘New’ functions for ‘old’ proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology.
        Cerebellum. 2002; 1: 241-258
        • Sewards T.V.
        • Sewards M.A.
        Input and output stations of the entorhinal cortex: superficial vs. deep layers or lateral vs. medial divisions?.
        Brain Res Brain Res Rev. 2003; 42: 243-251
        • Shenton M.E.
        • Dickey C.C.
        • Frumin M.
        • McCarley R.W.
        A review of MRI findings in schizophrenia.
        Schizophr Res. 2001; 49: 1-52
        • Simpson M.D.C.
        • Slater P.
        • Slater J.F.
        • Deakin J.F.W.
        • Royston M.C.
        • Skan W.J.
        Reduced GABA uptake sites in the temporal lobe in schizophrenia.
        Neuroscience Lett. 1989; 107: 211-215
        • Soares J.C.
        Contributions from brain imaging to the elucidation of pathophysiology of bipolar disorder.
        Int J Neuropsychopharmacol. 2003; 6: 171-180
        • Sorvari H.
        • Soininen H.
        • Paljarvi L.
        • Karkola K.
        • Pitkanen A.
        Distribution of parvalbumin-immunoreactive cells and fibers in the human amygdaloid complex.
        J Comp Neurol. 1995; 360: 185-212
        • Squire L.R.
        • Stark C.E.
        • Clark R.E.
        The medial temporal lobe.
        Annu Rev Neurosci. 2004; 27: 279-306
        • Starkstein S.E.
        • Fedoroff P.
        • Berthier M.L.
        • Robinson R.G.
        Manic-depressive and pure manic states after brain lesions.
        Biol Psychiatry. 1991; 29: 149-158
        • Strakowski S.M.
        • Delbello M.P.
        • Adler C.M.
        The functional neuroanatomy of bipolar disorder: A review of neuroimaging findings.
        Mol Psychiatry. 2005; 10: 105-116
        • Suzuki W.A.
        • Amaral D.G.
        Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices.
        J Neurosci. 1994; 14: 1856-1877
        • Sweet R.A.
        • Bergen S.E.
        • Sun Z.
        • Sampson A.R.
        • Pierri J.N.
        • Lewis D.A.
        Pyramidal cell size reduction in schizophrenia: Evidence for involvement of auditory feedforward circuits.
        Biol Psychiatry. 2004; 55: 1128-1137
        • Thomas E.A.
        • Dean B.
        • Scarr E.
        • Copolov D.
        • Sutcliffe J.G.
        Differences in neuroanatomical sites of apoD elevation discriminate between schizophrenia and bipolar disorder.
        Mol Psychiatry. 2003; 8: 167-175
        • Todtenkopf M.S.
        • Benes F.M.
        Distribution of glutamate decarboxylase 65 immunoreactive puncta on pyramidal and nonpyramidal neurons in hippocampus of schizophrenic brain.
        Synapse. 1998; 29: 323-332
        • Torrey E.F.
        Studies of individuals with schizophrenia never treated with antipsychotic medications: A review.
        Schizophr Res. 2002; 58: 101-115
        • Torrey E.F.
        • Barci B.M.
        • Webster M.J.
        • Bartko J.J.
        • Meador-Woodruff J.H.
        • Knable M.B.
        Neurochemical markers for schizophrenia, bipolar disorder, and major depression in postmortem brains.
        Biol Psychiatry. 2005; 57: 252-260
        • Tunon T.
        • Insausti R.
        • Ferrer I.
        • Sobreviela T.
        • Soriano E.
        Parvalbumin and calbindin D-28K in the human entorhinal cortex.
        Brain Res. 1992; 589: 24-32
        • Turetsky B.I.
        • Moberg P.J.
        • Roalf D.R.
        • Arnold S.E.
        • Gur R.E.
        Decrements in volume of anterior ventromedial temporal lobe and olfactory dysfunction in schizophrenia.
        Arch Gen Psychiatry. 2003; 60: 1193-1200
        • Vinogradova O.S.
        Hippocampus as comparator: Role of the two input and two output systems of the hippocampus in selection and registration of information.
        Hippocampus. 2001; 11: 578-598
        • Vreugdenhil M.
        • Jefferys J.G.
        • Celio M.R.
        • Schwaller B.
        Parvalbumin-deficiency facilitates repetitive IPSCs and gamma oscillations in the hippocampus.
        J Neurophysiol. 2003; 89: 1414-1422
        • Webster M.J.
        • Knable M.B.
        • O’Grady J.
        • Orthmann J.
        • Weickert C.S.
        Regional specificity of brain glucocorticoid receptor mRNA alterations in subjects with schizophrenia and mood disorders.
        Mol Psychiatry. 2002; 7 (985–994): 924
        • Wilke M.
        • Kowatch R.A.
        • DelBello M.P.
        • Mills N.P.
        • Holland S.K.
        Voxel-based morphometry in adolescents with bipolar disorder: First results.
        Psychiatry Res. 2004; 131: 57-69
        • Witter M.P.
        • Wouterlood F.G.
        • Naber P.A.
        • Van Haeften T.
        Anatomical organization of the parahippocampal-hippocampal network.
        Ann N Y Acad Sci. 2000; 911: 1-24
        • Wolf S.S.
        • Hyde T.M.
        • Saunders R.C.
        • Herman M.M.
        • Weinberger D.R.
        • Kleinman J.E.
        Autoradiographic characterization of neurotensin receptors in the entorhinal cortex of schizophrenic patients and control subjects.
        J Neural Transm Gen Sect. 1995; 102: 55-65
        • Woo T.U.
        • Walsh J.P.
        • Benes F.M.
        Density of glutamic acid decarboxylase 67 messenger RNA-containing neurons that express the N-methyl-D-aspartate receptor subunit NR2A in the anterior cingulate cortex in schizophrenia and bipolar disorder.
        Arch Gen Psychiatry. 2004; 61: 649-657
        • Woo T.U.
        • Whitehead R.E.
        • Melchitzky D.S.
        • Lewis D.A.
        A subclass of prefrontal gamma-aminobutyric acid axon terminals are selectively altered in schizophrenia.
        Proc Natl Acad Sci U S A. 1998; 95: 5341-5346
        • Wouterlood F.
        • Hartig W.
        • Bruckner G.
        • Witter M.
        Parvalbumin-immunoreactive neurons in the entorhinal cortex of the rat: Localization, morphology, connectivity and ultrastructure.
        J Neurocytol. 1995; 24: 135-153
        • Wouterlood F.G.
        Spotlight on the neurons (I): Cell types, local connectivity, microcircuits, and distribution of markers.
        in: Witter M. Wouterlood F. The Parahippocampal Region: Organization and Role in Cognitive Function. Oxford University Press, New York2002: 61-88
        • Zhang Z.J.
        • Reynolds G.P.
        A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia.
        Schizophr Res. 2002; 55: 1-10