NMDA antagonist ketamine reduces task selectivity in macaque dorsolateral prefrontal neurons and impairs performance of randomly interleaved prosaccades and antisaccades

Journal of Neuroscience

Volumn 32, Issue 35, 2012, Pages 12018-12027

  Skoblenick, Kevin ^a   Everling, Stefan ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CHANGE; COGNITION; CONTROLLED STUDY; MACACA MULATTA; MALE; NERVE CONDUCTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; PRIORITY JOURNAL; RESPONSE TIME; SACCADIC EYE MOVEMENT; TASK PERFORMANCE; VISUAL STIMULATION;

ANIMALS; EXCITATORY AMINO ACID ANTAGONISTS; KETAMINE; MACACA MULATTA; MALE; NEURONS; PREFRONTAL CORTEX; PSYCHOMOTOR PERFORMANCE; RANDOM ALLOCATION; RECEPTORS, N-METHYL-D-ASPARTATE; SACCADES;

EID: 84865527147     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1510-12.2012     Document Type: Article

References (76)

1. Adler CM, Malhotra AK, Elman I, Goldberg T, Egan M, Pickar D, Breier A (1999) Comparison of ketamine-induced thought disorder in healthy volunteers and thought disorder in schizophrenia. Am J Psychiatry 156:1646-1649.
2. Asaad WF, Rainer G, Miller EK (2000) Task-specific neural activity in the primate prefrontal cortex. J Neurophysiol 84:451-459.
3. Benes FM, McSparren J, Bird ED, SanGiovanni JP, Vincent SL (1991) Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 48:996-1001.
4. Buckley MJ, Mansouri FA, Hoda H, Mahboubi M, Browning PG, Kwok SC, Phillips A, Tanaka K (2009) Dissociable components of rule-guided behavior depend on distinct medial and prefrontal regions. Science 325:52-58.
5. Bussey TJ, Wise SP, Murray EA (2001) The role of ventral and orbital prefrontal cortex in conditional visuomotor learning and strategy use in rhesus monkeys (Macaca mulatta). Behav Neurosci 115:971-982.
6. Bussey TJ, Wise SP, Murray EA (2002) Interaction of ventral and orbital prefrontal cortex with inferotemporal cortex in conditional visuomotor learning. Behav Neurosci 116:703-715.
7. Condy C, Wattiez N, Rivaud-Péchoux S, Gaymard B (2005) Ketamineinduced distractibility: an oculomotor study in monkeys. Biol Psychiatry 57:366-372.
8. Dawson N, Morris BJ, Pratt JA (2011) Subanaesthetic ketamine treatment alters prefrontal cortex connectivity with thalamus and ascending subcortical systems. Schizophr Bull. Advance online publication. Retrieved July 24, 2012. doi:10.1093/schbul/sbr144.
9. Dorris MC, Paré M, Munoz DP (1997) Neuronal activity in monkey superior colliculus related to the initiation of saccadic eye movements. J Neurosci 17:8566-8579.
10. Duncan GE, Miyamoto S, Leipzig JN, Lieberman JA (1999) Comparison of brain metabolic activity patterns induced by ketamine, MK-801 and amphetamine in rats: support for NMDA receptor involvement in responses to subanesthetic dose of ketamine. Brain Res 843:171-183.
11. Duncan J, Emslie H, Williams P, Johnson R, Freer C (1996) Intelligence and the frontal lobe: the organization of goal-directed behavior. Cogn Psychol 30:257-303.
12. Duncan J, Parr A, Woolgar A, Thompson R, Bright P, Cox S, Bishop S, Nimmo-Smith I (2008) Goal neglect and Spearman's g: competing parts of a complex task. J Exp Psychol Gen 137:131-148.
13. Elvevåg B, Goldberg TE (2000) Cognitive impairment in schizophrenia is the core of the disorder. Crit Rev Neurobiol 14:1-21.
14. Everling S, DeSouza JF (2005) Rule-dependent activity for prosaccades and antisaccades in the primate prefrontal cortex. J Cogn Neurosci 17:1483-1496.
15. Everling S, Fischer B (1998) The antisaccade: a review of basic research and clinical studies. Neuropsychologia 36:885-899.
16. Everling S, Munoz DP (2000) Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. J Neurosci 20:387-400.
17. Everling S, Dorris MC, Klein RM, Munoz DP (1999) Role of primate superior colliculus in preparation and execution of anti-saccades and prosaccades. J Neurosci 19:2740-2754.
18. Everling S, Tinsley CJ, Gaffan D, Duncan J (2006) Selective representation of task-relevant objects and locations in the monkey prefrontal cortex. Eur J Neurosci 23:2197-2214.
19. Fischer B, Boch R, Ramsperger E (1984) Express-saccades of the monkey: effect of daily training on probability of occurrence and reaction time. Exp Brain Res 55:232-242.
20. Flohr H (1992) Qualia and brain processes. In: Emergence or reduction? Essays on the prospects of nonreductive phyiscalism (Beckermann A, Flohr H, Kim J, eds), pp 220-238. Berlin: De Gruyter.
21. Ford KA, Everling S (2009) Neural activity in primate caudate nucleus associated with pro- and antisaccades. J Neurophysiol 102:2334-2341.
22. Fukumoto-Motoshita M, Matsuura M, Ohkubo T, Ohkubo H, Kanaka N, Matsushima E, Taira M, Kojima T, Matsuda T (2009) Hyperfrontality in patients with schizophrenia during saccade and antisaccade tasks: a study with fMRI. Psychiatry Clin Neurosci 63:209-217.
23. Fukushima J, Fukushima K, Chiba T, Tanaka S, Yamashita I, Kato M (1988) Disturbances of voluntary control of saccadic eye movements in schizophrenic patients. Biol Psychiatry 23:670-677.
24. Goeree R, Farahati F, Burke N, Blackhouse G, O'Reilly D, Pyne J, Tarride JE (2005) The economic burden of schizophrenia in Canada in 2004. Curr Med Res Opin 21:2017-2028.
25. Goldman-Rakic PS, Castner SA, Svensson TH, Siever LJ, Williams GV (2004) Targeting the dopamine D1 receptor in schizophrenia: insights for cognitive dysfunction. Psychopharmacology (Berl) 174:3-16.
26. Gottlieb J, Goldberg ME (1999) Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task. Nat Neurosci 2:906-912.
27. Guitton D, Buchtel HA, Douglas RM (1985) Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goaldirected saccades. Exp Brain Res 58:455-472.
28. Holcomb HH, Lahti AC, Medoff DR, Cullen T, Tamminga CA (2005) Effects of noncompetitive NMDA receptor blockade on anterior cingulated cerebral blood flow in volunteers with schizophrenia. Neuropsychopharmacology 30:2275-2282.
29. Homayoun H, Moghaddam B (2007) NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. J Neurosci 27:11496-11500.
30. Honey RA, Honey GD, O'Loughlin C, Sharar SR, Kumaran D, Bullmore ET, Menon DK, Donovan T, Lupson VC, Bisbrown-Chippendale R, Fletcher PC (2004) Acute ketamine administration alters the brain responses to executive demands in a verbal working memory task: an FMRI study. Neuropsychopharmacology 29:1203-1214.
31. Hoshi E, Shima K, Tanji J (1998) Task-dependent selectivity of movementrelated neuronal activity in the primate prefrontal cortex. J Neurophysiol 80:3392-3397.
32. Jackson ME, Homayoun H, Moghaddam B (2004) NMDA receptor hypofunction produces concomitant firing rate potentiation and burst activity reduction in the prefrontal cortex. Proc Natl Acad Sci U S A 101:8467-8472.
33. Javitt DC (2009) When doors of perception close: bottom-up models of disrupted cognition in schizophrenia. Annu Rev Clin Psychol 5:249-275.
34. Johnston K, Everling S (2006a) Neural activity in monkey prefrontal cortex is modulated by task context and behavioral instruction during delayedmatch- to-sample and conditional prosaccade-antisaccade tasks. J Cogn Neurosci 18:749-765.
35. Johnston K, Everling S (2006b) Monkey dorsolateral prefrontal cortex sends task-selective signals directly to the superior colliculus. J Neurosci 26:12471-12478.
36. Johnston K, Everling S (2009) Task-relevant output signals are sent from monkey dorsolateral prefrontal cortex to the superior colliculus during a visuospatial working memory task. J Cogn Neurosci 21:1023-1038.
37. Johnston K, DeSouza JF, Everling S (2009) Monkey prefrontal cortical pyramidal and putative interneurons exhibit differential patterns of activity between prosaccade and antisaccade tasks. J Neurosci 29:5516-5524.
38. Kiss T, Hoffmann WE, Scott L, Kawabe TT, Milici AJ, Nilsen EA, Hajós M (2011) Role of thalamic projection in NMDA receptor-induced disruption of cortical slow oscillation and short-term plasticity. Front Psychiatry 2:14.
39. Koval MJ, Lomber SG, Everling S (2011) Prefrontal cortex deactivation in macaques alters activity in the superior colliculus and impairs voluntary control of saccades. J Neurosci 31:8659-8668.
40. Krystal JH, Karper LP, Seibyl JP, Freeman GK, Delaney R, Bremner JD, Heninger GR, Bowers MB Jr, Charney DS (1994) Subanesthetic effects of the noncompetitiveNMDAantagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry 51:199-214.
41. Kunimatsu J, Tanaka M (2010) Roles of the primate motor thalamus in the generation of antisaccades. J Neurosci 30:5108-5117.
42. Lahti AC, Koffel B, LaPorte D, Tamminga CA (1995) Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology 13:9-19.
43. Lahti AC, Weiler MA, Tamara Michaelidis BA, Parwani A, Tamminga CA (2001) Effects of ketamine in normal and schizophrenic volunteers. Neuropsychopharmacology 25:455-467.
44. Lewis DA, Pierri JN, Volk DW, Melchitzky DS, Woo TU (1999) Altered GABA neurotransmission and prefrontal cortical dysfunction in schizophrenia. Biol Psychiatry 46:616-626.
45. Lorrain DS, Baccei CS, Bristow LJ, Anderson JJ, Varney MA (2003) Effects of ketamine and N-methyl-D-aspartate on glutamate and dopamine release in the rat prefrontal cortex: modulation by a group II selective metabotropic glutamate receptor agonist LY379268. Neuroscience 117:697-706.
46. Malhotra AK, Pinals DA, Weingartner H, Sirocco K, Missar CD, Pickar D, Breier A (1996) NMDA receptor function and human cognition: the effects of ketamine in healthy volunteers. Neuropsychopharmacology 14:301-307.
47. Malhotra AK, Pinals DA, Adler CM, Elman I, Clifton A, Pickar D, Breier A (1997) Ketamine-induced exacerbation of psychotic symptoms and cognitive impairment in neuroleptic-free schizophrenics. Neuropsychopharmacology 17:141-150.
48. Marek GJ, Behl B, Bespalov AY, Gross G, Lee Y, Schoemaker H (2010) Glutamatergic (N-methyl-D-aspartate receptor) hypofrontality in schizophrenia: too little juice or a miswired brain? Mol Pharmacol 77:317-326.
49. McDowell JE, Brown GG, Paulus M, Martinez A, Stewart SE, Dubowitz DJ, Braff DL (2002) Neural correlates of refixation saccades and antisaccades in normal and schizophrenia subjects. Biol Psychiatry 51:216-223.
50. Mitchell JF, Sundberg KA, Reynolds JH (2007) Differential attentiondependent response modulation across cell classes in macaque visual area V4. Neuron 55:131-141.
51. Morris BJ, Cochran SM, Pratt JA (2005) PCP: from pharmacology to modeling schizophrenia. Curr Opin Pharmacol 5:101-106.
52. Mouri A, Noda Y, Enomoto T, Nabeshima T (2007) Phencyclidine animal models of schizophrenia: approaches from abnormality of glutamatergic neurotransmission and neurodevelopment. Neurochem Int 51:173-184.
53. Munoz DP, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5:218-228.
54. Newcomer JW, Farber NB, Jevtovic-Todorovic V, Selke G, Melson AK, Hershey T, Craft S, Olney JW (1999) Ketamine-induced NMDA receptor hypofunction as a model of memory impairment and psychosis. Neuropsychopharmacology 20:106-118.
55. Olney JW, Newcomer JW, Farber NB (1999) NMDAreceptor hypofunction model of schizophrenia. J Psychiatr Res 33:523-533.
56. Pierrot-Deseilligny C, Rivaud S, Gaymard B, Agid Y (1991) Cortical contro lof reflexive visually-guided saccades. Brain 114:1473-1485.
57. Populin LC (2005) Anesthetics change the excitation/inhibition balance that governs sensory processing in the cat superior colliculus. J Neurosci 25:5903-5914.
58. Pouget P, Wattiez N, Rivaud-Pechoux S, Gaymard B (2010) Rapid development of tolerance to sub-anaesthetic dose of ketamine: an oculomotor study in macaque monkeys. Psychopharmacology (Berl) 209:313-318.
59. Povinelli DJ, Preuss TM (1995) Theory of mind: evolutionary history of a cognitive specialization. Trends Neurosci 18:418-424.
60. Preuss TM (2000) Taking the measure of diversity: comparative alternatives to the model-animal paradigm in cortical neuroscience. Brain Behav Evol 55:287-299.
61. Radant AD, Bowdle A, Cowley DS, Kharasch ED, Roy-Byrne PP (1998) Does ketamine-mediated N-methyl-D-aspartate receptor antagonism cause schizophrenia-like oculomotor abnormalities? Neuropsychopharmacology 19:434-444.
62. Ragland JD, Yoon J, Minzenberg MJ, Carter CS (2007) Neuroimaging of cognitive disability in schizophrenia: search for a pathophysiological mechanism. Int Rev Psychiatry 19:417-427.
63. Rainer G, Asaad WF, Miller EK (1998) Memory fields of neurons in the primate prefrontal cortex. Proc Natl Acad Sci U S A 95:15008-15013.
64. Rotaru DC, Yoshino H, Lewis DA, Ermentrout GB, Gonzalez-Burgos G (2011) Glutamate receptor subtypes mediating synaptic activation of prefrontal cortex neurons: relevance for schizophrenia. J Neurosci 31:142-156.
65. Schlag-Rey M, Amador N, Sanchez H, Schlag J (1997) Antisaccade performance predicted by neuronal activity in the supplementary eye field. Nature 390:398-401.
66. Shen K, Kalwarowsky S, Clarence W, Brunamonti E, Pare M (2010) Beneficial effects of the NMDA antagonist ketamine on decision processes in visual search. J Neurosci 30:9947-9953.
67. Stoet G, Snyder LH (2006) Effects of the NMDA antagonist ketamine on task-switching performance: evidence for specific impairments of executive control. Neuropsychopharmacology 31:1675-1681.
68. Suzuki Y, Jodo E, Takeuchi S, Niwa S, Kayama Y (2002) Acute administration of phencyclidine induces tonic activation of medial prefrontal cortex neurons in freely moving rats. Neuroscience 114:769-779.
69. Taffe MA, Davis SA, Gutierrez T, Gold LH (2002) Ketamine impairs multiple cognitive domains in rhesus monkeys. Drug Alcohol Depend 68:175-187.
70. Tsai G, Passani LA, Slusher BS, Carter R, Baer L, Kleinman JE, Coyle JT (1995) Abnormal excitatory neurotransmitter metabolism in schizophrenic brains. Arch Gen Psychiatry 52:829-836.
71. van Os J, Kapur S (2009) Schizophrenia. Lancet 374:635-645.
72. Watanabe M, Munoz DP (2009) Neural correlates of conflict resolution between automatic and volitional actions by basal ganglia. Eur J Neurosci 30:2165-2176.
73. White IM, Wise SP (1999) Rule-dependent neuronal activity in the prefrontal cortex. Exp Brain Res 126:315-335.
74. Wise SP (2008) Forward frontal fields: phylogeny and fundamental function. Trends Neurosci 31:599-608.
75. Yoshida A, Tanaka M (2009) Enhanced modulation of neuronal activity during antisaccades in the primate globus pallidus. Cereb Cortex 19:206-217.
76. Zhang M, Barash S (2000) Neuronal switching of sensorimotor transformations for antisaccades. Nature 408:971-975.