Schizophrenia; From structure to function with special focus on the mediodorsal thalamic prefrontal loop

Acta Psychiatrica Scandinavica

Volumn 120, Issue 5, 2009, Pages 345-354

  Pakkenberg, B ^a   Scheel Kruger J ^a   Kristiansen, L V ^a  

^a BISPEBJERG HOSPITAL   (Denmark)

Author keywords

Cell counting; Glutamate; Neurostereology; Neurotransmitter; Optical fractionator; Prefrontal cortex; Thalamus

Indexed keywords

NEUROTRANSMITTER; PROTEIN; RNA;

AUTORADIOGRAPHY; BRAIN FUNCTION; BRAIN REGION; CADAVER; CELL COUNT; COGNITIVE DEFECT; HUMAN; MOLECULAR INTERACTION; NERVE CELL; NEUROANATOMY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVIEW; SCHIZOPHRENIA; STEREOLOGY; THALAMUS DORSOMEDIAL NUCLEUS; WESTERN BLOTTING;

CELL COUNT; GLUTAMIC ACID; HUMANS; MEDIODORSAL THALAMIC NUCLEUS; SCHIZOPHRENIA; SYNAPTIC TRANSMISSION; THALAMUS;

EID: 70349667454     PISSN: 0001690X     EISSN: 16000447     Source Type: Journal    
DOI: 10.1111/j.1600-0447.2009.01447.x     Document Type: Review

References (96)

1. Wunderlich G. Griesinger's psychiatric approach. Psychiatr Neurol Med Psychol 1985 37 : 541 547.
2. Gotfredsen E. Medicinens historie. Copenhagen : Nyt Nordisk Forlag, 1950.
3. Katschnig H. 100 years of scientific psychiatry. Sigmund Freud, Emil Kraepelin, Emile Durkheim and modern psychiatry. Wien Klin Wochenschr 1998 110 : 207 211.
4. Ragland JD, Yoon J, Minzenberg MJ, Carter CS. Neuroimaging of cognitive disability in schizophrenia: search for a pathophysiological mechanism. Int Rev Psychiatry 2007 19 : 417 427.
5. Shad MU, Tamminga CA, Cullum M, Haas GL, Keshavan MS. Insight and frontal cortical function in schizophrenia: a review. Schizophr Res 2006 86 : 54 70.
6. Monakow CV. Experimentelle und pathologisch-anatomische untersuchungen uber die haubenregion, den sehhugel und die regio subthalamica. Arch Psychiatr Nervenkr 1895 27 : 92.
7. Bäumer H. Veränderung des Thalamus bei Schizophrenie. J Hirnforsch 1954 1 : 16.
8. Jones EG. Thalamic organization and function after Cajal. Prog Brain Res 2002 136 : 333 357.
9. Steriade M, Jones EG, Mccormick DA. The thalamus. Oxford : Elsevier, 1997.
10. Groenewegen HJ, Berendse HW, Wolters JG, Lohman AH. The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization. Prog Brain Res 1990 85 : 95 116. discussion -8.
11. Mcfarland NR, Haber SN. Thalamic relay nuclei of the basal ganglia form both reciprocal and nonreciprocal cortical connections, linking multiple frontal cortical areas. J Neurosci 2002 22 : 8117 8132.
12. Groenewegen HJ, Galis-De Graaf Y, Smeets WJ. Integration and segregation of limbic cortico-striatal loops at the thalamic level: an experimental tracing study in rats. J Chem Neuroanat 1999 16 : 167 185.
13. Goldman-Rakic PS, Porrino LJ. The primate mediodorsal (MD) nucleus and its projection to the frontal lobe. J Comp Neurol 1985 242 : 535 560.
14. Alexander GE, Crutcher MD, Delong MR. Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. Prog Brain Res 1990 85 : 119 146.
15. Jones EG. A description of the human thalamus. In : Steriade M et al., eds. Thalamus: experimental and clinical aspects. Oxford : Elsevier Science, 1997 : 425 500.
16. Jones EG. Thalamic circuitry and thalamocortical synchrony. Philos Trans R Soc Lond B Biol Sci 2002 357 : 1659 1673.
17. Erickson SL, Lewis DA. Cortical connections of the lateral mediodorsal thalamus in cynomolgus monkeys. J Comp Neurol 2004 473 : 107 127.
18. Uylings HB, Van Eden CG. Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. Prog Brain Res 1990 85 : 31 62.
19. Sim K, Cullen T, Ongur D, Heckers S. Testing models of thalamic dysfunction in schizophrenia using neuroimaging. J Neural Transm 2006 113 : 907 928.
20. Alelu-Paz R, Gimenez-Amaya JM. The mediodorsal thalamic nucleus and schizophrenia. J Psychiatry Neurosci 2008 33 : 489 498.
21. Dewulf A. Anatomy of the normal human thalamus, topometry and standardised nomenclature. Amsterdam : Elsevier, 1971.
22. Hirai T, Jones EG. A new parcellation of the human thalamus on the basis of histochemical staining. Brain Res Brain Res Rev 1989 14 : 1 34.
23. Armstrong E. Limbic thalamus: anterior and mediodorsal nuclei. In : Paxinos G, ed. The human nervous system. San Diego : Academic Press, 1990 : 469 481.
24. Jelsing J, Hay-Schmidt A, Dyrby T, Hemmingsen R, Uylings HB, Pakkenberg B. The prefrontal cortex in the Gottingen minipig brain defined by neural projection criteria and cytoarchitecture. Brain Res Bull 2007 70 : 14.
25. Dorph-Petersen KA, Pierri JN, Sun Z, Sampson AR, Lewis DA. Stereological analysis of the mediodorsal thalamic nucleus in schizophrenia: volume, neuron number, and cell types. J Comp Neurol 2004 472 : 449 462.
26. Pakkenberg B. Pronounced reduction of total neuron number in mediodorsal thalamic nucleus and nucleus accumbens in schizophrenics. Arch Gen Psychiatry 1990 47 : 1023 1028.
27. Pakkenberg B. The volume of the mediodorsal thalamic nucleus in treated and untreated schizophrenics. Schizophr Res 1992 7 : 95 100.
28. Popken GJ, Bunney WE Jr., Potkin SG, Jones EG. Subnucleus-specific loss of neurons in medial thalamus of schizophrenics. Proc Natl Acad Sci U S A 2000 97 : 9276 9280.
29. Young KA, Manaye KF, Liang C, Hicks PB, German DC. Reduced number of mediodorsal and anterior thalamic neurons in schizophrenia. Biol Psychiatry 2000 47 : 944 953.
30. Byne W, Buchsbaum MS, Mattiace LA et al. Postmortem assessment of thalamic nuclear volumes in subjects with schizophrenia. Am J Psychiatry 2002 159 : 59 65.
31. Danos P, Schmidt A, Baumann B et al. Volume and neuron number of the mediodorsal thalamic nucleus in schizophrenia: a replication study. Psychiatry Res 2005 140 : 281 289.
32. Cullen TJ, Walker MA, Parkinson N et al. A postmortem study of the mediodorsal nucleus of the thalamus in schizophrenia. Schizophr Res 2003 60 : 157 166.
33. Young KA, Holcomb LA, Yazdani U, Hicks PB, German DC. Elevated neuron number in the limbic thalamus in major depression. Am J Psychiatry 2004 161 : 1270 1277.
34. Kreczmanski P, Heinsen H, Mantua V et al. Volume, neuron density and total neuron number in five subcortical regions in schizophrenia. Brain 2007 130 : 678 692.
35. Stark AK, Uylings HB, Sanz-Arigita E, Pakkenberg B. Glial cell loss in the anterior cingulate cortex, a subregion of the prefrontal cortex, in subjects with schizophrenia. Am J Psychiatry 2004 161 : 882 888.
36. Damgaard Nielsen R, Abitz M, Pakkenberg B. Neuron and glial cell numbers in the mediodorsal thalamic nucleus in brains of schizophrenic subjects. Image Anal Stereol 2008 27 : 9.
37. Abitz M, Nielsen RD, Jones EG, Laursen H, Graem N, Pakkenberg B. Excess of neurons in the human newborn mediodorsal thalamus compared with that of the adult. Cereb Cortex 2007 17 : 2573 2578.
38. Behrendt RP. Dysregulation of thalamic sensory "transmission" in schizophrenia: neurochemical vulnerability to hallucinations. J Psychopharmacol 2006 20 : 356 372.
39. Clinton SM, Meador-Woodruff JH. Thalamic dysfunction in schizophrenia: neurochemical, neuropathological, and in vivo imaging abnormalities. Schizophr Res 2004 69 : 237 253.
40. Bunney WE, Bunney BG. Evidence for a compromised dorsolateral prefrontal cortical parallel circuit in schizophrenia. Brain Res Brain Res Rev 2000 31 : 138 146.
41. Watis L, Chen SH, Chua HC, Chong SA, Sim K. Glutamatergic abnormalities of the thalamus in schizophrenia: a systematic review. J Neural Transm 2008 115 : 493 511.
42. Gray JA, Roth BL. Molecular targets for treating cognitive dysfunction in schizophrenia. Schizophr Bull 2007 33 : 1100 1119.
43. Harrison PJ, Weinberger DR. Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 2005 10 : 40 68.
44. Tashiro A, Yuste R. Structure and molecular organization of dendritic spines. Histol Histopathol 2003 18 : 617 634.
45. Albrecht J, Sonnewald U, Waagepetersen HS, Schousboe A. Glutamine in the central nervous system: function and dysfunction. Front Biosci 2007 12 : 332 343.
46. Danbolt NC. Glutamate uptake. Prog Neurobiol 2001 65 : 1 105.
47. Sheng M, Hoogenraad CC. The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem 2007 76 : 823 847.
48. Boeckers TM. The postsynaptic density. Cell Tissue Res 2006 326 : 409 422.
49. Kew JN, Kemp JA. Ionotropic and metabotropic glutamate receptor structure and pharmacology. Psychopharmacology (Berl) 2005 179 : 4 29.
50. Kristiansen LV, Huerta I, Beneyto M, Meador-Woodruff JH. NMDA receptors and schizophrenia. Curr Opin Pharmacol 2007 7 : 48 55.
51. Tsai G, Coyle JT. Glutamatergic mechanisms in schizophrenia. Annu Rev Pharmacol Toxicol 2002 42 : 165 179.
52. Krystal JH, Karper LP, Seibyl JP et al. Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry 1994 51 : 199 214.
53. Lahti AC, Weiler MA, Tamara Michaelidis BA, Parwani A, Tamminga CA. Effects of ketamine in normal and schizophrenic volunteers. Neuropsychopharmacology 2001 25 : 455 467.
54. Lewis DA, Glantz LA, Pierri JN, Sweet RA. Altered cortical glutamate neurotransmission in schizophrenia: evidence from morphological studies of pyramidal neurons. Ann N Y Acad Sci 2003 1003 : 102 112.
55. Kristiansen LV, Cowell RM, Biscaia M, Mccullumsmith RE, Meador-Woodruff J. Alterations of neurotransmitter receptors in schizophrenia: evidence from postmortem studies. In : Abel L et al., eds. Handbook of neurochemistry and molecular neurobiology. New York : Springer, 2009 : 1 32.
56. Tamminga CA. The neurobiology of cognition in schizophrenia. J Clin Psychiatry 2006 67 (suppl. 9 9 13. Discussion 36-42.
57. Lewis DA, Moghaddam B. Cognitive dysfunction in schizophrenia: convergence of gamma-aminobutyric acid and glutamate alterations. Arch Neurol 2006 63 : 1372 1376.
58. Royall DR, Lauterbach EC, Cummings JL et al. Executive control function: a review of its promise and challenges for clinical research. A report from the Committee on Research of the American Neuropsychiatric Association. J Neuropsychiatry Clin Neurosci 2002 14 : 377 405.
59. Oni-Orisan A, Kristiansen LV, Haroutunian V, Meador-Woodruff J, Mccullumsmith RE. Altered vesicular glutamate transporter expression in the anterior cingulate cortex in schizophrenia. Biol Psychiatry 2008 63 : 9.
60. Graziano A, Liu XB, Murray KD, Jones EG. Vesicular glutamate transporters define two sets of glutamatergic afferents to the somatosensory thalamus and two thalamocortical projections in the mouse. J Comp Neurol 2008 507 : 1258 1276.
61. Kristiansen LV, Beneyto M, Haroutunian V, Meador-Woodruff JH. Changes in NMDA receptor subunits and interacting PSD proteins in dorsolateral prefrontal and anterior cingulate cortex indicate abnormal regional expression in schizophrenia. Mol Psychiatry 2006 8 : 737 747.
62. Toro C, Deakin JF. NMDA receptor subunit NRI and postsynaptic protein PSD-95 in hippocampus and orbitofrontal cortex in schizophrenia and mood disorder. Schizophr Res 2005 80 : 323 330.
63. Clinton SM, Meador-Woodruff JH. Abnormalities of the NMDA receptor and associated intracellular molecules in the thalamus in schizophrenia and bipolar disorder. Neuropsychopharmacology 2004 29 : 1353 1362.
64. Emamian ES, Karayiorgou M, Gogos JA. Decreased phosphorylation of NMDA receptor type 1 at serine 897 in brains of patients with Schizophrenia. J Neurosci 2004 24 : 1561 1564.
65. Meador-Woodruff JH, Clinton SM, Beneyto M, Mccullumsmith RE. Molecular abnormalities of the glutamate synapse in the thalamus in schizophrenia. Ann N Y Acad Sci 2003 1003 : 75 93.
66. Ibrahim HM, Hogg AJ Jr., Healy DJ, Haroutunian V, Davis KL, Meador-Woodruff JH. Ionotropic glutamate receptor binding and subunit mRNA expression in thalamic nuclei in schizophrenia. Am J Psychiatry 2000 157 : 1811 1823.
67. Clinton SM, Haroutunian V, Meador-Woodruff JH. Up-regulation of NMDA receptor subunit and post-synaptic density protein expression in the thalamus of elderly patients with schizophrenia. J Neurochem 2006 4 : 1114 1125.
68. Lyne J, Kelly BD, O'connor WT. Schizophrenia: a review of neuropharmacology. Ir J Med Sci 2004 173 : 155 159.
69. Seeman P. Dopamine receptors and the dopamine hypothesis of schizophrenia. Synapse 1987 1 : 133 152.
70. Sedvall G. Monoamines and schizophrenia. Acta Psychiatr Scand Suppl 1990 358 : 7 13.
71. Hartman DS, Civelli O. Molecular attributes of dopamine receptors: new potential for antipsychotic drug development. Ann Med 1996 28 : 211 219.
72. Meltzer HY. The mechanism of action of novel antipsychotic drugs. Schizophr Bull 1991 17 : 263 287.
73. Harrison PJ. The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 1999 122 (Pt 4 593 624.
74. Ford JM, Mathalon DH. Neural synchrony in schizophrenia. Schizophr Bull 2008 34 : 904 906.
75. Imre G, Salomons A, Jongsma M, Fokkema DS, Den Boer JA, Ter Horst GJ. Effects of the mGluR2/3 agonist LY379268 on ketamine-evoked behaviours and neurochemical changes in the dentate gyrus of the rat. Pharmacol Biochem Behav 2006 84 : 392 399.
76. Moghaddam B. Targeting metabotropic glutamate receptors for treatment of the cognitive symptoms of schizophrenia. Psychopharmacology (Berl) 2004 174 : 39 44.
77. Pratt JA, Winchester C, Egerton A, Cochran SM, Morris BJ. Modelling prefrontal cortex deficits in schizophrenia: implications for treatment. Br J Pharmacol 2008 153 (suppl. 1 S465 S470.
78. Gonzalez-Burgos G, Lewis DA. GABA neurons and the mechanisms of network oscillations: implications for understanding cortical dysfunction in schizophrenia. Schizophr Bull 2008 34 : 944 961.
79. Lewis DA, Cho RY, Carter CS et al. Subunit-selective modulation of GABA type A receptor neurotransmission and cognition in schizophrenia. Am J Psychiatry 2008 165 : 1585 1593.
80. Grace AA, Floresco SB, Goto Y, Lodge DJ. Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci 2007 30 : 220 227.
81. Benes FM. Emerging principles of altered neural circuitry in schizophrenia. Brain Res Brain Res Rev 2000 31 : 251 269.
82. Tseng KY, Lewis BL, Hashimoto T et al. A neonatal ventral hippocampal lesion causes functional deficits in adult prefrontal cortical interneurons. J Neurosci 2008 28 : 12691 12699.
83. Fletcher P. The missing link: a failure of fronto-hippocampal integration in schizophrenia. Nat Neurosci 1998 1 : 266 267.
84. Heckers S, Rauch SL, Goff D et al. Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nat Neurosci 1998 1 : 318 323.
85. Kostovic I. Structural and histochemical reorganization of the human prefrontal cortex during perinatal and postnatal life. Prog Brain Res 1990 85 : 223 239.
86. Petanjek Z, Judas M, Kostovic I, Uylings HB. Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefrontal cortex: a layer-specific pattern. Cereb Cortex 2008 18 : 915 929.
87. Winterer G, Weinberger DR. Genes, dopamine and cortical signal-to-noise ratio in schizophrenia. Trends Neurosci 2004 27 : 683 690.
88. Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 2005 6 : 312 324.
89. Lewis DA, Volk DW, Hashimoto T. Selective alterations in prefrontal cortical GABA neurotransmission in schizophrenia: a novel target for the treatment of working memory dysfunction. Psychopharmacology (Berl) 2004 174 : 143 150.
90. Blum BP, Mann JJ. The GABAergic system in schizophrenia. Int J Neuropsychopharmacol 2002 5 : 159 179.
91. Rotaru DC, Barrionuevo G, Sesack SR. Mediodorsal thalamic afferents to layer III of the rat prefrontal cortex: synaptic relationships to subclasses of interneurons. J Comp Neurol 2005 490 : 220 238.
92. Lewis DA, Cruz DA, Melchitzky DS, Pierri JN. 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.
93. Braun I, Genius J, Grunze H, Bender A, Moller HJ, Rujescu D. Alterations of hippocampal and prefrontal GABAergic interneurons in an animal model of psychosis induced by NMDA receptor antagonism. Schizophr Res 2007 97 : 254 263.
94. Abekawa T, Ito K, Nakagawa S, Koyama T. Prenatal exposure to an NMDA receptor antagonist, MK-801 reduces density of parvalbumin-immunoreactive GABAergic neurons in the medial prefrontal cortex and enhances phencyclidine-induced hyperlocomotion but not behavioral sensitization to methamphetamine in postpubertal rats. Psychopharmacology (Berl) 2007 192 : 303 316.
95. Lahti AC, Koffel B, Laporte D, Tamminga CA. Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology 1995 13 : 9 19.
96. Abdul-Monim Z, Neill JC, Reynolds GP. Sub-chronic psychotomimetic phencyclidine induces deficits in reversal learning and alterations in parvalbumin-immunoreactive expression in the rat. J Psychopharmacol 2007 21 : 198 205.