Tonic and phasic release of glutamate and acetylcholine neurotransmission in sub-regions of the rat prefrontal cortex using enzyme-based microelectrode arrays

Journal of Neuroscience Methods

Volumn 202, Issue 2, 2011, Pages 199-208

  Mattinson, Catherine E ^a   Burmeister, Jason J ^a   Quintero, Jorge E ^a   Pomerleau, Francois ^a   Huettl, Peter ^a   Gerhardt, Greg A ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Acetylcholine; Amperometry; Glutamate; Medial prefrontal cortex; Microelectrode array

Indexed keywords

ACETYLCHOLINE; GLUTAMIC ACID; POTASSIUM CHLORIDE;

ACETYLCHOLINE RELEASE; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BRAIN REGION; CINGULATE GYRUS; CONTROLLED STUDY; ENZYME BASED MICROELECTRODE ARRAY; ENZYME ELECTRODE; GLUTAMIC ACID RELEASE; IN VIVO STUDY; MEDICAL PREFRONTAL CORTEX; NEUROSECRETION; NEUROTRANSMISSION; NONHUMAN; PREFRONTAL CORTEX; PRELIMBIC CORTEX; PRIORITY JOURNAL; RAT;

ACETYLCHOLINE; ANIMALS; ELECTROCHEMICAL TECHNIQUES; GLUTAMIC ACID; MALE; MICROELECTRODES; PREFRONTAL CORTEX; RATS; RATS, INBRED F344; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 81055140388     PISSN: 01650270     EISSN: 1872678X     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2011.08.020     Document Type: Article

References (87)

1. Abekawa T., Ohmori T., Ito K., Koyama T. D1 dopamine receptor activation reduces extracellular glutamate and GABA concentrations in the medial prefrontal cortex. Brain Res 2000, 867:250-254.
2. Arnold H.M., Fadel J., Sarter M., Bruno J.P. Amphetamine-stimulated cortical acetylcholine release: role of the basal forebrain. Brain Res 2001, 894:74-87.
3. Arnold H.M., Nelson C.L., Sarter M., Bruno J.P. Sensitization of cortical acetylcholine release by repeated administration of nicotine in rats. Psychopharmacology (Berl) 2003, 165:346-358.
4. 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.
5. Bauer D., Gupta D., Harotunian V., Meador-Woodruff J.H., McCullumsmith R.E. Abnormal expression of glutamate transporter and transporter interacting molecules in prefrontal cortex in elderly patients with schizophrenia. Schizophr Res 2008, 104:108-120.
6. Benes F.M., Sorensen I., Vincent S.L., Bird E.D., Sathi M. Increased density of glutamate-immunoreactive vertical processes in superficial laminae in cingulate cortex of schizophrenic brain. Cereb Cortex 1992, 2:503-512.
7. Berger B., Thierry A.M., Tassin J.P., Moyne M.A. Dopaminergic innervation of the rat prefrontal cortex: a fluorescence histochemical study. Brain Res 1976, 106:133-145.
8. Bigl V., Woolf N.J., Butcher L.L. Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res Bull 1982, 8:727-749.
9. Brooks J.M., Sarter M., Bruno J.P. D2-like receptors in nucleus accumbens negatively modulate acetylcholine release in prefrontal cortex. Neuropharmacology 2007, 53:455-463.
10. Brown R.M., Crane A.M., Goldman P.S. Regional distribution of monoamines in the cerebral cortex and subcortical structures of the rhesus monkey: concentrations and in vivo synthesis rates. Brain Res 1979, 168:133-150.
11. Bruno J.P., Gash C., Martin B., Zmarowski A., Pomerleau F., Burmeister J., et al. Second-by-second measurement of acetylcholine release in prefrontal cortex. Eur J Neurosci 2006, 24:2749-2757.
12. Burbaeva G., Boksha I.S., Tereshkina E.B., Savushkina O.K., Starodubtseva L.I., Turishcheva M.S. Glutamate metabolizing enzymes in prefrontal cortex of Alzheimer's disease patients. Neurochem Res 2005, 30:1443-1451.
13. Burmeister J.J., Gerhardt G.A. Self-referencing ceramic-based multisite microelectrodes for the detection and elimination of interferences from the measurement of l-glutamate and other analytes. Anal Chem 2001, 73:1037-1042.
14. Burmeister J.J., Moxon K., Gerhardt G.A. Ceramic-based multisite microelectrodes for electrochemical recordings. Anal Chem 2000, 72:187-192.
15. Burmeister J.J., Pomerleau F., Huettl P., Gash C.R., Werner C.E., Bruno J.P., et al. Ceramic-based multisite microelectrode arrays for simultaneous measures of choline and acetylcholine in CNS. Biosens Bioelectron 2008, 23:1382-1389.
16. Burmeister J.J., Pomerleau F., Palmer M., Day B.K., Huettl P., Gerhardt G.A. Improved ceramic-based multisite microelectrode for rapid measurements of l-glutamate in the CNS. J Neurosci Methods 2002, 119:163-171.
17. Clapp-Lilly K.L., Roberts R.C., Duffy L.K., Irons K.P., Hu Y., Drew K.L. An ultrastructural analysis of tissue surrounding a microdialysis probe. J Neurosci Methods 1999, 90:129-142.
18. Crook J.M., Tomaskovic-Crook E., Copolov D.L., Dean B. Low muscarinic receptor binding in prefrontal cortex from subjects with schizophrenia: a study of Brodmann's areas 8, 9, 10, and 46 and the effects of neuroleptic drug treatment. Am J Psychiatry 2001, 158:918-925.
19. Danbolt N.C. Glutamate uptake. Prog Neurobiol 2001, 65:1-105.
20. Day B.K., Pomerleau F., Burmeister J.J., Huettl P., Gerhardt G.A. Microelectrode array studies of basal and potassium-evoked release of l-glutamate in the anesthetized rat brain. J Neurochem 2006, 96:1626-1635.
21. de Brabander J.M., van Eden C.G., de Bruin J.P., Feenstra M.G. Monoamine concentrations in rat prefrontal cortex and other mesolimbocortical structures in response to partial neonatal lesions of the medial prefrontal cortex. Brain Res 1993, 601:20-27.
22. Del Arco A., Martinez R., Mora F. Amphetamine increases extracellular concentrations of glutamate in the prefrontal cortex of the awake rat: a microdialysis study. Neurochem Res 1998, 23:1153-1158.
23. Del Arco A., Segovia G., Garrido P., de Blas M., Mora F. Stress, prefrontal cortex and environmental enrichment: studies on dopamine and acetylcholine release and working memory performance in rats. Behav Brain Res 2007, 176:267-273.
24. Ferraro L., Tomasini M.C., Gessa G.L., Bebe B.W., Tanganelli S., Antonelli T. The cannabinoid receptor agonist WIN 55,212-2 regulates glutamate transmission in rat cerebral cortex: an in vivo and in vitro study. Cereb Cortex 2001, 11:728-733.
25. Francis P.T., Palmer A.M., Snape M., Wilcock G.K. The cholinergic hypothesis of Alzheimer's disease: a review of progress. J Neurol Neurosurg Psychiatry 1999, 66:137-147.
26. Frantz K., Harte M., Ungerstedt U., O'Connor W.T. A dual probe characterization of dialysate amino acid levels in the medial prefrontal cortex and ventral tegmental area of the awake freely moving rat. J Neurosci Methods 2002, 119:109-119.
27. Friedemann M.N., Gerhardt G.A. Regional effects of aging on dopaminergic function in the Fischer-344 rat. Neurobiol Aging 1992, 13:325-332.
28. Georgieva J., Luthman J., Mohringe B., Magnusson O. Tissue and microdialysate changes after repeated and permanent probe implantation in the striatum of freely moving rats. Brain Res Bull 1993, 31:463-470.
29. Gigg J., Tan A.M., Finch D.M. Glutamatergic excitatory responses of anterior cingulate neurons to stimulation of the mediodorsal thalamus and their regulation by GABA: an in vivo iontophoretic study. Cereb Cortex 1992, 2:477-484.
30. Gigg J., Tan A.M., Finch D.M. Glutamatergic hippocampal formation projections to prefrontal cortex in the rat are regulated by GABAergic inhibition and show convergence with glutamatergic projections from the limbic thalamus. Hippocampus 1994, 4:189-198.
31. Giuliano C., Parikh V., Ward J.R., Chiamulera C., Sarter M. Increases in cholinergic neurotransmission measured by using choline-sensitive microelectrodes: enhanced detection by hydrolysis of acetylcholine on recording sites?. Neurochem Int 2008, 52:1343-1350.
32. Grabb M.C., Sciotti V.M., Gidday J.M., Cohen S.A., van Wylen D.G. Neurochemical and morphological responses to acutely and chronically implanted brain microdialysis probes. J Neurosci Methods 1998, 82:25-34.
33. Gratton A., Hoffer B.J., Gerhardt G.A. In vivo electrochemical studies of monoamine release in the medial prefrontal cortex of the rat. Neuroscience 1989, 29:57-64.
34. Hara K., Harris R.A. The anesthetic mechanism of urethane: the effects on neurotransmitter-gated ion channels. Anesth Analg 2002, 94:313-318. (table of contents).
35. Hascup E.R., Hascup K.N., Stephens M., Pomerleau F., Huettl P., Gratton A., et al. Rapid microelectrode measurements and the origin and regulation of extracellular glutamate in rat prefrontal cortex. J Neurochem 2010, 115:1608-1620.
36. Hascup K.N., Rutherford E.C., Quintero J.E., Day B.K., Nickell J.R., Pomerleau F., Huettl P., Burmeister J.J., Gerhardt G.A. Second-by-second measures of l-glutamate and other neurotransmitters using enzyme-based microelectrode arrays. Electrochemical Methods for Neuroscience 2007, CRC Press, Boca Raton (FL), Chapter 19. A.C. Michael, L.M. Borland (Eds.).
37. Hedou G., Homberg J., Martin S., Wirth K., Feldon J., Heidbreder C.A. Effect of amphetamine on extracellular acetylcholine and monoamine levels in subterritories of the rat medial prefrontal cortex. Eur J Pharmacol 2000, 390:127-136.
38. Henny P., Jones B.E. Projections from basal forebrain to prefrontal cortex comprise cholinergic, GABAergic and glutamatergic inputs to pyramidal cells or interneurons. Eur J Neurosci 2008, 27:654-670.
39. Hernandez L.F., Segovia G., Mora F. Chronic treatment with a dopamine uptake blocker changes dopamine and acetylcholine but not glutamate and GABA concentrations in prefrontal cortex, striatum and nucleus accumbens of the awake rat. Neurochem Int 2008, 52:457-469.
40. Herzog C.D., Nowak K.A., Sarter M., Bruno J.P. Microdialysis without acetylcholinesterase inhibition reveals an age-related attenuation in stimulated cortical acetylcholine release. Neurobiol Aging 2003, 24:861-863.
41. Houser C.R., Crawford G.D., Salvaterra P.M., Vaughn J.E. Immunocytochemical localization of choline acetyltransferase in rat cerebral cortex: a study of cholinergic neurons and synapses. J Comp Neurol 1985, 234:17-34.
42. Huang M., Li Z., Dai J., Shahid M., Wong E.H., Meltzer H.Y. Asenapine increases dopamine, norepinephrine, and acetylcholine efflux in the rat medial prefrontal cortex and hippocampus. Neuropsychopharmacology 2008, 33:2934-2945.
43. Hugues S., Garcia R., Lena I. Time course of extracellular catecholamine and glutamate levels in the rat medial prefrontal cortex during and after extinction of conditioned fear. Synapse 2007, 61:933-937.
44. Jay T.M., Thierry A.M., Wiklund L., Glowinski J. Excitatory amino acid pathway from the hippocampus to the prefrontal cortex. Contribution of AMPA receptors in hippocampo-prefrontal cortex transmission. Eur J Neurosci 1992, 4:1285-1295.
45. Karreman M., Moghaddam B. Effect of a pharmacological stressor on glutamate efflux in the prefrontal cortex. Brain Res 1996, 716:180-182.
46. Kashani A., Lepicard E., Poirel O., Videau C., David J.P., Fallet-Bianco C., et al. Loss of VGLUT1 and VGLUT2 in the prefrontal cortex is correlated with cognitive decline in Alzheimer disease. Neurobiol Aging 2008, 29:1619-1630.
47. Lawler H.C. Turnover time of acetylcholinesterase. J Biol Chem 1961, 236:2296-2301.
48. Leonard C.M. The prefrontal cortex of the rat. I. Cortical projection of the mediodorsal nucleus. II. Efferent connections. Brain Res 1969, 12:321-343.
49. Lu W., Monteggia L.M., Wolf M.E. Withdrawal from repeated amphetamine administration reduces NMDAR1 expression in the rat substantia nigra, nucleus accumbens and medial prefrontal cortex. Eur J Neurosci 1999, 11:3167-3177.
50. Lupinsky D., Moquin L., Gratton A. Interhemispheric regulation of the medial prefrontal cortical glutamate stress response in rats. J Neurosci 2010, 30:7624-7633.
51. McDonald A.J. Glutamate and aspartate immunoreactive neurons of the rat basolateral amygdala: colocalization of excitatory amino acids and projections to the limbic circuit. J Comp Neurol 1996, 365:367-379.
52. McFarland K., Lapish C.C., Kalivas P.W. Prefrontal glutamate release into the core of the nucleus accumbens mediates cocaine-induced reinstatement of drug-seeking behavior. J Neurosci 2003, 23:3531-3537.
53. McGaughy J., Kaiser T., Sarter M. Behavioral vigilance following infusions of 192 IgG-saporin into the basal forebrain: selectivity of the behavioral impairment and relation to cortical AChE-positive fiber density. Behav Neurosci 1996, 110:247-265.
54. Mesulam M.M., Mufson E.J., Wainer B.H., Levey A.I. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 1983, 10:1185-1201.
55. Meyer E.M., Engel D.A., Cooper J.R. Acetylation and phosphorylation of choline following high or low affinity uptake by rat cortical synaptosomes. Neurochem Res 1982, 7:749-759.
56. Miele M., Berners M., Boutelle M.G., Kusakabe H., Fillenz M. The determination of the extracellular concentration of brain glutamate using quantitative microdialysis. Brain Res 1996, 707:131-133.
57. Mork A., Witten L.M., Arnt J. Effect of sertindole on extracellular dopamine, acetylcholine, and glutamate in the medial prefrontal cortex of conscious rats: a comparison with risperidone and exploration of mechanisms involved. Psychopharmacology (Berl) 2009, 206:39-49.
58. Mrzljak L., Goldman-Rakic P.S. Acetylcholinesterase reactivity in the frontal cortex of human and monkey: contribution of AChE-rich pyramidal neurons. J Comp Neurol 1992, 324:261-281.
59. Nandi P., Lunte S.M. Recent trends in microdialysis sampling integrated with conventional and microanalytical systems for monitoring biological events: a review. Anal Chim Acta 2009, 651:1-14.
60. Neigh-McCandless G., Kravitz B.A., Sarter M., Bruno J.P. Stimulation of cortical acetylcholine release following blockade of ionotropic glutamate receptors in nucleus accumbens. Eur J Neurosci 2002, 16:1259-1266.
61. Nickell J., Pomerleau F., Allen J., Gerhardt G.A. Age-related changes in the dynamics of potassium-evoked l-glutamate release in the striatum of Fischer 344 rats. J Neural Transm 2005, 112:87-96.
62. Nirogi R., Mudigonda K., Kandikere V., Ponnamaneni R. Quantification of acetylcholine, an essential neurotransmitter, in brain microdialysis samples by liquid chromatography mass spectrometry. Biomed Chromatogr 2010, 24:39-48.
63. Okuda T., Haga T., Kanai Y., Endou H., Ishihara T., Katsura I. Identification and characterization of the high-affinity choline transporter. Nat Neurosci 2000, 3:120-125.
64. Olbrich H.M., Valerius G., Rusch N., Buchert M., Thiel T., Hennig J., et al. Frontolimbic glutamate alterations in first episode schizophrenia: evidence from a magnetic resonance spectroscopy study. World J Biol Psychiatry 2008, 9:59-63.
65. Oni-Orisan A., Kristiansen L.V., Haroutunian V., Meador-Woodruff J.H., McCullumsmith R.E. Altered vesicular glutamate transporter expression in the anterior cingulate cortex in schizophrenia. Biol Psychiatry 2008, 63:766-775.
66. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2004, Academic Press, San Diego, CA. 5th ed.
67. Perry J.L., Joseph J.E., Jiang Y., Zimmerman R.S., Kelly T.H., Darna M., et al. Prefrontal cortex and drug abuse vulnerability: translation to prevention and treatment interventions. Brain Res Rev 2011, 65:124-149.
68. Pirot S., Jay T.M., Glowinski J., Thierry A.M. Anatomical and electrophysiological evidence for an excitatory amino acid pathway from the thalamic mediodorsal nucleus to the prefrontal cortex in the rat. Eur J Neurosci 1994, 6:1225-1234.
69. Prus A.J., Huang M., Li Z., Dai J., Meltzer H.Y. The neurotensin analog NT69L enhances medial prefrontal cortical dopamine and acetylcholine efflux: potentiation of risperidone-, but not haloperidol-, induced dopamine efflux. Brain Res 2007, 1184:354-364.
70. Ragozzino M.E., Unick K.E., Gold P.E. Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose. Proc Natl Acad Sci USA 1996, 93:4693-4698.
71. Rajkowska G., Niewiadomska G., Kosmal A. Regional and laminar variations in acetylcholinesterase activity within the frontal cortex of the dog. J Chem Neuroanat 1993, 6:117-130.
72. Romanides A.J., Duffy P., Kalivas P.W. Glutamatergic and dopaminergic afferents to the prefrontal cortex regulate spatial working memory in rats. Neuroscience 1999, 92:97-106.
73. Rutherford E.C., Pomerleau F., Huettl P., Stromberg I., Gerhardt G.A. Chronic second-by-second measures of l-glutamate in the central nervous system of freely moving rats. J Neurochem 2007, 102:712-722.
74. Sarter M., Nelson C.L., Bruno J.P. Cortical cholinergic transmission and cortical information processing in schizophrenia. Schizophr Bull 2005, 31:117-138.
75. Schultz K.N., Kennedy R.T. Time-resolved microdialysis for in vivo neurochemical measurements and other applications. Annu Rev Anal Chem (Palo Alto Calif) 2008, 1:627-661.
76. Selim M., Bradberry C.W. Effect of ethanol on extracellular 5-HT and glutamate in the nucleus accumbens and prefrontal cortex: comparison between the Lewis and Fischer 344 rat strains. Brain Res 1996, 716:157-164.
77. Sofuoglu M., Mooney M. Cholinergic functioning in stimulant addiction: implications for medications development. CNS Drugs 2009, 23:939-952.
78. Stephens M.L., Quintero J.E., Pomerleau F., Huettl P., Gerhardt G.A. Age-related changes in glutamate release in the CA3 and dentate gyrus of the rat hippocampus. Neurobiol Aging 2011, 32(5):811-820.
79. Thierry A.M., Deniau J.M., Chevalier G., Ferron A., Glowinski J. An electrophysiological analysis of some afferent and efferent pathways of the rat prefrontal cortex. Prog Brain Res 1983, 58:257-261.
80. Timmerman W., Westerink B.H. Brain microdialysis of GABA and glutamate: what does it signify?. Synapse 1997, 27:242-261.
81. Torres E.M., Perry T.A., Blockland A., Wilkinson L.S., Wiley R.G., Lappi D.A., et al. Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neuroscience 1994, 63:95-122.
82. Trabace L., Cassano T., Colaianna M., Castrignano S., Giustino A., Amoroso S., et al. Neurochemical and neurobehavioral effects of ganstigmine (CHF2819), a novel acetylcholinesterase inhibitor, in rat prefrontal cortex: an in vivo study. Pharmacol Res 2007, 56:288-294.
83. Tsai G., Passani L.A., Slusher B.S., Carter R., Baer L., Kleinman J.E., et al. Abnormal excitatory neurotransmitter metabolism in schizophrenic brains. Arch Gen Psychiatry 1995, 52:829-836.
84. Welty N., Shoblock J.R. The effects of thioperamide on extracellular levels of glutamate and GABA in the rat prefrontal cortex. Psychopharmacology (Berl) 2009, 207:433-438.
85. Williams J.M., Steketee J.D. Cocaine increases medial prefrontal cortical glutamate overflow in cocaine-sensitized rats: a time course study. Eur J Neurosci 2004, 20:1639-1646.
86. Woo T.U., Kim A.M., Viscidi E. Disease-specific alterations in glutamatergic neurotransmission on inhibitory interneurons in the prefrontal cortex in schizophrenia. Brain Res 2008, 1218:267-277.
87. Zmarowski A., Wu H.Q., Brooks J.M., Potter M.C., Pellicciari R., Schwarcz R., et al. Astrocyte-derived kynurenic acid modulates basal and evoked cortical acetylcholine release. Eur J Neurosci 2009, 29:529-538.