Inhibition of Mediodorsal Thalamus Disrupts Thalamofrontal Connectivity and Cognition

Neuron

Volumn 77, Issue 6, 2013, Pages 1151-1162

  Parnaudeau, Sebastien ^a,b   O'Neill, Pia Kelsey ^a   Bolkan, Scott S ^a,b   Ward, Ryan D ^a   Abbas, Atheir I ^a   Roth, Bryan L ^c   Balsam, Peter D ^a   Gordon, Joshua A ^a   Kellendonk, Christoph ^a,b  

^a NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUSCARINIC M4 RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BETA RHYTHM; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; GAMMA RHYTHM; IN VIVO STUDY; MALE; MEMORY DISORDER; MOUSE; NERVE CELL; NONHUMAN; PHARMACOGENETICS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHIZOPHRENIA; TASK PERFORMANCE; THALAMUS DORSOMEDIAL NUCLEUS; THETA RHYTHM; WORKING MEMORY;

ANIMALS; COGNITION; MALE; MEDIODORSAL THALAMIC NUCLEUS; MEMORY, SHORT-TERM; MICE; MICE, INBRED C57BL; NEURAL INHIBITION; NEURAL PATHWAYS; PREFRONTAL CORTEX; PSYCHOMOTOR PERFORMANCE;

EID: 84875512175     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.01.038     Document Type: Article

References (59)

1. Adhikari A., Topiwala M.A., Gordon J.A. Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 2010, 65:257-269.
2. Alexander G.M., Rogan S.C., Abbas A.I., Armbruster B.N., Pei Y., Allen J.A., Nonneman R.J., Hartmann J., Moy S.S., Nicolelis M.A., et al. Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 2009, 63:27-39.
3. 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.
4. Armbruster B.N., Li X., Pausch M.H., Herlitze S., Roth B.L. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl. Acad. Sci. USA 2007, 104:5163-5168.
5. Bailey K.R., Mair R.G. Lesions of specific and nonspecific thalamic nuclei affect prefrontal cortex-dependent aspects of spatial working memory. Behav. Neurosci. 2005, 119:410-419.
6. Bechara A., Damasio H., Tranel D., Anderson S.W. Dissociation of working memory from decision making within the human prefrontal cortex. J. Neurosci. 1998, 18:428-437.
7. Beracochea D.J., Jaffard R., Jarrard L.E. Effects of anterior or dorsomedial thalamic ibotenic lesions on learning and memory in rats. Behav. Neural Biol. 1989, 51:364-376.
8. Berlin H.A., Rolls E.T., Kischka U. Impulsivity, time perception, emotion and reinforcement sensitivity in patients with orbitofrontal cortex lesions. Brain 2004, 127:1108-1126.
9. Block A.E., Dhanji H., Thompson-Tardif S.F., Floresco S.B. Thalamic-prefrontal cortical-ventral striatal circuitry mediates dissociable components of strategy set shifting. Cereb. Cortex 2007, 17:1625-1636.
10. Boulougouris V., Dalley J.W., Robbins T.W. Effects of orbitofrontal, infralimbic and prelimbic cortical lesions on serial spatial reversal learning in the rat. Behav. Brain Res. 2007, 179:219-228.
11. Byne W., Hazlett E.A., Buchsbaum M.S., Kemether E. The thalamus and schizophrenia: current status of research. Acta Neuropathol. 2009, 117:347-368.
12. Chudasama Y., Bussey T.J., Muir J.L. Effects of selective thalamic and prelimbic cortex lesions on two types of visual discrimination and reversal learning. Eur. J. Neurosci. 2001, 14:1009-1020.
13. Deiber M.P., Missonnier P., Bertrand O., Gold G., Fazio-Costa L., Ibañez V., Giannakopoulos P. Distinction between perceptual and attentional processing in working memory tasks: a study of phase-locked and induced oscillatory brain dynamics. J. Cogn. Neurosci. 2007, 19:158-172.
14. Dias R., Aggleton J.P. Effects of selective excitotoxic prefrontal lesions on acquisition of nonmatching- and matching-to-place in the T-maze in the rat: differential involvement of the prelimbic-infralimbic and anterior cingulate cortices in providing behavioural flexibility. Eur. J. Neurosci. 2000, 12:4457-4466.
15. Dias R., Robbins T.W., Roberts A.C. Dissociation in prefrontal cortex of affective and attentional shifts. Nature 1996, 380:69-72.
16. Dias R., Robbins T.W., Roberts A.C. Dissociable forms of inhibitory control within prefrontal cortex with an analog of the Wisconsin Card Sort Test: restriction to novel situations and independence from "on-line" processing. J. Neurosci. 1997, 17:9285-9297.
17. Engel A.K., Fries P. Beta-band oscillations-signalling the status quo?. Curr. Opin. Neurobiol. 2010, 20:156-165.
18. Floresco S.B., Braaksma D.N., Phillips A.G. Thalamic-cortical-striatal circuitry subserves working memory during delayed responding on a radial arm maze. J. Neurosci. 1999, 19:11061-11071.
19. Forbes N.F., Carrick L.A., McIntosh A.M., Lawrie S.M. Working memory in schizophrenia: a meta-analysis. Psychol. Med. 2009, 39:889-905.
20. Funahashi S., Bruce C.J., Goldman-Rakic P.S. Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic "scotomas". J. Neurosci. 1993, 13:1479-1497.
21. Garner A.R., Rowland D.C., Hwang S.Y., Baumgaertel K., Roth B.L., Kentros C., Mayford M. Generation of a synthetic memory trace. Science 2012, 335:1513-1516.
22. Green M.F. What are the functional consequences of neurocognitive deficits in schizophrenia?. Am. J. Psychiatry 1996, 153:321-330.
23. Guettier J.M., Gautam D., Scarselli M., Ruiz de Azua I., Li J.H., Rosemond E., Ma X., Gonzalez F.J., Armbruster B.N., Lu H., et al. A chemical-genetic approach to study G protein regulation of beta cell function in vivo. Proc. Natl. Acad. Sci. USA 2009, 106:19197-19202.
24. Haber S.N., Calzavara R. The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res. Bull. 2009, 78:69-74.
25. Hornak J., O'Doherty J., Bramham J., Rolls E.T., Morris R.G., Bullock P.R., Polkey C.E. Reward-related reversal learning after surgical excisions in orbito-frontal or dorsolateral prefrontal cortex in humans. J. Cogn. Neurosci. 2004, 16:463-478.
26. Hunt P.R., Aggleton J.P. Medial dorsal thalamic lesions and working memory in the rat. Behav. Neural Biol. 1991, 55:227-246.
27. Hunt P.R., Aggleton J.P. Neurotoxic lesions of the dorsomedial thalamus impair the acquisition but not the performance of delayed matching to place by rats: a deficit in shifting response rules. J. Neurosci. 1998, 18:10045-10052.
28. Jahnsen H., Llinás R. Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J. Physiol. 1984, 349:227-247.
29. Jann M.W., Lam Y.W., Chang W.H. Rapid formation of clozapine in guinea-pigs and man following clozapine-N-oxide administration. Arch. Int. Pharmacodyn. Ther. 1994, 328:243-250.
30. Jones E.G. The Thalamus 2007, Cambridge University Press, New York. 2nd Edition.
31. Jones M.W., Wilson M.A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol. 2005, 3:e402.
32. Kellendonk C., Simpson E.H., Polan H.J., Malleret G., Vronskaya S., Winiger V., Moore H., Kandel E.R. Transient and selective overexpression of dopamine D2 receptors in the striatum causes persistent abnormalities in prefrontal cortex functioning. Neuron 2006, 49:603-615.
33. Kuroda M., Yokofujita J., Murakami K. An ultrastructural study of the neural circuit between the prefrontal cortex and the mediodorsal nucleus of the thalamus. Prog. Neurobiol. 1998, 54:417-458.
34. Lavin A., Grace A.A. Response of the ventral pallidal/mediodorsal thalamic system to antipsychotic drug administration: involvement of the prefrontal cortex. Neuropsychopharmacology 1998, 18:352-363.
35. Leeson V.C., Robbins T.W., Matheson E., Hutton S.B., Ron M.A., Barnes T.R., Joyce E.M. Discrimination learning, reversal, and set-shifting in first-episode schizophrenia: stability over six years and specific associations with medication type and disorganization syndrome. Biol. Psychiatry 2009, 66:586-593.
36. Löffler S., Körber J., Nubbemeyer U., Fehsel K. Comment on "Impaired respiratory and body temperature control upon acute serotonergic neuron inhibition". Science 2012, 337:646.
37. Marenco S., Stein J.L., Savostyanova A.A., Sambataro F., Tan H.Y., Goldman A.L., Verchinski B.A., Barnett A.S., Dickinson D., Apud J.A., et al. Investigation of anatomical thalamocortical connectivity and FMRI activation in schizophrenia. Neuropsychopharmacology 2012, 37:499-507.
38. McOmish C.E., Lira A., Hanks J.B., Gingrich J.A. Clozapine-induced locomotor suppression is mediated by 5-HT(2A) receptors in the forebrain. Neuropsychopharmacology 2012, 37:2747-2755.
39. Minzenberg M.J., Laird A.R., Thelen S., Carter C.S., Glahn D.C. Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. Arch. Gen. Psychiatry 2009, 66:811-822.
40. Mitchell A.S., Dalrymple-Alford J.C. Dissociable memory effects after medial thalamus lesions in the rat. Eur. J. Neurosci. 2005, 22:973-985.
41. Mitelman S.A., Byne W., Kemether E.M., 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.
42. Neave N., Sahgal A., Aggleton J.P. Lack of effect of dorsomedial thalamic lesions on automated tests of spatial memory in the rat. Behav. Brain Res. 1993, 55:39-49.
43. Pettersson-Yeo W., Allen P., Benetti S., McGuire P., Mechelli A. Dysconnectivity in schizophrenia: where are we now?. Neurosci. Biobehav. Rev. 2011, 35:1110-1124.
44. Ray R.S., Corcoran A.E., Brust R.D., Kim J.C., Richerson G.B., Nattie E., Dymecki S.M. Impaired respiratory and body temperature control upon acute serotonergic neuron inhibition. Science 2011, 333:637-642.
45. Rolls E.T., Hornak J., Wade D., McGrath J. Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. J. Neurol. Neurosurg. Psychiatry 1994, 57:1518-1524.
46. Rygula R., Walker S.C., Clarke H.F., Robbins T.W., Roberts A.C. Differential contributions of the primate ventrolateral prefrontal and orbitofrontal cortex to serial reversal learning. J. Neurosci. 2010, 30:14552-14559.
47. Schoenbaum G., Nugent S.L., Saddoris M.P., Setlow B. Orbitofrontal lesions in rats impair reversal but not acquisition of go, no-go odor discriminations. Neuroreport 2002, 13:885-890.
48. Siapas A.G., Lubenov E.V., Wilson M.A. Prefrontal phase locking to hippocampal theta oscillations. Neuron 2005, 46:141-151.
49. Siegel M., Warden M.R., Miller E.K. Phase-dependent neuronal coding of objects in short-term memory. Proc. Natl. Acad. Sci. USA 2009, 106:21341-21346.
50. Sigurdsson T., Stark K.L., Karayiorgou M., Gogos J.A., Gordon J.A. Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 2010, 464:763-767.
51. Simpson E.H., Kellendonk C., Kandel E. A possible role for the striatum in the pathogenesis of the cognitive symptoms of schizophrenia. Neuron 2010, 65:585-596.
52. Tallon-Baudry C., Bertrand O., Fischer C. Oscillatory synchrony between human extrastriate areas during visual short-term memory maintenance. J. Neurosci. 2001, 21:RC177.
53. Tallon-Baudry C., Mandon S., Freiwald W.A., Kreiter A.K. Oscillatory synchrony in the monkey temporal lobe correlates with performance in a visual short-term memory task. Cereb. Cortex 2004, 14:713-720.
54. Uhlhaas P.J., Singer W. Abnormal neural oscillations and synchrony in schizophrenia. Nat. Rev. 2010, 11:100-113.
55. Vinck M., Battaglia F.P., Womelsdorf T., Pennartz C. Improved measures of phase-coupling between spikes and the local field potential. J. Comput. Neurosci. 2012, 33:53-75.
56. Watanabe Y., Funahashi S. Thalamic mediodorsal nucleus and working memory. Neurosci. Biobehav. Rev. 2012, 36:134-142.
57. Weinberger D.R., Berman K.F. Prefrontal function in schizophrenia: confounds and controversies. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1996, 351:1495-1503.
58. Woodward N.D., Karbasforoushan H., Heckers S. Thalamocortical dysconnectivity in schizophrenia. Am. J. Psychiatry 2012, 169:1092-1099.
59. Yoon T., Okada J., Jung M.W., Kim J.J. Prefrontal cortex and hippocampus subserve different components of working memory in rats. Learn. Mem. 2008, 15:97-105.