Hallucinogen-induced UP states in the brain slice of rat prefrontal cortex: Role of glutamate spillover and NR2B-NMDA receptors

Neuropsychopharmacology

Volumn 31, Issue 8, 2006, Pages 1682-1689

  Lambe, Evelyn K ^a   Aghajanian, George K ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

5 HT2A receptors; Electrophysiology; Extrasynaptic; Glutamate; NMDA receptors; Prefrontal cortex; UP states

Indexed keywords

4 BENZYL ALPHA (4 HYDROXYPHENYL) BETA METHYL 1 PIPERIDINEPROPANOL; DEXTRAN; GLUTAMIC ACID; IFENPRODIL; METABOTROPIC RECEPTOR 2; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PSYCHEDELIC AGENT; RO 256981; SEROTONIN 2A RECEPTOR;

ADDITION REACTION; AFFECT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN SLICE; COGNITION; CONTROLLED STUDY; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; EXTRACELLULAR SPACE; HYPOTHESIS; MACROMOLECULE; NERVE CELL NETWORK; NEUROTRANSMISSION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT; SENSORY SYSTEM; VISCOSITY;

ANIMALS; EXTRACELLULAR SPACE; GLUTAMIC ACID; HALLUCINOGENS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 33746296454     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1300944     Document Type: Article

References (58)

1. 2 receptor regulation of extracellular GABA levels in the prefrontal cortex. Neuropsychopharmacology 20: 92-96.
2. 2A receptors, increases EPSCs in layer V pyramidal cells of prefrontal cortex by an asynchronous mode of glutamate release. Brain Res 825: 161-171.
3. Aoki C, Fujisawa S, Mahadomrongkul V, Shah PJ, Nader K, Erisir A (2003). NMDA receptor blockade in intact adult cortex increases trafficking of NR2A subunits into spines, postsynaptic densities, and axon terminals. Brain Res 963: 139-149.
4. Barbour B, Hausser M (1997). Intersynaptic diffusion of neurotransmitter. Trends Neurosci 20: 377-384.
5. 7 receptors. J Neurosci 24: 4807-4817.
6. 2 receptors and serotonergic axons in rat neocortex. Brain Res 453: 315-328.
7. Charton JP, Herkert M, Becker CM, Schroder H (1999). Cellular and subcellular localization of the 2B-subunit of the NMDA receptor in the adult rat telencephalon. Brain Res 816: 609-617.
8. Conti F, Barbaresi P, Melone M, Ducati A (1999). Neuronal and glial localization of NR1 and NR2A/B subunits of the NMDA receptor in the human cerebral cortex. Cereb Cortex 9: 110-120.
9. 2A receptor in the central nervous system of adult rat. J Comp Neurol 409: 187-209.
10. Diamond JS (2001). Neuronal glutamate transporters limit activation of NMDA receptors by neurotransmitter spillover on CA1 pyramidal cells. J Neurosci 21: 8328-8338.
11. Duguid IC, Smart TG (2004). Retrograde activation of presynaptic NMDA receptors enhances GABA release at cerebellar interneuron-Purkinje cell synapses. Nat Neurosci 7: 525-533.
12. Fellin T, Pascual O, Gobbo S, Pozzan T, Haydon PG, Carmignoto G (2004). Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43: 729-743.
13. Fischer G, Mutel V, Trube G, Malherbe P, Kew JN, Mohacsi E et al (1997). Ro 25-6981, a highly potent and selective blocker of N-methyl-D-aspartate receptors containing the NR2B subunit. Characterization in vitro. J Pharmacol Exp Ther 283: 1285-1292.
14. Fujisawa S, Aoki C (2003). In vivo blockade of N-methyl-D-aspartate receptors induces rapid trafficking of NR2B subunits away from synapses and out of spines and terminals in adult cortex. Neuroscience 121: 51-63.
15. Gabbott PL, Bacon SJ (1996). The organisation of dendritic bundles in the prelimbic cortex (area 32) of the rat. Brain Res 730: 75-86.
16. Gouzoulis-Mayfrank E, Schreckenberger M, Sabri O, Arning C, Thelen B, Spitzer M et al (1999). Neurometabolic effects of psilocybin, 3,4-methylenedioxyethylamphetamine (MDE) and d-methamphetamine in healthy volunteers. A double-blind, placebo-controlled PET study with [18F]FDG. Neuropsychopharmacology 20: 565-581.
17. 2A receptor in rat cerebral cortex and olfactory system revealed by immunohistochemistry using two antibodies raised in rabbit and chicken. Mol Brain Res 54: 199-211.
18. Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, McCormick DA (2005). Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47: 423-435.
19. Higgins GA, Ballard TM, Enderlin M, Haman M, Kemp JA (2005). Evidence for improved performance in cognitive tasks following selective NR2B NMDA receptor antagonist pre-treatment in the rat. Psychopharmacology (Berl) 179: 85-98.
20. Huang YH, Bergles DE (2004). Glutamate transporters bring competition to the synapse. Curr Opin Neurobiol 14: 346-352.
21. 2A serotonin receptors in the primate cerebral cortex: possible site of action of hallucinogenic and antipsychotic drugs in pyramidal cell apical dendrites. Proc Natl Acad Sci 95: 735-740.
22. Janssen WG, Vissavajjhala P, Andrews G, Moran T, Hof PR, Morrison JH (2005). Cellular and synaptic distribution of NR2A and NR2B in macaque monkey and rat hippocampus as visualized with subunit-specific monoclonal antibodies. Exp Neural 191(Suppl 1): S28-S44.
23. Kalandadze A, Wu Y, Robinson MB (2002). Protein kinase C activation decreases cell surface expression of the GLT-1 subtype of glutamate transporter. Requirement of a carboxyl-terminal domain and partial dependence on serine 486. J Biol Chem 277: 45741-45750.
24. Kullmann DM, Erdemli G, Asztely F (1996). LTP of AMPA and NMDA receptor-mediated signals: evidence for presynaptic expression and extrasynaptic glutamate spill-over. Neuron 17: 461-474.
25. Lambe EK, Aghajanian GK (2003). Hypocretin (orexin) induces calcium transients in single spines postsynaptic to identified thalamocortical boutons in prefrontal slice. Neuron 40: 139-150.
26. Liu XB, Murray KD, Jones EG (2004). Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J Neurosci 24: 8885-8895.
27. Lozovaya NA, Grebenyuk SE, Tsintsadze T, Feng B, Monaghan DT, Krishtal OA (2004). Extrasynaptic NR2B and NR2D subunits of NMDA receptors shape 'superslow' afterburst EPSC in rat hippocampus. J Physiol 558: 451-463.
28. 2A receptor or alpha1-adrenoceptor activation induces excitatory postsynaptic currents in layer V pyramidal cells of the medial prefrontal cortex. Eur J Pharmacol 367: 197-206.
29. Melendez RI, Vuthiganon J, Kalivas PW (2005). Regulation of extracellular glutamate in the prefrontal cortex: focus on the cystine glutamate exchanger and group I metabotropic glutamate receptors. J Pharmacol Exp Ther 314: 139-147.
30. Merchant RE, Bullock MR, Carmack CA, Shah AK, Wilner KD, Ko G et al (1999). A double-blind, placebo-controlled study of the safety, tolerability and pharmacokinetics of CP-101,606 in patients with a mild or moderate traumatic brain injury. Ann NY Acad Sci 890: 42-50.
31. Min MY, Rusakov DA, Kullmann DM (1998). Activation of AMPA, kainate, and metabotropic receptors at hippocampal mossy fiber synapses: role of glutamate diffusion. Neuron 21: 561-570.
32. Miner LA, Backstrom JR, Sanders-Bush E, Sesack SR (2003). Ultrastructural localization of serotonin2A receptors in the middle layers of the rat prelimbic prefrontal cortex. Neuroscience 116: 107-117.
33. Muschamp JW, Regina MJ, Hull EM, Winter JC, Rabin RA (2004). Lysergic acid diethylamide and [-]-2,5-dimethoxy-4-methyl-amphetamine increase extracellular glutamate in rat prefrontal cortex. Brain Res 1023: 134-140.
34. Nichols DE (2004). Hallucinogens. Pharmacol Ther 101: 131-181.
35. Nielsen TA, DiGregorio DA, Silver RA (2004). Modulation of glutamate mobility reveals the mechanism underlying slow-rising AMPAR EPSCs and the diffusion coefficient in the synaptic cleft. Neuron 42: 757-771.
36. Perrais D, Ropert N (2000). Altering the concentration of GABA in the synaptic cleft potentiates miniature IPSCs in rat occipital cortex. Eur J Neurosci 12: 400-404.
37. Piet R, Vargova L, Sykova E, Poulain DA, Oliet SH (2004). Physiological contribution of the astrocytic environment of neurons to intersynaptic crosstalk. Proc Natl Acad Sci USA 101: 2151-2155.
38. Rodin E, Luby E (1966). Effects of LSD-25 on the EEG and photic evoked responses. Arch Gen Psychiatry 14: 435-441.
39. Rumbaugh G, Vicini S (1999). Distinct synaptic and extrasynaptic NMDA receptors in developing cerebellar granule neurons. J Neurosci 19: 10603-10610.
40. Rusakov DA, Kullmann DM (1998). Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J Neurosci 18: 3158-3170.
41. Savtchenko LP, Rusakov DA (2005). Extracellular diffusivity determines contribution of high-versus low-affinity receptors to neural signaling. Neuroimage 25: 101-111.
42. Scimemi A, Fine A, Kullmann DM, Rusakov DA (2004). NR2B-containing receptors mediate cross talk among hippocampal synapses. J Neurosci 24: 4767-4777.
43. Scruggs JL, Schmidt D, Deutch AY (2003). The hallucinogen 1-[2,5-dimethoxy-4-iodophenyl]-2-aminopropane (DOI) increases cortical extracellular glutamate levels in rats. Neurosci Lett 346: 137-140.
44. Shu Y, Hasenstaub A, McCormick DA (2003). Turning on and off recurrent balanced cortical activity. Nature 423: 288-293.
45. Skoglund TS, Pascher R, Berthold CH (2004). Aspects of the organization of neurons and dendritic bundles in primary somatosensory cortex of the rat. Neurosci Res 50: 189-198.
46. Spacek J (1985). Three-dimensional analysis of dendritic spines. III. Glial sheath. Anat Embryol (Berl) 171: 245-252.
47. Steriade M, Timofeev I, Grenier F (2001). Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85: 1969-1985.
48. Stocca G, Vicini S (1998). Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. J Physiol 507(Part 1): 13-24.
49. Stutzmann GE, Marek GJ, Aghajanian GK (2001). Adenosine preferentially suppresses serotonin2A receptor-enhanced excitatory postsynaptic currents in layer V neurons of the rat medial prefrontal cortex. Neuroscience 105: 55-69.
50. Sutor B, Hablitz JJ (1989). EPSPs in rat neocortical neurons in vitro. II. Involvement of NMDA receptors in the generation of EPSPs. J Neurophysiol 61: 621-634.
51. Tovar KR, Westbrook GL (1999). The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 19: 4180-4188.
52. Townsend M, Yoshii A, Mishina M, Constantine-Paton M (2003). Developmental loss of miniature N-methyl-D-aspartate receptor currents in NR2A knockout mice. Proc Natl Acad Sci USA 100: 1340-1345.
53. Vollenweider FX, Leenders KL, Scharfetter C, Maguire P, Stadelmann O, Angst J (1997). Positron emission tomography and fluorodeoxyglucose studies of metabolic hyperfrontality and psychopathology in the psilocybin model of psychosis. Neuropsychopharmacology 16: 357-372.
54. Williams K (1993). Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol Pharmacol 44: 851-859.
55. 2A receptors are expressed on pyramidal cells and interneurons in the rat cortex. Synapse 27: 79-82.
56. 2A) receptors in the rat brain. Brain Res Bull 51: 499-505.
57. Zhang ZW (2003). Serotonin induces tonic firing in layer V pyramidal neurons of rat prefrontal cortex during postnatal development. J Neurosci 23: 3373-3384.
58. Zhang ZW, Arsenault D (2005). Gain modulation by serotonin in pyramidal neurones of the rat prefrontal cortex. J Physiol 566: 379-394.