NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons

Journal of Neuroscience

Volumn 27, Issue 43, 2007, Pages 11496-11500

  Homayoun, Houman ^a   Moghaddam, Bita ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Antipsychotic drugs; Ensemble unit recording; GABA; Glutamate; Metabotropic glutamate receptors; Schizophrenia

Indexed keywords

4 AMINOBUTYRIC ACID; DIZOCILPINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

ANALYTIC METHOD; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; INTERNEURON; NERVE CELL INHIBITION; NERVE CELL STIMULATION; NERVE CONDUCTION; NONHUMAN; PATHOPHYSIOLOGY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SCHIZOPHRENIA;

ANIMALS; HUMANS; INTERNEURONS; NEURAL INHIBITION; NEURONS; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION;

EID: 35548991088     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2213-07.2007     Document Type: Article

References (51)

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. Akbarian S, Kim JJ, Potkin SG, Hagman JO, Tafazzoli A, Bunney Jr WE, Jones EG (1995) Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch Gen Psychiatry 52:258-266.
3. Arvanov VL, Wang RY (1997) NMDA-induced response in pyramidal neurons of the rat medial prefrontal cortex slices consists of NMDA and non-NMDA components. Brain Res 768:361-364.
4. Breier A, Malhotra AK, Pinals DA, Weisenfeld NI, Pickar D (1997) Association of ketamine-induced psychosis with focal activation of the prefrontal cortex in healthy volunteers. Am J Psychiat 154:805-811.
5. Chen L, Muhlhauser M, Yang CR (2003) Glycine tranporter-1 blockade potentiates NMDA-mediated responses in rat prefrontal cortical neurons in vitro and in vivo. J Neurophysiol 89:691-703.
6. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-78.
7. Cochran SM, Fujimura M, Morris BJ, Pratt JA (2003) Acute and delayed effects of phencyclidine upon mRNA levels of markers of glutamatergic and GABAergic neurotransmitter function in the rat brain. Synapse 46:206-214.
8. Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13:99-104.
9. Constantinidis C, Goldman-Rakic P (2002) Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. J Neurophysiol 88:3487-3497.
10. Coyle JT (1996) The glutamatergic dysfunction hypothesis for schizophrenia. Harvard Rev Psychiatry 3:241-253.
11. Coyle JT (2004) The GABA-glutamate connection in schizophrenia: which is the proximate cause? Biochem Pharmacol 68:1507-1514.
12. 2+ dynamics. J Physiol (Lond) 551:67-78.
13. Goldman-Rakic P (1999) The "psychic" neuron of the cerebral cortex. Ann NY Acad Sci 868:13-26.
14. Harrison P, Weinberger D (2005) Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Molecular Psychiat 10:40-68.
15. Hirsch JC, Crepel F (1991) Blockade of NMDA receptors unmasks a long-term depression in synaptic efficacy in rat prefrontal neurons in vitro. Exp Brain Res 85:621-624.
16. Homayoun H, Moghaddam B (2006) Progression of cellular adaptations in medial prefrontal and orbitofrontal cortex in response to repeated amphetamine. J Neurosci 26:8025-8039.
17. Homayoun H, Moghaddam B (2007) Fine-tuning of awake prefrontal cortex neurons by clozapine: comparison with haloperidol and N-desmethylclozapine. Biol Psychiatry 61:679-687.
18. Homayoun H, Jackson ME, Moghaddam B (2004a) Activation of metabotropic glutamate 2/3 (mGlu2/3) receptors reverses the effects of NMDA receptor hypofunction on prefrontal cortex unit activity in awake rats. J Neurophysiol 93:1989-2001.
19. Homayoun H, Stefani MR, Adams BW, Tamagan GD, Moghaddam B (2004b) Functional interaction between NMDA and mGlu5 receptors: effects on working memory, instrumental learning, motor behaviors, and dopamine release. Neuropsychopharmacology 29:1259-1269.
20. Jackson M, 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 USA 101:6391-6396.
21. Javitt DC, Zukin SR (1991) Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 148:1301-1308.
22. Jones RS, Buhl EH (1999) Basket-like interneurones in layer II of the entorhinal cortex exhibit a powerful NMDA-mediated synaptic excitation. Neurosci Lett 149:35-39.
23. Kawaguchi Y (2001) Distinct firing patterns of neuronal subtypes in cortical synchronized activities. J Neurosci 21:7261-7272.
24. Kawaguchi Y, Kubota Y (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70:387-396.
25. Koulakov AA, Raghavachari S, Kepecs A, Lisman JE (2002) Model for a robust neural integrator. Nat Neurosci 5:775-782.
26. Krystal JH, Karper LP, Seibyl JP, Freeman GK, Delaney R, Bremner JD, Heninger GR, Bowers Jr M, Charney DS (1994) Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans: psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry 51:199-214.
27. Krystal JH, D'Souza DC, Mathalon D, Perry E, Belger A, Hoffman R (2003) NMDA receptor antagonist effects, cortical glutamatergic function, and schizophrenia: toward a paradigm shift in medication development. Psychopharmacology (Berl) 169:215-233.
28. Lahti AC, Holocomb HH, Medoff DR, Tammings CA (1995a) Ketamine activates psychosis and alters limbic blood flow in schizophrenia. Neuro-Report 6:869-872.
29. Lahti AC, Koffel B, LaPorte D, Tamminga CA (1995b) Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology 13:9-19.
30. Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6:312-324.
31. Lisman J, Fellous J, Wang X (1998) A role for NMDA-receptor channels in working memory. Nat Neurosci 1:273-275.
32. Luby E, Cohen B, Rosenbaum G, Gottlieb J, Kelley R (1959) Study of a new schizophrenomimetic drug; sernyl. Am Med Assoc Arch Neurol Psychiatry 81:363-369.
33. 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.
34. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.
35. McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782-806.
36. Moghaddam B (2003) Bringing order to the glutamate chaos in schizophrenia. Neuron 40:881-884.
37. Moghaddam B, Adams B (1998) Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats. Science 281:1349-1352.
38. Moghaddam B, Adams B, Verma A, Daly D (1997) Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J Neurosci 17:2921-2927.
39. 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.
40. Olney J, Farber N (1995) Glutamate receptor dysfunction and schizophrenia. Arch Gen Psychiatry 52:998-1007.
41. Patil ST, Zhang L, Martenyi F, Lowe SL, Jackson KA, Andreev BV, Avedisova AS, Bardenstein LM, Gurovich IY, Morozova MA, Mosolov SN, Neznanov NG, Reznik AM, Smulevich AB, Tochilov VA, Johnson BG, Monn JA, Schoepp DD (2007) Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a randomized Phase 2 clinical trial. Nat Med 13:1102-1107.
42. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. San Diego: Academic.
43. Povysheva NV, Gonzalez-Burgos G, Zaitsev AV, Kroner S, Barrionuevo G, Lewis DA, Krimer LS (2006) Properties of excitatory synaptic responses in fast-spiking interneurons and pyramidal cells from monkey and rat prefrontal cortex. Cereb Cortex 16:541-552.
44. Rao A, Cha EM, Craig AM (2000) Mismatched appositions of presynaptic and postsynaptic components in isolated hippocampal neurons. J Neurosci 20:8344-8353.
45. Stefani MR, Moghaddam B (2005) Systemic and prefrontal cortical NMDA receptor blockade differentially affect discrimination learning and set-shift ability in rats. Behav Neurosci 119:420-428.
46. 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. Neurosci 114:769-779.
47. Tierney P, Degenetais E, Thierry AM, Glowinski J, Gioanni Y (2004) Influence of the hippocampus on interneurons of the rat prefrontal cortex. Eur J Neurosci 20:514-524.
48. Verma A, Moghaddam B (1996) NMDA receptor antagonists impair prefrontal cortex function as assessed via spatial delayed alternation performance in rats: modulation by dopamine. J Neurosci 16:373-379.
49. Vollenweider FX, Leenders KL, Oye I, Hell D, Angst J (1997) Differential psychopathology and patterns of cerebral glucose utilisation produced by (S)- and (R)-ketamine in healthy volunteers using positron emission tomography (PET). Eur Neuropsychopharmacol 7:25-38.
50. Wilson FA, O'Scalaidhe SP, Goldman-Rakic PS (1994) Functional synergism between putative γ-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex. Proc Natl Acad Sci USA 91:4009-4013.
51. Wong KF, Wange XJ (2006) A recurrent network mechanism of time integration in perceptual decisions. J Neurosci 26:1314-1328.