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Published in: European Archives of Psychiatry and Clinical Neuroscience 6/2013

01-09-2013 | Original Paper

Neuropathological changes in the nucleus basalis in schizophrenia

Authors: M. R. Williams, R. Marsh, C. D. Macdonald, J. Jain, R. K. B. Pearce, S. R. Hirsch, O. Ansorge, S. M. Gentleman, M. Maier

Published in: European Archives of Psychiatry and Clinical Neuroscience | Issue 6/2013

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Abstract

The nucleus basalis has not been examined in detail in severe mental illness. Several studies have demonstrated decreases in glia and glial markers in the cerebral cortex in schizophrenia, familial bipolar disorder and recurrent depression. Changes in neocortical neuron size and shape have also been reported. The nucleus basalis is a collection of large cholinergic neurons in the basal forebrain receiving information from the midbrain and limbic system, projecting to the cortex and involved with attention, learning and memory, and receives regulation from serotonergic inputs. Forty-one cases aged 41–60 years with schizophrenia or major depressive disorder with age-matched controls were collected. Formalin-fixed paraffin-embedded coronal nucleus basalis sections were histologically stained for oligodendrocyte identification with cresyl-haematoxylin counterstain, for neuroarchitecture with differentiated cresyl violet stain and astrocytes were detected by glial fibrillary acid protein immunohistochemistry. Cell density and neuroarchitecture were measured using Image Pro Plus. There were larger NB oval neuron soma in the combined schizophrenia and major depression disorder groups (p = 0.038), with no significant change between controls and schizophrenia and major depression disorder separately. There is a significant reduction in oligodendrocyte density (p = 0.038) in the nucleus basalis in schizophrenia. The ratio of gemistocytic to fibrillary astrocytes showed a greater proportion of the former in schizophrenia (18.1 %) and major depressive disorder (39.9 %) than in controls (7.9 %). These results suggest glial cell abnormalities in the nucleus basalis in schizophrenia possibly leading to cortical-limbic disturbance and subcortical dysfunction.
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Literature
1.
go back to reference Aasen I, Kumari V, Sharma T (2005) Effects of rivastigmine on sustained attention in schizophrenia: an fMRI study. J Clin Psychopharmacol 25:311–317PubMedCrossRef Aasen I, Kumari V, Sharma T (2005) Effects of rivastigmine on sustained attention in schizophrenia: an fMRI study. J Clin Psychopharmacol 25:311–317PubMedCrossRef
2.
go back to reference Afifi M (2007) Gender differences in mental health. Singap Med J 48:385–391 Afifi M (2007) Gender differences in mental health. Singap Med J 48:385–391
3.
go back to reference Amunts VV (2007) Structural asymmetry of the basal nucleus of Meynert in men and women. Neurosci Behav Physiol 37:517–521PubMedCrossRef Amunts VV (2007) Structural asymmetry of the basal nucleus of Meynert in men and women. Neurosci Behav Physiol 37:517–521PubMedCrossRef
4.
go back to reference Bancher C, Paulus W, Paukner K, Jellinger K (1997) Neuropathologic diagnosis of Alzheimer disease: consensus between practicing neuropathologists? Alzheimer Dis Assoc Disord 11:207–219PubMed Bancher C, Paulus W, Paukner K, Jellinger K (1997) Neuropathologic diagnosis of Alzheimer disease: consensus between practicing neuropathologists? Alzheimer Dis Assoc Disord 11:207–219PubMed
5.
go back to reference Bartus RT, Dean RL, Beer B 3rd, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408–414PubMedCrossRef Bartus RT, Dean RL, Beer B 3rd, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408–414PubMedCrossRef
6.
go back to reference Benes FM, Lange N (2001) Two-dimensional versus three-dimensional cell counting: a practical perspective. Trends Neurosci 24:11–17PubMedCrossRef Benes FM, Lange N (2001) Two-dimensional versus three-dimensional cell counting: a practical perspective. Trends Neurosci 24:11–17PubMedCrossRef
7.
go back to reference Bennett JP Jr, Enna SJ, Bylund DB, Gillin JC, Wyatt RJ, Snyder SH (1979) Neurotransmitter receptors in frontal cortex of schizophrenics. Arch Gen Psychiatry 36:927–934PubMedCrossRef Bennett JP Jr, Enna SJ, Bylund DB, Gillin JC, Wyatt RJ, Snyder SH (1979) Neurotransmitter receptors in frontal cortex of schizophrenics. Arch Gen Psychiatry 36:927–934PubMedCrossRef
8.
go back to reference Bilder RM, Wu H, Bogerts B, Degreef G, Ashtari M, Alvir JM, Snyder PJ, Lieberman JA (1994) Absence of regional hemispheric volume asymmetries in first-episode schizophrenia. Am J Psychiatry 151:1437–1447PubMed Bilder RM, Wu H, Bogerts B, Degreef G, Ashtari M, Alvir JM, Snyder PJ, Lieberman JA (1994) Absence of regional hemispheric volume asymmetries in first-episode schizophrenia. Am J Psychiatry 151:1437–1447PubMed
9.
go back to reference Bora E, Veznedaroglu B, Kayahan B (2005) The effect of galantamine added to clozapine on cognition of five patients with schizophrenia. Clin Neuropharmacol 28:139–141PubMedCrossRef Bora E, Veznedaroglu B, Kayahan B (2005) The effect of galantamine added to clozapine on cognition of five patients with schizophrenia. Clin Neuropharmacol 28:139–141PubMedCrossRef
10.
go back to reference Bushong EA, Martone ME, Ellisman MH (2004) Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. Int J Dev Neurosci 22:73–86PubMedCrossRef Bushong EA, Martone ME, Ellisman MH (2004) Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. Int J Dev Neurosci 22:73–86PubMedCrossRef
11.
go back to reference Carnes KM, Fuller TA, Price JL (1990) Sources of presumptive glutamatergic/aspartatergic afferents to the magnocellular basal forebrain in the rat. J Comp Neurol 302:824–852PubMedCrossRef Carnes KM, Fuller TA, Price JL (1990) Sources of presumptive glutamatergic/aspartatergic afferents to the magnocellular basal forebrain in the rat. J Comp Neurol 302:824–852PubMedCrossRef
12.
go back to reference Chiba AA, Bucci DJ, Holland PC, Gallagher M (1995) Basal forebrain cholinergic lesions disrupt increments but not decrements in conditioned stimulus processing. J Neurosci Off J Soc Neurosci 15:7315–7322 Chiba AA, Bucci DJ, Holland PC, Gallagher M (1995) Basal forebrain cholinergic lesions disrupt increments but not decrements in conditioned stimulus processing. J Neurosci Off J Soc Neurosci 15:7315–7322
13.
go back to reference Choi CY, Han SR, Yee GT, Lee CH (2010) A understanding of the temporal stem. J Korean Neurosurg Soc 47:365–369PubMedCrossRef Choi CY, Han SR, Yee GT, Lee CH (2010) A understanding of the temporal stem. J Korean Neurosurg Soc 47:365–369PubMedCrossRef
14.
go back to reference Cotter DR, Pariante CM, Everall IP (2001) Glial cell abnormalities in major psychiatric disorders: the evidence and implications. Brain Res Bull 55:585–595PubMedCrossRef Cotter DR, Pariante CM, Everall IP (2001) Glial cell abnormalities in major psychiatric disorders: the evidence and implications. Brain Res Bull 55:585–595PubMedCrossRef
15.
go back to reference Cowell PE, Kostianovsky DJ, Gur RC, Turetsky BI, Gur RE (1996) Sex differences in neuroanatomical and clinical correlations in schizophrenia. Am J Psychiatry 153:799–805PubMed Cowell PE, Kostianovsky DJ, Gur RC, Turetsky BI, Gur RE (1996) Sex differences in neuroanatomical and clinical correlations in schizophrenia. Am J Psychiatry 153:799–805PubMed
16.
go back to reference Crook JM, Dean B, Pavey G, Copolov D (1999) The binding of [3H]AFDX 384 is reduced in the caudate-putamen of subjects with schizophrenia. Life Sci 64:1761–1771PubMedCrossRef Crook JM, Dean B, Pavey G, Copolov D (1999) The binding of [3H]AFDX 384 is reduced in the caudate-putamen of subjects with schizophrenia. Life Sci 64:1761–1771PubMedCrossRef
17.
go back to reference Crook JM, Tomaskovic-Crook E, Copolov DL, Dean B (2000) Decreased muscarinic receptor binding in subjects with schizophrenia: a study of the human hippocampal formation. Biol Psychiatry 48:381–388PubMedCrossRef Crook JM, Tomaskovic-Crook E, Copolov DL, Dean B (2000) Decreased muscarinic receptor binding in subjects with schizophrenia: a study of the human hippocampal formation. Biol Psychiatry 48:381–388PubMedCrossRef
18.
go back to reference Crook JM, Tomaskovic-Crook E, Copolov DL, Dean B (2000) Low muscarinic receptor binding in prefrontal cortex from subjects with schizophrenia: a study of Brodmann’s areas 8, 9, 10, and 46 and the effects of neuroleptic drug treatment. Am J Psychiatry 158:918–925 Crook JM, Tomaskovic-Crook E, Copolov DL, Dean B (2000) Low muscarinic receptor binding in prefrontal cortex from subjects with schizophrenia: a study of Brodmann’s areas 8, 9, 10, and 46 and the effects of neuroleptic drug treatment. Am J Psychiatry 158:918–925
19.
go back to reference Cummings JL, Kaufer D (1996) Neuropsychiatric aspects of Alzheimer’s disease: the cholinergic hypothesis revisited. Neurology 47:876–883PubMedCrossRef Cummings JL, Kaufer D (1996) Neuropsychiatric aspects of Alzheimer’s disease: the cholinergic hypothesis revisited. Neurology 47:876–883PubMedCrossRef
20.
go back to reference Dean B, Crook JM, Opeskin K, Hill C, Keks N, Copolov DL (1996) The density of muscarinic M1 receptors is decreased in the caudate-putamen of subjects with schizophrenia. Mol Psychiatry 1:54–58PubMed Dean B, Crook JM, Opeskin K, Hill C, Keks N, Copolov DL (1996) The density of muscarinic M1 receptors is decreased in the caudate-putamen of subjects with schizophrenia. Mol Psychiatry 1:54–58PubMed
21.
go back to reference Dean B, McLeod M, Keriakous D, McKenzie J, Scarr E (2002) Decreased muscarinic 1 receptors in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol Psychiatry 7:1083–1091PubMedCrossRef Dean B, McLeod M, Keriakous D, McKenzie J, Scarr E (2002) Decreased muscarinic 1 receptors in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol Psychiatry 7:1083–1091PubMedCrossRef
22.
go back to reference Drevets WC, Gautier C, Price JC, Kupfer DJ, Kinahan PE, Grace AA, Price JL, Mathis CA (2001) Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria. Biol Psychiatry 49:81–96PubMedCrossRef Drevets WC, Gautier C, Price JC, Kupfer DJ, Kinahan PE, Grace AA, Price JL, Mathis CA (2001) Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria. Biol Psychiatry 49:81–96PubMedCrossRef
23.
go back to reference Emsley JG, Macklis JD (2006) Astroglial heterogeneity closely reflects the neuronal-defined anatomy of the adult murine CNS. Neuron Glia Biol 2:175–186PubMedCrossRef Emsley JG, Macklis JD (2006) Astroglial heterogeneity closely reflects the neuronal-defined anatomy of the adult murine CNS. Neuron Glia Biol 2:175–186PubMedCrossRef
24.
go back to reference Erickson SK, Schwarzkopf SB, Palumbo D, Badgley-Fleeman J, Smirnow AM, Light GA (2005) Efficacy and tolerability of low-dose donepezil in schizophrenia. Clin Neuropharmacol 28:179–184PubMedCrossRef Erickson SK, Schwarzkopf SB, Palumbo D, Badgley-Fleeman J, Smirnow AM, Light GA (2005) Efficacy and tolerability of low-dose donepezil in schizophrenia. Clin Neuropharmacol 28:179–184PubMedCrossRef
25.
go back to reference Falkai P, Honer WG, David S, Bogerts B, Majtenyi C, Bayer TA (1999) No evidence for astrogliosis in brains of schizophrenic patients. A post-mortem study. Neuropathol Appl Neurobiol 25:48–53PubMedCrossRef Falkai P, Honer WG, David S, Bogerts B, Majtenyi C, Bayer TA (1999) No evidence for astrogliosis in brains of schizophrenic patients. A post-mortem study. Neuropathol Appl Neurobiol 25:48–53PubMedCrossRef
26.
go back to reference Fellner L, Jellinger KA, Wenning GK, Stefanova N (2011) Glial dysfunction in the pathogenesis of α-synucleinopathies: emerging concepts. Acta Neuropathol 121:675–693PubMedCrossRef Fellner L, Jellinger KA, Wenning GK, Stefanova N (2011) Glial dysfunction in the pathogenesis of α-synucleinopathies: emerging concepts. Acta Neuropathol 121:675–693PubMedCrossRef
27.
go back to reference Freudenreich O, Herz L, Deckersbach T, Evins AE, Henderson DC, Cather C, Goff DC (2005) Added donepezil for stable schizophrenia: a double-blind, placebo-controlled trial. Psychopharmacology (Berlin) 181:358–363CrossRef Freudenreich O, Herz L, Deckersbach T, Evins AE, Henderson DC, Cather C, Goff DC (2005) Added donepezil for stable schizophrenia: a double-blind, placebo-controlled trial. Psychopharmacology (Berlin) 181:358–363CrossRef
28.
go back to reference Gasbarri A, Sulli A, Pacitti C, McGaugh JL (1999) Serotonergic input to cholinergic neurons in the substantia innominata and nucleus basalis magnocellularis in the rat. Neuroscience 91:1129–1142PubMedCrossRef Gasbarri A, Sulli A, Pacitti C, McGaugh JL (1999) Serotonergic input to cholinergic neurons in the substantia innominata and nucleus basalis magnocellularis in the rat. Neuroscience 91:1129–1142PubMedCrossRef
29.
go back to reference Guest PC, Schwarz E, Krishnamurthy D, Harris LW, Leweke FM, Rothermundt M, van Beveren NJ, Spain M, Barnes A, Steiner J, Rahmoune H, Bahn S (2011) Altered levels of circulating insulin and other neuroendocrine hormones associated with the onset of schizophrenia. Psychoneuroendocrinology 36:1092–1096PubMedCrossRef Guest PC, Schwarz E, Krishnamurthy D, Harris LW, Leweke FM, Rothermundt M, van Beveren NJ, Spain M, Barnes A, Steiner J, Rahmoune H, Bahn S (2011) Altered levels of circulating insulin and other neuroendocrine hormones associated with the onset of schizophrenia. Psychoneuroendocrinology 36:1092–1096PubMedCrossRef
30.
go back to reference Hafner H, Maurer K, Loffler W, Riecher-Rossler A (1993) The influence of age and sex on the onset and early course of schizophrenia. Brit J Psychiatry J Mental Sci 162:80–86CrossRef Hafner H, Maurer K, Loffler W, Riecher-Rossler A (1993) The influence of age and sex on the onset and early course of schizophrenia. Brit J Psychiatry J Mental Sci 162:80–86CrossRef
31.
go back to reference Hakak Y, Walker JR, Li C, Wong WH, Davis KL, Buxbaum JD, Haroutunian V, Fienberg AA (2001) Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc Natl Acad Sci USA 98:4746–4751PubMedCrossRef Hakak Y, Walker JR, Li C, Wong WH, Davis KL, Buxbaum JD, Haroutunian V, Fienberg AA (2001) Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc Natl Acad Sci USA 98:4746–4751PubMedCrossRef
32.
go back to reference Hamidi M, Drevets WC, Price JL (2004) Glial reduction in amygdala in major depressive disorder is due to oligodendrocytes. Biol Psychiatry 55:563–569PubMedCrossRef Hamidi M, Drevets WC, Price JL (2004) Glial reduction in amygdala in major depressive disorder is due to oligodendrocytes. Biol Psychiatry 55:563–569PubMedCrossRef
33.
34.
35.
go back to reference Hof PR, Haroutunian V, Friedrich VL Jr, Byne W, Buitron C, Perl DP, Davis KL (2003) Loss and altered spatial distribution of oligodendrocytes in the superior frontal gyrus in schizophrenia. Biol Psychiatry 53:1075–1085PubMedCrossRef Hof PR, Haroutunian V, Friedrich VL Jr, Byne W, Buitron C, Perl DP, Davis KL (2003) Loss and altered spatial distribution of oligodendrocytes in the superior frontal gyrus in schizophrenia. Biol Psychiatry 53:1075–1085PubMedCrossRef
36.
go back to reference Hutchinson M, Fazzini E (1996) Cholinesterase inhibition in Parkinson’s disease. J Neurol Neurosurg Psychiatry 61:324–325PubMedCrossRef Hutchinson M, Fazzini E (1996) Cholinesterase inhibition in Parkinson’s disease. J Neurol Neurosurg Psychiatry 61:324–325PubMedCrossRef
37.
go back to reference Ishibashi T, Dakin KA, Stevens B, Lee PR, Kozlov SV, Stewart CL, Fields RD (2006) Astrocytes promote myelination in response to electrical impulses. Neuron 49:823–832PubMedCrossRef Ishibashi T, Dakin KA, Stevens B, Lee PR, Kozlov SV, Stewart CL, Fields RD (2006) Astrocytes promote myelination in response to electrical impulses. Neuron 49:823–832PubMedCrossRef
38.
go back to reference Jellinger KA (2009) Lewy body/alpha-synucleinopathy in schizophrenia and depression: a preliminary neuropathological study. Acta Neuropathol 117:423–427PubMedCrossRef Jellinger KA (2009) Lewy body/alpha-synucleinopathy in schizophrenia and depression: a preliminary neuropathological study. Acta Neuropathol 117:423–427PubMedCrossRef
39.
go back to reference Johnston-Wilson NL, Sims CD, Hofmann JP, Anderson L, Shore AD, Torrey EF, Yolken RH (2000) Disease-specific alterations in frontal cortex brain proteins in schizophrenia, bipolar disorder, and major depressive disorder. Stanley Neuropathol Consortium Mol Psychiatry 5:142–149 Johnston-Wilson NL, Sims CD, Hofmann JP, Anderson L, Shore AD, Torrey EF, Yolken RH (2000) Disease-specific alterations in frontal cortex brain proteins in schizophrenia, bipolar disorder, and major depressive disorder. Stanley Neuropathol Consortium Mol Psychiatry 5:142–149
40.
go back to reference Jones BE, Cuello AC (1989) Afferents to the basal forebrain cholinergic cell area from pontomesencephalic–catecholamine, serotonin, and acetylcholine–neurons. Neuroscience 31:37–61PubMedCrossRef Jones BE, Cuello AC (1989) Afferents to the basal forebrain cholinergic cell area from pontomesencephalic–catecholamine, serotonin, and acetylcholine–neurons. Neuroscience 31:37–61PubMedCrossRef
41.
go back to reference Jones EG, Burton H, Saper CB, Swanson LW (1976) Midbrain, diencephalic and cortical relationships of the basal nucleus of Meynert and associated structures in primates. J Comp Neurol 167:385–419PubMedCrossRef Jones EG, Burton H, Saper CB, Swanson LW (1976) Midbrain, diencephalic and cortical relationships of the basal nucleus of Meynert and associated structures in primates. J Comp Neurol 167:385–419PubMedCrossRef
42.
go back to reference Kasper BS, Taylor DC, Janz D, Kasper EM, Maier M, Williams MR, Crow TJ (2010) Neuropathology of epilepsy and psychosis: the contributions of J.A.N. Corsellis Brain 133:3795–3805CrossRef Kasper BS, Taylor DC, Janz D, Kasper EM, Maier M, Williams MR, Crow TJ (2010) Neuropathology of epilepsy and psychosis: the contributions of J.A.N. Corsellis Brain 133:3795–3805CrossRef
43.
go back to reference Katerina Z, Andrew K, Filomena M, Xu-Feng H (2004) Investigation of m1/m4 muscarinic receptors in the anterior cingulate cortex in schizophrenia, bipolar disorder, and major depression disorder. Neuropsychopharmacology 29:619–625PubMedCrossRef Katerina Z, Andrew K, Filomena M, Xu-Feng H (2004) Investigation of m1/m4 muscarinic receptors in the anterior cingulate cortex in schizophrenia, bipolar disorder, and major depression disorder. Neuropsychopharmacology 29:619–625PubMedCrossRef
44.
go back to reference Laming PR (2000) Potassium signalling in the brain: its role in behaviour. Neurochem Int 36:271–290PubMedCrossRef Laming PR (2000) Potassium signalling in the brain: its role in behaviour. Neurochem Int 36:271–290PubMedCrossRef
45.
go back to reference Lara DR, Gama CS, Belmonte-de-Abreu P, Portela LV, Goncalves CA, Fonseca M, Hauck S, Souza DO (2001) Increased serum S100B protein in schizophrenia: a study in medication-free patients. J Psychiatr Res 35:11–14PubMedCrossRef Lara DR, Gama CS, Belmonte-de-Abreu P, Portela LV, Goncalves CA, Fonseca M, Hauck S, Souza DO (2001) Increased serum S100B protein in schizophrenia: a study in medication-free patients. J Psychiatr Res 35:11–14PubMedCrossRef
46.
go back to reference Lenzi A, Maltinti E, Poggi E, Fabrizio L, Coli E (2003) Effects of rivastigmine on cognitive function and quality of life in patients with schizophrenia. Clin Neuropharmacol 26:317–321PubMedCrossRef Lenzi A, Maltinti E, Poggi E, Fabrizio L, Coli E (2003) Effects of rivastigmine on cognitive function and quality of life in patients with schizophrenia. Clin Neuropharmacol 26:317–321PubMedCrossRef
47.
go back to reference Lim KO, Hedehus M, Moseley M, de Crespigny A, Sullivan EV, Pfefferbaum A (1999) Compromised white matter tract integrity in schizophrenia inferred from diffusion tensor imaging. Arch Gen Psychiatry 56:367–374PubMedCrossRef Lim KO, Hedehus M, Moseley M, de Crespigny A, Sullivan EV, Pfefferbaum A (1999) Compromised white matter tract integrity in schizophrenia inferred from diffusion tensor imaging. Arch Gen Psychiatry 56:367–374PubMedCrossRef
48.
go back to reference Mai J, Assheuer J, Paxinos G (2004) Atlas of the human brain, 2nd edn. Elsevier publishing, Amsterdam Mai J, Assheuer J, Paxinos G (2004) Atlas of the human brain, 2nd edn. Elsevier publishing, Amsterdam
49.
go back to reference Mattsson A, Olson L, Svensson TH, Schilström B (2007) Cortical cholinergic deficiency enhances amphetamine-induced dopamine release in the accumbens but not striatum. Exp Neurol 208:73–79PubMedCrossRef Mattsson A, Olson L, Svensson TH, Schilström B (2007) Cortical cholinergic deficiency enhances amphetamine-induced dopamine release in the accumbens but not striatum. Exp Neurol 208:73–79PubMedCrossRef
50.
go back to reference Mesulam MM, Mufson EJ (1984) Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. Brain A J Neurol 107:253–274CrossRef Mesulam MM, Mufson EJ (1984) Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. Brain A J Neurol 107:253–274CrossRef
51.
go back to reference Mesulam MM, Mufson EJ, Levey AI, Wainer BH (1983) Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 214:170–197PubMedCrossRef Mesulam MM, Mufson EJ, Levey AI, Wainer BH (1983) Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 214:170–197PubMedCrossRef
52.
go back to reference Miller R, Chouinard G (1993) Loss of striatal cholinergic neurons as a basis for tardive and L-dopa-induced dyskinesias, neuroleptic-induced supersensitivity psychosis and refractory schizophrenia. Biol Psychiatry 34:713–738PubMedCrossRef Miller R, Chouinard G (1993) Loss of striatal cholinergic neurons as a basis for tardive and L-dopa-induced dyskinesias, neuroleptic-induced supersensitivity psychosis and refractory schizophrenia. Biol Psychiatry 34:713–738PubMedCrossRef
53.
go back to reference Moises HW, Zoega T, Gottesman II (2002) The glial growth factors deficiency and synaptic destabilization hypothesis of schizophrenia. BMC Psychiatry 2:8PubMedCrossRef Moises HW, Zoega T, Gottesman II (2002) The glial growth factors deficiency and synaptic destabilization hypothesis of schizophrenia. BMC Psychiatry 2:8PubMedCrossRef
54.
go back to reference Pakkenberg B (1990) Pronounced reduction of total neuron number in mediodorsal thalamic nucleus and nucleus accumbens in schizophrenics. Arch Gen Psychiatry 47:1023–1028PubMedCrossRef Pakkenberg B (1990) Pronounced reduction of total neuron number in mediodorsal thalamic nucleus and nucleus accumbens in schizophrenics. Arch Gen Psychiatry 47:1023–1028PubMedCrossRef
55.
go back to reference Pariante CM, Pearce BD, Pisell TL, Owens MJ, Miller AH (1997) Steroid-independent translocation of the glucocorticoid receptor by the antidepressant desipramine. Mol Pharmacol 52:571–581PubMed Pariante CM, Pearce BD, Pisell TL, Owens MJ, Miller AH (1997) Steroid-independent translocation of the glucocorticoid receptor by the antidepressant desipramine. Mol Pharmacol 52:571–581PubMed
56.
go back to reference Perry EK, Marshall E, Perry RH, Irving D, Smith CJ, Blessed G, Fairbairn AF (1990) Cholinergic and dopaminergic activities in senile dementia of Lewy body type. Alzheimer Dis Assoc Disord 4:87–95PubMed Perry EK, Marshall E, Perry RH, Irving D, Smith CJ, Blessed G, Fairbairn AF (1990) Cholinergic and dopaminergic activities in senile dementia of Lewy body type. Alzheimer Dis Assoc Disord 4:87–95PubMed
57.
go back to reference Pinto T, Lanctôt KL, Herrmann N (2011) Revisiting the cholinergic hypothesis of behavioral and psychological symptoms in dementia of the Alzheimer’s Type. Ageing Res Rev 10:404–412PubMed Pinto T, Lanctôt KL, Herrmann N (2011) Revisiting the cholinergic hypothesis of behavioral and psychological symptoms in dementia of the Alzheimer’s Type. Ageing Res Rev 10:404–412PubMed
58.
go back to reference Raedler TJ, Knable MB, Jones DW, Urbina RA, Gorey JG, Lee KS, Egan MF, Coppola R, Weinberger DR (2003) In vivo determination of muscarinic acetylcholine receptor availability in schizophrenia. Am J Psychiatry 160:118–127PubMedCrossRef Raedler TJ, Knable MB, Jones DW, Urbina RA, Gorey JG, Lee KS, Egan MF, Coppola R, Weinberger DR (2003) In vivo determination of muscarinic acetylcholine receptor availability in schizophrenia. Am J Psychiatry 160:118–127PubMedCrossRef
59.
go back to reference Rajkowska G, Miguel-Hidalgo JJ, Makkos Z, Meltzer H, Overholser J, Stockmeier C (2002) Layer-specific reductions in GFAP-reactive astroglia in the dorsolateral prefrontal cortex in schizophrenia. Schizophr Res 57:127–138PubMedCrossRef Rajkowska G, Miguel-Hidalgo JJ, Makkos Z, Meltzer H, Overholser J, Stockmeier C (2002) Layer-specific reductions in GFAP-reactive astroglia in the dorsolateral prefrontal cortex in schizophrenia. Schizophr Res 57:127–138PubMedCrossRef
60.
go back to reference Rao TS, Correa LD, Adams P, Santori EM, Sacaan AI (2003) Pharmacological characterization of dopamine, norepinephrine and serotonin release in the rat prefrontal cortex by neuronal nicotinic acetylcholine receptor agonists. Brain Res 990:203–208PubMedCrossRef Rao TS, Correa LD, Adams P, Santori EM, Sacaan AI (2003) Pharmacological characterization of dopamine, norepinephrine and serotonin release in the rat prefrontal cortex by neuronal nicotinic acetylcholine receptor agonists. Brain Res 990:203–208PubMedCrossRef
61.
go back to reference Rasmusson DD, Szerb IC, Jordan JL (1996) Differential effects of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid and N-methyl-D-aspartate receptor antagonists applied to the basal forebrain on cortical acetylcholine release and electroencephalogram desynchronization. Neuroscience 72:419–427PubMedCrossRef Rasmusson DD, Szerb IC, Jordan JL (1996) Differential effects of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid and N-methyl-D-aspartate receptor antagonists applied to the basal forebrain on cortical acetylcholine release and electroencephalogram desynchronization. Neuroscience 72:419–427PubMedCrossRef
62.
go back to reference Rothermundt M, Missler U, Arolt V, Peters M, Leadbeater J, Wiesmann M, Rudolf S, Wandinger KP, Kirchner H (2001) Increased S100B blood levels in unmedicated and treated schizophrenic patients are correlated with negative symptomatology. Mol Psychiatry 6:445–449PubMedCrossRef Rothermundt M, Missler U, Arolt V, Peters M, Leadbeater J, Wiesmann M, Rudolf S, Wandinger KP, Kirchner H (2001) Increased S100B blood levels in unmedicated and treated schizophrenic patients are correlated with negative symptomatology. Mol Psychiatry 6:445–449PubMedCrossRef
63.
go back to reference Satoh J, Tabunoki H, Yamamura T, Arima K, Konno H (2007) Human astrocytes express aquaporin-1 and aquaporin-4 in vitro and in vivo. Neuropathol Off J Jpn Soc Neuropathol 27:245–256CrossRef Satoh J, Tabunoki H, Yamamura T, Arima K, Konno H (2007) Human astrocytes express aquaporin-1 and aquaporin-4 in vitro and in vivo. Neuropathol Off J Jpn Soc Neuropathol 27:245–256CrossRef
64.
go back to reference Schmitt A, Steyskal C, Bernstein HG, Schneider-Axmann T, Parlapani E, Schaeffer EL, Gattaz WF, Bogerts B, Schmitz C, Falkai P (2009) Stereologic investigation of the posterior part of the hippocampus in schizophrenia. Acta Neuropathol 117:395–407PubMedCrossRef Schmitt A, Steyskal C, Bernstein HG, Schneider-Axmann T, Parlapani E, Schaeffer EL, Gattaz WF, Bogerts B, Schmitz C, Falkai P (2009) Stereologic investigation of the posterior part of the hippocampus in schizophrenia. Acta Neuropathol 117:395–407PubMedCrossRef
65.
go back to reference Sinclair D, Tsai SY, Woon HG, Weickert CS (2011) Abnormal glucocorticoid receptor mRNA and protein isoform expression in the prefrontal cortex in psychiatric illness. Neuropsychopharmacology 36:2698–2709PubMedCrossRef Sinclair D, Tsai SY, Woon HG, Weickert CS (2011) Abnormal glucocorticoid receptor mRNA and protein isoform expression in the prefrontal cortex in psychiatric illness. Neuropsychopharmacology 36:2698–2709PubMedCrossRef
66.
go back to reference Smiley JF, Mesulam MM (1999) Cholinergic neurons of the nucleus basalis of Meynert receive cholinergic, catecholaminergic and GABAergic synapses: an electron microscopic investigation in the monkey. Neuroscience 88:241–255PubMedCrossRef Smiley JF, Mesulam MM (1999) Cholinergic neurons of the nucleus basalis of Meynert receive cholinergic, catecholaminergic and GABAergic synapses: an electron microscopic investigation in the monkey. Neuroscience 88:241–255PubMedCrossRef
67.
go back to reference Stark AK, Uylings HB, Sanz-Arigita E, Pakkenberg B (2004) Glial cell loss in the anterior cingulate cortex, a subregion of the prefrontal cortex, in subjects with schizophrenia. Am J Psychiatry 161:882–888PubMedCrossRef Stark AK, Uylings HB, Sanz-Arigita E, Pakkenberg B (2004) Glial cell loss in the anterior cingulate cortex, a subregion of the prefrontal cortex, in subjects with schizophrenia. Am J Psychiatry 161:882–888PubMedCrossRef
68.
go back to reference Steiner J, Bernstein HG, Bielau H, Farkas N, Winter J, Dobrowolny H, Brisch R, Gos T, Mawrin C, Myint AM, Bogerts B (2008) S100B-immunopositive glia is elevated in paranoid as compared to residual schizophrenia: a morphometric study. J Psychiatr Res 42:868–876PubMedCrossRef Steiner J, Bernstein HG, Bielau H, Farkas N, Winter J, Dobrowolny H, Brisch R, Gos T, Mawrin C, Myint AM, Bogerts B (2008) S100B-immunopositive glia is elevated in paranoid as compared to residual schizophrenia: a morphometric study. J Psychiatr Res 42:868–876PubMedCrossRef
69.
go back to reference Steriade M, Parent A, Pare D, Smith Y (1987) Cholinergic and non-cholinergic neurons of cat basal forebrain project to reticular and mediodorsal thalamic nuclei. Brain Res 408:372–376PubMedCrossRef Steriade M, Parent A, Pare D, Smith Y (1987) Cholinergic and non-cholinergic neurons of cat basal forebrain project to reticular and mediodorsal thalamic nuclei. Brain Res 408:372–376PubMedCrossRef
70.
go back to reference Stoehr JD, Mobley SL, Roice D, Brooks R, Baker LM, Wiley RG, Wenk GL (1997) The effects of selective cholinergic basal forebrain lesions and aging upon expectancy in the rat. Neurobiol Learn Mem 67:214–227PubMedCrossRef Stoehr JD, Mobley SL, Roice D, Brooks R, Baker LM, Wiley RG, Wenk GL (1997) The effects of selective cholinergic basal forebrain lesions and aging upon expectancy in the rat. Neurobiol Learn Mem 67:214–227PubMedCrossRef
71.
go back to reference Stryer R, Strous R, Bar F, Shaked G, Shiloh R, Rozencwaig S, Grupper D, Buchman N, Kotler M, Rabey JM, Weizman A (2004) Donepezil augmentation of clozapine monotherapy in schizophrenia patients: a double blind cross-over study. Hum Psychopharmacol 19:343–346CrossRef Stryer R, Strous R, Bar F, Shaked G, Shiloh R, Rozencwaig S, Grupper D, Buchman N, Kotler M, Rabey JM, Weizman A (2004) Donepezil augmentation of clozapine monotherapy in schizophrenia patients: a double blind cross-over study. Hum Psychopharmacol 19:343–346CrossRef
72.
go back to reference Stryer R, Strous RD, Bar F, Werber E, Shaked G, Buhiri Y et al (2003) Beneficial effect of donepezil augmentation for the management of comorbid schizophrenia and dementia. Clin Neuropharmacol 26:12–17CrossRef Stryer R, Strous RD, Bar F, Werber E, Shaked G, Buhiri Y et al (2003) Beneficial effect of donepezil augmentation for the management of comorbid schizophrenia and dementia. Clin Neuropharmacol 26:12–17CrossRef
73.
go back to reference Sugai T, Kawamura M, Iritani S, Araki K, Makifuchi T, Imai C, Nakamura R, Kakita A, Takahashi H, Nawa H (2004) Prefrontal abnormality of schizophrenia revealed by DNA microarray: impact on glial and neurotrophic gene expression. Ann N Y Acad Sci 1025:84–91PubMedCrossRef Sugai T, Kawamura M, Iritani S, Araki K, Makifuchi T, Imai C, Nakamura R, Kakita A, Takahashi H, Nawa H (2004) Prefrontal abnormality of schizophrenia revealed by DNA microarray: impact on glial and neurotrophic gene expression. Ann N Y Acad Sci 1025:84–91PubMedCrossRef
74.
go back to reference Tugal O, Yazici KM, Yagcioglu AE, Gogus A (2004) A double-blind, placebo controlled, cross-over trial of adjunctive donepezil for cognitive impairment in schizophrenia. Int J Neuropsychopharmacol 7:117–123PubMedCrossRef Tugal O, Yazici KM, Yagcioglu AE, Gogus A (2004) A double-blind, placebo controlled, cross-over trial of adjunctive donepezil for cognitive impairment in schizophrenia. Int J Neuropsychopharmacol 7:117–123PubMedCrossRef
75.
go back to reference Uranova NA, Vostrikov VM, Vikhreva OV, Zimina IS, Kolomeets NS, Orlovskaya DD (2007) The role of oligodendrocyte pathology in schizophrenia. Int J Neuropsychopharmacol 10:537–545PubMedCrossRef Uranova NA, Vostrikov VM, Vikhreva OV, Zimina IS, Kolomeets NS, Orlovskaya DD (2007) The role of oligodendrocyte pathology in schizophrenia. Int J Neuropsychopharmacol 10:537–545PubMedCrossRef
76.
go back to reference Uranova NA, Vostrikov VM, Orlovskaya DD, Rachmanova VI (2004) Oligodendroglial density in the prefrontal cortex in schizophrenia and mood disorders: a study from the Stanley neuropathology consortium. Schizophr Res 67:269–275PubMedCrossRef Uranova NA, Vostrikov VM, Orlovskaya DD, Rachmanova VI (2004) Oligodendroglial density in the prefrontal cortex in schizophrenia and mood disorders: a study from the Stanley neuropathology consortium. Schizophr Res 67:269–275PubMedCrossRef
77.
go back to reference van Haren NE, Schnack HG, Cahn W, van den Heuvel MP, Lepage C, Collins L, Evans AC, Hulshoff Pol HE, Kahn RS (2011) Changes in cortical thickness during the course of illness in schizophrenia. Arch Gen Psychiatry 68:871–880PubMedCrossRef van Haren NE, Schnack HG, Cahn W, van den Heuvel MP, Lepage C, Collins L, Evans AC, Hulshoff Pol HE, Kahn RS (2011) Changes in cortical thickness during the course of illness in schizophrenia. Arch Gen Psychiatry 68:871–880PubMedCrossRef
78.
go back to reference Virgin CE Jr, Ha TP, Packan DR, Tombaugh GC, Yang SH, Horner HC, Sapolsky RM (1991) Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: implications for glucocorticoid neurotoxicity. J Neurochem 57:1422–1428PubMedCrossRef Virgin CE Jr, Ha TP, Packan DR, Tombaugh GC, Yang SH, Horner HC, Sapolsky RM (1991) Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: implications for glucocorticoid neurotoxicity. J Neurochem 57:1422–1428PubMedCrossRef
79.
go back to reference Watanabe S, Nishikawa T, Takashima M, Toru M (1983) Increased muscarinic cholinergic receptors in prefrontal cortices of medicated schizophrenics. Life Sci 33:2187–2196PubMedCrossRef Watanabe S, Nishikawa T, Takashima M, Toru M (1983) Increased muscarinic cholinergic receptors in prefrontal cortices of medicated schizophrenics. Life Sci 33:2187–2196PubMedCrossRef
80.
go back to reference Webster MJ, Knable MB, Johnston-Wilson N, Nagata K, Inagaki M, Yolken RH (2001) Immunohistochemical localization of phosphorylated glial fibrillary acidic protein in the prefrontal cortex and hippocampus from patients with schizophrenia, bipolar disorder, and depression. Brain Behav Immun 15:388–400PubMedCrossRef Webster MJ, Knable MB, Johnston-Wilson N, Nagata K, Inagaki M, Yolken RH (2001) Immunohistochemical localization of phosphorylated glial fibrillary acidic protein in the prefrontal cortex and hippocampus from patients with schizophrenia, bipolar disorder, and depression. Brain Behav Immun 15:388–400PubMedCrossRef
81.
go back to reference Webster MJ, O’Grady J, Kleinman JE, Weickert CS (2005) Glial fibrillary acidic protein mRNA levels in the cingulate cortex of individuals with depression, bipolar disorder and schizophrenia. Neuroscience 133:453–461PubMedCrossRef Webster MJ, O’Grady J, Kleinman JE, Weickert CS (2005) Glial fibrillary acidic protein mRNA levels in the cingulate cortex of individuals with depression, bipolar disorder and schizophrenia. Neuroscience 133:453–461PubMedCrossRef
82.
go back to reference Wenk GL (1997) The nucleus basalis magnocellularis cholinergic system: one hundred years of progress. Neurobiol Learn Mem 67:85–95PubMedCrossRef Wenk GL (1997) The nucleus basalis magnocellularis cholinergic system: one hundred years of progress. Neurobiol Learn Mem 67:85–95PubMedCrossRef
83.
go back to reference Whitehouse PJ, Hedreen JC, White CL, Price DL (1983) Basal forebrain neurons in the dementia of Parkinson disease. Ann Neurol 13:243–248PubMedCrossRef Whitehouse PJ, Hedreen JC, White CL, Price DL (1983) Basal forebrain neurons in the dementia of Parkinson disease. Ann Neurol 13:243–248PubMedCrossRef
84.
go back to reference 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 10:122–126PubMedCrossRef 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 10:122–126PubMedCrossRef
85.
go back to reference Williams MR, Chaudhry R, Perera S, Pearce RKB, Hirsch SR, Ansorge O, Thom M, Maier M (2012a). Changes in cortical thickness in the frontal lobes in schizophrenia are a result of thinning of pyramidal cell layers. Eur Arch Psychiatry Clin Neurosci (May 19th Epub) Williams MR, Chaudhry R, Perera S, Pearce RKB, Hirsch SR, Ansorge O, Thom M, Maier M (2012a). Changes in cortical thickness in the frontal lobes in schizophrenia are a result of thinning of pyramidal cell layers. Eur Arch Psychiatry Clin Neurosci (May 19th Epub)
86.
go back to reference Williams MR, Hampton T, Pearce RKB, Hirsch SR, Ansorge O, Thom M, Maier M (2012b) Astrocyte decrease in the subgenual cingulate and callosal genu in schizophrenia. Eur Arch Psychiatry Clin Neurosci (June 4th Epub) Williams MR, Hampton T, Pearce RKB, Hirsch SR, Ansorge O, Thom M, Maier M (2012b) Astrocyte decrease in the subgenual cingulate and callosal genu in schizophrenia. Eur Arch Psychiatry Clin Neurosci (June 4th Epub)
87.
go back to reference Williams MR, Pearce RKB, Hirsch SR, Ansorge O, Thom M, Maier M (2006) Astrocytes abnormalities differentiate schizophrenia from affective disorders in post-mortem brain. Schizophr Res 81(supp):72 Williams MR, Pearce RKB, Hirsch SR, Ansorge O, Thom M, Maier M (2006) Astrocytes abnormalities differentiate schizophrenia from affective disorders in post-mortem brain. Schizophr Res 81(supp):72
88.
go back to reference Zaborszky L, Cullinan WE (1992) Projections from the nucleus accumbens to cholinergic neurons of the ventral pallidum: a correlated light and electron microscopic double-immunolabeling study in rat. Brain Res 570:92–101PubMedCrossRef Zaborszky L, Cullinan WE (1992) Projections from the nucleus accumbens to cholinergic neurons of the ventral pallidum: a correlated light and electron microscopic double-immunolabeling study in rat. Brain Res 570:92–101PubMedCrossRef
89.
go back to reference Zaborszky L, Gaykema RP, Swanson DJ, Cullinan WE (1997) Cortical input to the basal forebrain. Neuroscience 79:1051–1078PubMedCrossRef Zaborszky L, Gaykema RP, Swanson DJ, Cullinan WE (1997) Cortical input to the basal forebrain. Neuroscience 79:1051–1078PubMedCrossRef
Metadata
Title
Neuropathological changes in the nucleus basalis in schizophrenia
Authors
M. R. Williams
R. Marsh
C. D. Macdonald
J. Jain
R. K. B. Pearce
S. R. Hirsch
O. Ansorge
S. M. Gentleman
M. Maier
Publication date
01-09-2013
Publisher
Springer Berlin Heidelberg
Published in
European Archives of Psychiatry and Clinical Neuroscience / Issue 6/2013
Print ISSN: 0940-1334
Electronic ISSN: 1433-8491
DOI
https://doi.org/10.1007/s00406-012-0387-7

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