Abnormalities in thalamic neurophysiology in schizophrenia: Could psychosis be a result of potassium channel dysfunction?

Neuroscience and Biobehavioral Reviews

Volumn 36, Issue 2, 2012, Pages 960-968

  Vukadinovic, Zoran ^a   Rosenzweig, Ivana ^b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b ROYAL BROMPTON HOSPITAL   (United Kingdom)

Author keywords

Antipsychotics; K+ channels; Schizophrenia; Thalamus

Indexed keywords

POTASSIUM CHANNEL;

BRAIN FUNCTION; DRUG TARGETING; EXPERIMENTAL MODEL; FUNCTIONAL MORPHOLOGY; HUMAN; NERVE EXCITABILITY; NERVE POTENTIAL; NEUROPATHOLOGY; NEUROTRANSMISSION; NONHUMAN; PHARMACOLOGICAL STIMULATION; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA; THALAMUS; THALAMUS RETICULAR NUCLEUS;

ANIMALS; ANTIPSYCHOTIC AGENTS; HUMANS; NEURAL PATHWAYS; POTASSIUM CHANNELS; SCHIZOPHRENIA; THALAMUS;

EID: 84856082855     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2011.11.005     Document Type: Review

References (110)

1. Akhondzadeh S., Shasavand E., Jamilian H., Shabestari O., Kamalipour A. Dipyridamole in the treatment of schizophrenia: adenosine-dopamine receptor interactions. J. Clin. Pharm. Ther. 2000, 2:131-137.
2. Akhondzadeh S., Mojtahedzadeh V., Mirsepassi G.R., Moin M., Amini-Nooshabadi H., Kamalipour A. Diazoxide in the treatment of schizophrenia: novel application of potassium channel openers in the treatment of schizophrenia. J. Clin. Pharm. Ther. 2002, 27(6):453-459.
3. Akhondzadeh S., Safarcherati A., Amini H. Beneficial antipsychotic effects of allopurinol as add-on therapy for schizophrenia: a double blind, randomized and placebo controlled trial. Prog. Neuropharmacol. Biol. Psychiatry 2005, 2:253-259.
4. Albrecht T., Quäschling U., Zippel U., Davidowa H. Effects of dopamine on neurons of the lateral geniculate nucleus: an iontophoretic study. Synapse 1996, 23:70-78.
5. Alelu-Paz R., Gimenez-Amaya J.M. The mediodorsal thalamic nucleus and schizophrenia. J. Psychiatry Neurosci. 2008, 33(6):489-498.
6. Alexander G.M., Godwin D.W. Unique presynaptic and postsynaptic roles of group II metabotropic glutamate receptors in the modulation of thalamic network activity. Neuroscience 2006, 141:501-513.
7. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 2000, Text Revision, American Psychiatric Association, Washington, DC. 4th ed.
8. Andrews J., Wang L., Csernansky J.G., Gado M.H., Barch D.M. Abnormalities of thalamic activation and cognition in schizophrenia. Am. J. Psychiatry 2006, 163:463-469.
9. Anselmetti S., Cavallaro R., Bechi M., Angelone S.M., Ermoli E., Cocchi F., Smeraldi E. Psychopathological and neuropsychological correlates of source monitoring impairment in schizophrenia. Psychiatry Res. 2007, 150:51-59.
10. Bazhenov M., Timofeev I., Steriade M., Sejnowski T. Spiking-bursting activity in the thalamic reticular nucleus initiates sequences of spindle oscillations in thalamic networks. J. Neurophysiol. 2000, 84:1076-1087.
11. Behrendt R.P. Contribution of hippocampal region CA3 to consciousness and schizophrenic hallucinations. Neurosci. Biobehav. Rev. 2010, 34:1121-1136.
12. Bellebaum C., Daum I., Koch B., Schwartz M., Hoffman K.-P. The role of the human thalamus in processing corollary discharge. Brain 2005, 128:1139-1154.
13. Berman R.A., Wurtz R.H. Functional identification of a pulvinar path from superior colliculus to cortical area MT. J. Neurosci. 2010, 30(18):6342-6354.
14. Brebion G., Amador X., David A., Malaspina D., Sharif Z., Gorman J.M. Positive symptomatology and source-monitoring failure in schizophrenia-an analysis of symptom-specific effects. Psychiatry Res. 2000, 95(2):119-131.
15. Brickman A.M., Buchsbaum M.S., Shihabuddin L., Byne W., Newmark R.E., Brand J., Ahmed S., Mitelman S.A., Hazlett E.A. Thalamus size and outcome in schizophrenia. Schizophr. Res. 2004, 71:473-484.
16. Browne R.G., Welch W.M. Stereoselective antagonism of phencyclidine's discriminative properties by adenosine receptor agonists. Science 1982, 4565:1157-1159.
17. Brunstein M.G., Belmonte-d-Abreu P., Souza D.O., Lara D.R. Therapeutic benefit of adjunctive dipyridamole in schizophrenia is probably due to adenosine-glutamate interactions. J. Clin. Pharm. Ther. 2001, 2:155-156.
18. Brunstein M.G., Ghisolfe E.S., Ramos F.L., Lara D.R. Clinical trial for allopurinol adjuvant therapy for poorly responsive schizophrenia. Schizophr. Res. 2004, S142.
19. Buzsaki G. Petit mal epilepsy and parkinsonian tremor: hypothesis of a common pacemaker. Neuroscience 1990, 36(1):1-14.
20. Buzsaki G. The thalamic clock: emergent network properties. Neuroscience 1991, 41(2/3):351-364.
21. Bymaster F.P., Shannon H.E., Rasmussen K., Delapp N.W., Mitch C.H., Ward J.S., Calligaro D.O., Ludvigsen T.S., Sheardown M.J., Olesen P.H., Swedberg M.D., Sauerberg P., Fink-Gensen A. Unexpected antipsychotic-like activity with the muscarinic receptor ligand (5R,6R)6-(3-propylthio-1,2,5-thiadiazol-4-yl)-1-azabicyclo[3.2.1]octane. Eur. J. Pharmacol. 1998, 356:109-119.
22. Byne W., Hazlett E.A., Buchsbaum M.S., Kemether E. The thalamus and schizophrenia: current status of research. Acta Neuropathol. 2009, 117:347-368.
23. Cochran S.M., Kennedy M., McKerchar C.E., Steward L.J., Pratt J.A., Morris B.J. Induction of metabolic hypofunction and neurochemical deficits after chronic intermittent exposure to phencyclidine: differential modulation by antipsychotic drugs. Neuropsychopharmacology 2003, 28:265-275.
24. Cox C.L., Sherman S.M. Glutamate inhibits thalamic reticular neurons. J. Neurosci. 1999, 19:6694-6699.
25. Crick F. Function of the thalamic reticular complex: the searchlight hypothesis. Proc. Natl. Acad. Sci. U. S. A. 1984, 81:4586-4590.
26. Crunelli V., Leresche N. A role for GABAB receptors in excitation and inhibition of thalamocortical cells. Trends Neurosci. 1991, 14(1):16-21.
27. D'Aleo G., Cammaroto S., Rifici C., Marra G., Sessa E., Bramanti P., Di Bella P. Hallucinations after abrupt withdrawal of oral and intrathecal baclofen. Funct. Neurol. 2007, 22:81-88.
28. Danos P., Baumann B., Kramer A., Bernstein H.G., Stauch R., Krell D., Falkai P., Bogerts B. Volumes of association thalamic nuclei in schizophrenia: a postmortem study. Schizophr. Res. 2003, 60:141-155.
29. Daskalakis Z.J., George T.P. Clozapine, GABA B, and the treatment of resistant schizophrenia. J. Clin. Pharm. Ther. 2009, 86:442-446.
30. Destexhe A., Sejnowski T.J. The initiation of bursts in thalamic neurons and the cortical control of thalamic sensitivity. Philos. Trans. R. Soc. Lond. B 2002, 357:1649-1657.
31. Fanselow E.F., Sameshima K., Baccala L.A., Nicolelis M.A.L. Thalamic bursting in rats during different awake behavioral states. Proc. Natl. Acad. Sci. U. S. A. 2001, 98(26):15330-15335.
32. Feinberg I. Corollary discharge, hallucinations and dreaming. Schizophr. Bull. 2011, 37(1):1-3.
33. Ferrarelli F., Huber R., Peterson M.J., Massimini M., Murphy M., Riedner B.A., Watson A., Bria P., Tononi G. Reduced sleep spindle activity in schizophrenia patients. Am. J. Psychiatry 2007, 164:483-492.
34. Ferrarelli F., Peterson M.J., Sarasso S., Riedner B.A., Murphy M.J., Benca R.M., Bria P., Kalin N.H., Tononi G. Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles. Am. J. Psychiatry 2010, 167:1339-1348.
35. Floran B., Floran L., Erlij D., Aceves J. Activation of dopamine D4 receptors modulates [3H]GABA release in slices of the rat thalamic reticular nucleus. Neuropharmacology 2004, 46(4):497-503.
36. Ford J.M., Mathalon D.H., Whitfield S., Faustman W.O., Roth W.T. Reduced communication between frontal and temporal lobes during talking in schizophrenia. Biol. Psychiatry 2002, 52:485-492.
37. Ford J.M., Gray M., Faustman W.O., Roach B.J., Mathalon D.H. Dissecting corollary discharge dysfunction in schizophrenia. Psychophysiology 2007, 44:522-529.
38. Franck N., Farrer C., Georgieff N., Marie-Cardine M., Dalery J., d'Amato T., Jeannerodm M. Defective recognition of one's own actions in schizophrenic patients. Am. J. Psychiatry 2001, 158:454-459.
39. Frith C.D., Blackemore S.J., Wolpert D.M. Explaining the symptoms of schizophrenia: abnormalities in the awareness of action. Brain Res. Rev. 2000, 31:357-363.
40. Fuster J.M. The Prefrontal Cortex 2008, Elsevier, London, UK. 4th ed.
41. Govindaiah G., Cox C.L. Excitatory actions of dopamine via D1-like receptors in the rat lateral geniculate nucleus. J. Neurophysiol. 2005, 94(6):3708-3718.
42. Govindaiah G., Cox C.L. Metabotropic glutamate receptors differentially regulate GABAergic inhibition in thalamus. J. Neurosci. 2006, 26(52):13443-13453.
43. Govindaiah G., Cox C.L. Excitatory actions of synaptically released catecholamines in the rat lateral geniculate nucleus. Neuroscience 2006, 137:671-683.
44. Govindaiah G., Wang T., Gilette M.U., Crandall S.R., Cox C.L. Regulation of inhibitory synapses by presynaptic D4 dopamine receptors in thalamus. J. Neurophysiol. 2010, 104:2757-2765.
45. Govindaiah G., Wang Y., Cox C.L. Dopamine enhances the excitability of somatosensory thalamocortical neurons. Neuroscience 2010, 170(4):981-991.
46. Gray J.A. Integrating schizophrenia. Schizophr. Bull. 1998, 24:249-266.
47. Guillery R.W., Sherman S.M. Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron 2002, 33:163-175.
48. Guillery R.W., Sherman S.M. Branched thalamic afferents: what are the messages that they relay to the cortex?. Brain Res. Rev. 2010, 66:205-219.
49. Huffaker S.J., Chan J., Nicodemus K.K., Sambataro F., Yang F., Mattay V., Lipska B.K., Hyde T.M., Song J., Rujescu D., Giegling I., Mayilyan K., Proust M.J., Soghoyan A., Caforio G., Callecott J.H., Bertolino A., Meyer-Lindenberg A., Chang J., Ji Y., Egan M.F., Goldberg T.E., Kleinman J.E., Lu B., Weinberger D.R. Primate-specific, brain isoform of KCNH2 affects cortical physiology, cognition, neuronal repolarization and risk of schizophrenia. Nat. Med. 2009, 15:509-518.
50. Johns L.C., Rossell S., Frith C., Agmad F., Hemsley D., Kuipers E., McGuire P.K. Verbal self-monitoring and auditory verbal hallucinations in patients with schizophrenia. Psychol. Med. 2001, 31:705-715.
51. Jones C.K., Eberle E.L., Shaw D.B., McKinzie D.L., Shannon H.E. Pharmacologic interactions between the muscarinic cholinergic and dopaminergic systems in the modulation of prepulse inhibition in rats. J. Pharmacol. Exp. Ther. 2005, 312:1055-1063.
52. Kafka S.H., Corbett R. Selective adenosine A2A receptor-dopamine D2 receptor interactions in animal models of schizophrenia. Eur. J. Pharmacol. 1996, 2-3:147-154.
53. Keefe R.S., Arnold M.C., Bayen U.K., Harvey P.D. Source-monitoring deficits in patients with schizophrenia: a multinomial modeling analysis. Psychol. Med. 1999, 29(4):903-914.
54. Keefe R.S., Arnold M.C., Bayen U.K., McEvoy J.P., Wilson W.H. Source monitoring deficits for self-generated stimuli in schizophrenia: multinomial modeling of data from three sources. Schizophr. Res. 2002, 57:51-67.
55. Kehrer C., Maziashvili N., Dugladze T., Gloveli T. Altered excitatory-inhibitory balance in the NMDA-hypofunction model of schizophrenia. Front. Mol. Neurosci. 2008, 1(6):1-7.
56. Kim U., Sanchez-Vives M.V., McCormick D.A. Functional dynamics of GABAergic inhibition in the thalamus. Science 1997, 278(5335):130-134.
57. Krahe R., Gabbiani F. Burst firing in sensory systems. Nat. Rev. Neurosci. 2004, 5:13-23.
58. Kramer M.S., Last B., Getson A., Reines S.A. The effects of a selective D4 dopamine receptor antagonist (L745,870) in acutely psychotic inpatients with schizophrenia. Arch. Gen. Psychiatry 1997, 54(6):567-572.
59. Kumari V., Fannon D., Ffytuche D.H., Raveenrdran V., Antonova E., Premkumar P., et al. Functional MRI of verbal self-monitoring in schizophrenia: performance and illness-specific effects. Schizophr. Bull. 2010, 36(4):740-755.
60. Lara D.R., Brunstein M.G., Ghisolfi E.S., Lobato M.I., Belmonte-de-Abreu P., Souza D.O. Allopurinol augmentation for poorly responsive schizophrenia. Int. Clin. Psychopharmacol. 2001, 4:235-237.
61. Lara D.R., Dall-Egna O.P., Ghisolfi E.S., Brunstein M.G. Involvement of adenosine in the neurobiology of schizophrenia and its therapeutic implications. Prog. Neuropsychopharmacol. Biol. Psychiatry 2006, 30:617-629.
62. Lavine A., Grace A.A. Dopamine modulates the responsivity of mediodorsal thalamic cells recorded in vitro. J. Neurosci. 1998, 18(24):10566-10578.
63. Lieberman J.A., Stroup T.S., McEvoy J.P., Swartz M.S., Rosenheck R.A., Perkins D.O., Keefe R.S., Davis S.M., Davis C.E., Lebowitz B.D., Severe J., Hsiao J.K. Effectiveness of antipsychotic drugs in patients with chronic schizophrenia. N. Engl. J. Med. 2005, 353(12):1209-1223.
64. Madeja M., Margineanu D.G., Gorji A., Siep E., Boerrigter P., Klitgaard H., Speckmann E.J. Reduction of voltage-operated potassium currents by levetiracetam: a novel antiepileptic mechanism of action?. Neuropharmacology 2003, 45:661-671.
65. Malenka R.C., Angel R.W., Thieman S., Weitz C.J., Berger P.A. Central error-correcting behavior in schizophrenia and depression. Biol. Psychiatry 1986, 21:263-273.
66. Malhotra T., Rosenzweig I. Baclofen withdrawal causes psychosis in otherwise unclouded consciousness. J. Neuropsychiatry Clin. Neurosci. 2009, 21:476.
67. McCormick D.A. Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog. Neurobiol. 1992, 39:337-388.
68. Mitelman S.A., Byne W., Kemether E., Hazlett E.A., Buchsbaum M.S. Metabolic disconnection between the mediodorsal nucleus of the thalamus and cortical Brodmann's areas of the left hemisphere in schizophrenia. Am. J. Psychiatry 2005, 162:1733-1735.
69. Moghaddam B., Adams B.W. Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats. Science 1998, 281:1349-1352.
70. Mölle M., Marshall L., Gais S., Born J. Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J. Neurosci. 2002, 22(24):10941-10947.
71. Mooney D.M., Zhang L., Basile C., Senatorov V.V., Ngsee J., Omar A., Hu B. Distinct forms of cholinergic modulation in parallel thalamic sensory pathways. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:320-324.
72. Mrzljak L., Bergson C., Pappy M., Huff R., Levenson R., Goldman-Rakic P.S. Localization of dopamine D4 receptors in GABAergic neurons of the primate brain. Nature 1996, 381:245-248.
73. Nicolelis M.A.L., Fanselow E.F. Dynamic shifting in thalamocortical processing during different behavioural states. Philos. Trans. R. Soc. Lond. B 2002, 357:1753-1758.
74. Ostendorf F., Liebermann D., Ploner C.J. Human thalamus contributes to perceptual stability across eye movements. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(3):1229-1234.
75. Papa M., Boscea F., Canitano A., Castaldo P., Selletti S., Annunziato L., Taglealatela M. Expression pattern of the ether-a-gogo-related (ERG) K+ channel-encoding genes ERG1, ERG2, and ERG3 in the adult rat central nervous system. J. Comp. Neurol. 2003, 466:119-135.
76. Patil S.T., Zhang L., Martenyi F., Lowe S.L., Jackson K.A., Andreev B.V., Avedisova A.S., Bardenstein L.M., Gurovich I.Y., Morozova M.A., Mosolov S.N., Neznanov N.G., Reznik A.M., Smulevich A.B., Tochilov V.A., Johnson B.G., Monn J.A., Schoepp D.D. Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a randomized phase 2 clinical trial. Nat. Med. 2007, 13:1102-1107.
77. Pinault D. Dysfunctional thalamus-related networks in schizophrenia. Schizophr. Bull. 2011, 37(2):238-243.
78. Popoli P., Reggio R., Pezzola A. Adenosine A1 and A2 receptor agonists significantly prevent the electroencephalographic effects induced by MK-801 in rats. Eur. J. Pharmacol. 1997, 2-3:143-146.
79. Raedler T.J., Bymaster F.P., Tandon R., Copolov D., Dean B. Towards a muscarinic hypothesis of schizophrenia. Mol. Psychiatry 2007, 12:232-246.
80. Ramcharan E.J., Gnadt J.W., Sherman S.M. Higher-order thalamic relays burst more than first-order relays. Proc. Natl. Acad. Sci. USA 2005, 102(34):12236-12241.
81. Rasmussen T., Fink-Gensen A., Sauerberg P., Swedberg M.D., Thomsen C., Sheardown M.G., Jeppesen L., Calligaro D.O., DeLapp N.W., Whitesitt C., Ward J.S., Shannon H.E., Bymaster F.P. The muscarinic receptor agonist BuTAC, a novel potential antipsychotic, does not impair learning and memory in mouse passive avoidance. Schizophr. Res. 2001, 49:193-201.
82. Rieck R.W., Ansari M.S., Whetsell W.O., Deutsch A.Y., Kessler R.M. Distribution of dopamine D2-like receptors in the human thalamus: autoradiographic and PET studies. Neuropsychopharmacology 2004, 29:362-372.
83. Rimondini R., Ferre S., Ogren S.O., Fuxe K. Adenosine A2A agonists: a potential new type of atypical antipsychotic. Neuropsychopharmacology 1997, 2:82-91.
84. Rogawski M.A., Aghajanian G.K. Activation of lateral geniculate neurons by norepinephrine: mediation by an alpha-adrenergic receptor. Brain Res. 1980, 182:345-359.
85. Rosenzweig I., Valentin A., Brex P.A., Elwes R.D., Alarcon G. Face-related ictal hallucinations and illusions and reflex-type phenomena. J. Neuropsychiatry Clin. Neurosci. 2009, 21:469-470.
86. Saganich M.J., Machado E., Rudy B. Differential expression of genes encoding subthreshold-operating voltage-gated K+ channels in brain. J. Neurosci. 2001, 21:4609-4624.
87. Sanchez-Gonzalez M.A., Garcia-Cabezas M.A., Rico B., Cavada C. The primate thalamus is a key target for brain dopamine. J. Neurosci. 2005, 25(26):6076-6083.
88. Seeman P., Chau-Wong M., Tedesco J., Wong K. Brain receptors for antipsychotic drugs and dopamine: direct binding assays. Proc. Natl. Acad. Sci. U. S. A. 1975, 72:4376-4380.
89. Seeman P., Guan H.C., Van Tol H.H.M. Dopamine D4 receptors elevated in schizophrenia. Nature 1993, 365:441-445.
90. Sharp F.R., Tomitaka M., Bemaudin M., Tomitaka S. Psychosis: pathological activation of limbic thalamocortical circuits by psychomimetics and schizophrenia?. Trends Neurosci. 2001, 24(5):330-334.
91. Sherman S.M. Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci. 2001, 24(2):122-126.
92. Sherman S.M., Guillery R.W. Exploring the Thalamus and its Role in Cortical Function 2006, The MIT Press, Cambridge, MA. 2nd ed.
93. Sherman S.M., Guillery R.W. Distinct functions for direct and transthalamic corticocortical connections. J. Neurophysiol. 2011, 106:1068-1077.
94. Sillis T.L., Azampanah A., Fletcher P.J. The adenosine A1 receptor agonist N6-cyclopentyladenosine blocks the disruptive effect of phencyclidine on prepulse inhibition of the acoustic startle response in the rat. Eur. J. Pharmacol. 1999, 3:325-329.
95. Sotti F., Damgaard T., Montezinho L.P., Mork A., Olsen C.K., Bundgaard C., Husum H. Antipsychotic-like effects of retigabine [N-(2-amino-4-(fluorobenzylamino)-phenyl)carbamic acid ester], a KCNQ potassium channel opener, via modulation of mesolimbic dopaminergic neurotransmission. J. Pharmacol. Exp. Ther. 2009, 328(3):951-962.
96. Steriade M. Neuronal Substrates of Sleep and Epilepsy 2003, Cambridge University Press, Cambridge, UK.
97. Steriade M. Grouping of brain rhythms in corticothalamic systems. Neuroscience 2006, 137:1087-1106.
98. Tanibuchi I., Goldman-Rakic P.S. Dissociation of spatial-, object-, and sound-coding neurons in the mediodorsal nucleus of the primate thalamus. J. Neurophysiol. 2003, 89:1067-1077.
99. Turner J.P., Salt T.E. Group II and III metabotropic glutamate receptors and the control of nucleus reticularis thalami input to rat thalamocortical neurones in vitro. Neuroscience 2003, 122:459-469.
100. Varela C., Sherman S.M. Differences in response to muscarinic activation between first and higher order thalamic relays. J. Neurophysiol. 2007, 98:3547-3583.
101. Vukadinovic Z. Sleep abnormalities in schizophrenia may suggest impaired trans-thalamic cortico-cortical communication: towards a dynamic model of the illness. Eur. J. Neurosci. 2011, 34(7):1031-1039.
102. Wade J.F., Dang C.V., Nelson L., Wasserberger J. Emergent complications of the newer anticonvulsants. J. Emerg. Med. 2010, 38:231-237.
103. Wieronska J.M., Kusek M., Tokarski K., Wabno J., Froesti W., Pilc A. The GABA B receptor agonist CGP44532 and the positive modulator GS39783 reverse some behavioural changes related to positive syndromes of psychosis in mice. Br. J. Pharmacol. 2011, 163(5):1034-1047.
104. Woodward T.S., Weinstein S., Cairo T.A., Metzak P., Ngan E.T.C., Kumar D. Hallucinations are associated with aberrant activation in inner speech regions during source monitoring. Schizophr. Res. Suppl. 2008, 102(2):96.
105. Wurtz R.H., Sommer M.A. Identifying corollary discharges for movement in the prime brain. Prog. Brain Res. 2004, 144:47-60.
106. Zhang Z.W., Deschenes M. Projections to layer VI of the posteromedial barrel field in the rat: a reappraisal of the role of corticothalamic pathways. Cereb. Cortex 1998, 8(5):428-436.
107. Zhao Y., Kerscher N., Eysel U., Funke K. D1 and D2 receptor-mediated dopaminergic modulation of visual responses in cat dorsal lateral geniculate nucleus. J. Physiol. 2002, 539(1):223-238.
108. Zhu J.J., Lo F.S. Control of recurrent inhibition of the lateral posterior-pulvinar complex by afferents from the deep layers of the superior colliculus of the rabbit. J. Neurophysiol. 1998, 80:1122-1131.
109. Zhu J.J., Lo F.S. Three GABA receptor-mediated postsynaptic potentials in interneurons in the rat lateral geniculate nucleus. J. Neurosci. 1999, 19(14):5721-5730.
110. Zikopoulos B., Barbas H. Circuits for multisensory integration and attentional modulation through the prefrontal cortex and the thalamic reticular nucleus in primates. Rev. Neurosci. 2007, 18:417-438.