Chemical gradients within brain extracellular space measured using low flow push-pull perfusion sampling in vivo

ACS Chemical Neuroscience

Volumn 4, Issue 2, 2013, Pages 321-329

  Slaney, Thomas R ^a   Mabrouk, Omar S ^a   Porter Stransky, Kirsten A ^a   Aragona, Brandon J ^a   Kennedy, Robert T ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Dopamine; glutamate; in vivo; microdialysis; push pull perfusion; spatial resolution

Indexed keywords

4 AMINOBUTYRIC ACID; 5 HYDROXYINDOLEACETIC ACID; ACETYLCHOLINE; ASPARTIC ACID; DOPAMINE; GLUTAMIC ACID; GLYCINE; HOMOVANILLIC ACID; NEUROTRANSMITTER; NORADRENALIN; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN PERFUSION; BRAIN REGION; CORPUS STRIATUM; IN VIVO STUDY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RED NUCLEUS; VENTRAL TEGMENTUM;

ACETYLCHOLINE; ANIMALS; ASPARTIC ACID; BRAIN; DOPAMINE; EXTRACELLULAR SPACE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GLYCINE; MALE; MICRODIALYSIS; NEUROTRANSMITTER AGENTS; NOREPINEPHRINE; NUCLEUS ACCUMBENS; PERFUSION; RATS; RED NUCLEUS; SEROTONIN; VENTRAL TEGMENTAL AREA;

EID: 84874037653     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn300158p     Document Type: Article

References (63)

1. Peciña, S. and Berridge, K. C. (2005) Hedonic Hot Spot in Nucleus Accumbens Shell: Where Do μ-Opioids Cause Increased Hedonic Impact of Sweetness? J. Neurosci. 25, 11777-11786
2. Brown, P. and Molliver, M. E. (2000) Dual Serotonin (5-HT) Projections to the Nucleus Accumbens Core and Shell: Relation of the 5-HT Transporter to Amphetamine-Induced Neurotoxicity J. Neurosci. 20, 1952-1963
3. Van Bockstaele, E. J. and Pickel, V. M. (1993) Ultrastructure of serotonin-immunoreactive terminals in the core and shell of the rat nucleus accumbens: Cellular substrates for interactions with catecholamine afferents J. Comp. Neurol. 334, 603-617
4. Willoughby, J., Glover, V., and Sandler, M. (1988) Histochemical localisation of monoamine oxidase A and B in rat brain J. Neural Transm. 74, 29-42
5. Baldo, B. A., Daniel, R. A., Berridge, C. W., and Kelley, A. E. (2003) Overlapping distributions of orexin/hypocretin-and dopamine-β-hydroxylase immunoreactive fibers in rat brain regions mediating arousal, motivation, and stress J. Comp. Neurol. 464, 220-237
6. 2C Receptors Localize to Dopamine and GABA Neurons in the Rat Mesoaccumbens Pathway PLoS One 6, e20508
7. Yung, K. K. L., Bolam, J. P., Smith, A. D., Hersch, S. M., Ciliax, B. J., and Levey, A. I. (1995) Immunocytochemical localization of D1 and D2 dopamine receptors in the basal ganglia of the rat: Light and electron microscopy Neuroscience 65, 709-730
8. Freed, C., Revay, R., Vaughan, R. A., Kriek, E., Grant, S., Uhl, G. R., and Kuhar, M. J. (1995) Dopamine transporter immunoreactivity in rat brain J. Comp. Neurol. 359, 340-349
9. Miner, L. H., Schroeter, S., Blakely, R. D., and Sesack, S. R. (2003) Ultrastructural localization of the norepinephrine transporter in superficial and deep layers of the rat prelimbic prefrontal cortex and its spatial relationship to probable dopamine terminals J. Comp. Neurol. 466, 478-494
10. Kalivas, P. W. (2009) The glutamate homeostasis hypothesis of addiction Nat. Rev. Neurosci. 10, 561-572
11. Knackstedt, L. A., LaRowe, S., Mardikian, P., Malcolm, R., Upadhyaya, H., Hedden, S., Markou, A., and Kalivas, P. W. (2009) The Role of Cystine-Glutamate Exchange in Nicotine Dependence in Rats and Humans Biol. Psychiatry 65, 841-845
12. Westerink, B. H. C. and Timmerman, W. (1999) Do neurotransmitters sampled by brain microdialysis reflect functional release? Anal. Chim. Acta 379, 263-274
13. Fuxe, K., Dahlstroem, A. B., Jonsson, G., Marcellino, D., Guescini, M., Dam, M., Manger, P., and Agnati, L. (2010) The discovery of central monoamine neurons gave volume transmission to the wired brain Prog. Neurobiol. (Amsterdam, Neth.) 90, 82-100
14. Nandi, P. and Lunte, S. M. (2009) Recent trends in microdialysis sampling integrated with conventional and microanalytical systems for monitoring biological events: A review Anal. Chim. Acta 651, 1-14
15. Robinson, D. L., Hermans, A., Seipel, A. T., and Wightman, R. M. (2008) Monitoring Rapid Chemical Communication in the Brain Chem. Rev. 108, 2554-2584
16. Park, J., Aragona, B. J., Kile, B. M., Carelli, R. M., and Wightman, R. M. (2010) In vivo voltammetric monitoring of catecholamine release in subterritories of the nucleus accumbens shell Neuroscience 169, 132-142
17. Robinson, D. L., Howard, E. C., McConnell, S., Gonzales, R. A., and Wightman, R. M. (2009) Disparity Between Tonic and Phasic Ethanol-Induced Dopamine Increases in the Nucleus Accumbens of Rats Alcohol.: Clin. Exp. Res. 33, 1187-1196
18. Robinson, D. L., Venton, B. J., Heien, M. L. A. V., and Wightman, R. M. (2003) Detecting Subsecond Dopamine Release with Fast-Scan Cyclic Voltammetry in Vivo Clin. Chem. 49, 1763-1773
19. Kottegoda, S., Shaik, I., and Shippy, S. A. (2002) Demonstration of low flow push-pull perfusion J. Neurosci. Methods 121, 93-101
20. Gaddum, J. H. (1961) Push-Pull Cannulae J. Physiol. (London, U.K.) 155, 1P-2P
21. Slaney, T. R., Nie, J., Hershey, N. D., Thwar, P. K., Linderman, J., Burns, M. A., and Kennedy, R. T. (2011) Push-Pull Perfusion Sampling with Segmented Flow for High Temporal and Spatial Resolution in Vivo Chemical Monitoring Anal. Chem. 83, 5207-5213
22. Cellar, N. A., Burns, S. T., Meiners, J. C., Chen, H., and Kennedy, R. T. (2005) Microfluidic Chip for Low-Flow Push-Pull Perfusion Sampling in Vivo with On-Line Analysis of Amino Acids Anal. Chem. 77, 7067-7073
23. Cellar, N. A. and Kennedy, R. T. (2006) A capillary-PDMS hybrid chip for separations-based sensing of neurotransmitters in vivo Lab Chip 6, 1205-1212
24. Song, P., Mabrouk, O. S., Hershey, N. D., and Kennedy, R. T. (2012) In Vivo Neurochemical Monitoring Using Benzoyl Chloride Derivatization and Liquid Chromatography-Mass Spectrometry Anal. Chem. 84, 412-419
25. Lin, Z., Canales, J. J., Bjorgvinsson, T., Thomsen, M., Qu, H., Liu, Q.-R., Torres, G. E., Caine, S. B., and Shafiqur, R. (2011) Monoamine Transporters: Vulnerable and Vital Doorkeepers. In Progress in Molecular Biology and Translational Science, Chapter 1, Vol. 98, pp 1-46, Academic Press: London, UK.
26. Ikemoto, S. (2010) Brain reward circuitry beyond the mesolimbic dopamine system: A neurobiological theory Neurosci. Biobehav. Rev. 35, 129-150
27. McKittrick, C. R. and Abercrombie, E. D. (2007) Catecholamine mapping within nucleus accumbens: differences in basal and amphetamine-stimulated efflux of norepinephrine and dopamine in shell and core J. Neurochem. 100, 1247-1256
28. Owesson-White, C. A., Roitman, M. F., Sombers, L. A., Belle, A. M., Keithley, R. B., Peele, J. L., Carelli, R. M., and Wightman, R. M. (2012) Sources contributing to the average extracellular concentration of dopamine in the nucleus accumbens J. Neurochem. 121, 252-262
29. Heidbreder, C. and Feldon, J. (1998) Amphetamine-induced neurochemical and locomotor responses are expressed differentially across the anteroposterior axis of the core and shell subterritories of the nucleus accumbens Synapse 29, 310-322
30. Aragona, B. J., Cleaveland, N. A., Stuber, G. D., Day, J. J., Carelli, R. M., and Wightman, R. M. (2008) Preferential enhancement of dopamine transmission within the nucleus accumbens shell by cocaine is attributable to a direct increase in phasic dopamine release events J. Neurosci. 28, 8821-8831
31. Aragona, B. J., Day, J. J., Roitman, M. F., Cleaveland, N. A., Wightman, R. M., and Carelli, R. M. (2009) Regional specificity in the real-time development of phasic dopamine transmission patterns during acquisition of a cue-cocaine association in rats Eur. J. Neurosci. 30, 1889-1899
32. Lammel, S., Hetzel, A., Häckel, O., Jones, I., Liss, B., and Roeper, J. (2008) Unique Properties of Mesoprefrontal Neurons within a Dual Mesocorticolimbic Dopamine System Neuron 57, 760-773
33. Richardson, R. R., Jr., Miller, J. A., and Reichert, W. M. (1993) Polyimides as biomaterials: preliminary biocompatibility testing Biomaterials 14, 627-635
34. Szerb, J. C. (1967) Model Experiments with Gaddum's Push-Pull Cannulas Can. J. Physiol. Pharmacol. 45, 613-620
35. Nicholson, C. and Phillips, J. M. (1981) Ion diffusion modified by tortuosity and volume fraction in the extracellular microenvironment of the rat cerebellum J. Physiol. (London, U.K.) 321, 225-257
36. 3H]mannitol diffusion in agar and rat striatum J. Neurochem. 81, 80-93
37. Rice, M. E., Patel, J. C., and Cragg, S. J. (2011) Dopamine release in the basal ganglia Neuroscience 198, 112-137
38. Tang, A., Bungay, P. M., and Gonzales, R. A. (2003) Characterization of probe and tissue factors that influence interpretation of quantitative microdialysis experiments for dopamine J. Neurosci. Methods 126, 1-11
39. Abercrombie, E. D., Keefe, K. A., Difrischia, D. S., and Zigmond, M. J. (1989) Differential Effect of Stress on in Vivo Dopamine Release in Striatum, Nucleus Accumbens, and Medial Frontal-Cortex J. Neurochem. 52, 1655-1658
40. Wood, P. L. and Altar, C. A. (1988) Dopamine release in vivo from nigrostriatal, mesolimbic, and mesocortical neurons: utility of 3-methoxytyramine measurements Pharmacol. Rev. 40, 163-187
41. Roffler-Tarlov, S., Sharman, D. F., and Tegerdine, P. (1971) 3,4-Dihydroxyphenylacetic acid and 4-hydroxy-3-methoxyphenylacetic acid in the mouse striatum: a reflection of intra-and extra-neuronal metabolism of dopamine? Br. J. Pharmacol. 42, 343-351
42. Bast, T., Diekamp, B., Thiel, C., Schwarting, R. K. W., and Gunturkun, O. (2002) Functional aspects of dopamine metabolism in the putative prefrontal cortex analogue and striatum of pigeons (Columba livia) J. Comp. Neurol. 446, 58-67
43. Hardebo, J. E. and Owman, C. H. (1980) Characterization of the in vitro uptake of monoamines into brain microvessels Acta Physiol. Scand. 108, 223-229
44. Tanahashi, S., Ueda, Y., Nakajima, A., Yamamura, S., Nagase, H., and Okada, M. (2012) Novel δ1-receptor agonist KNT-127 increases the release of dopamine and l-glutamate in the striatum, nucleus accumbens and median pre-frontal cortex Neuropharmacology 62, 2057-2067
45. Moroni, F., Cozzi, A., Carpendo, R., Cipriani, G., Veneroni, O., and Izzo, E. (2005) Kynurenine 3-mono-oxygenase inhibitors reduce glutamate concentration in the extracellular spaces of the basal ganglia but not in those of the cortex or hippocampus Neuropharmacology 48, 788-795
46. Lehre, K. P., Levy, L. M., Ottersen, O. P., Storm-Mathisen, J., and Danbolt, N. C. (1995) Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations J. Neurosci. 15, 1835-1853
47. D'Este, L., Casini, A., Puglisi-Allegra, S., Cabib, S., and Renda, T. G. (2007) Comparative immunohistochemical study of the dopaminergic systems in two inbred mouse strains (C57BL/6J and DBA/2J) J. Chem. Neuroanat. 33, 67-74
48. -, in the Mouse Brain J. Neurosci. 22, 8028-8033
49. Herrera-Marschitz, M., You, Z. B., Goiny, M., Meana, J. J., Silveira, R., Godukhin, O. V., Chen, Y., Espinoza, S., Pettersson, E., Loidl, C. F., Lubec, G., Andersson, K., Nylander, I., Terenius, L., and Ungerstedt, U. (1996) On the Origin of Extracellular Glutamate Levels Monitored in the Basal Ganglia of the Rat by In Vivo Microdialysis J. Neurochem. 66, 1726-1735
50. David, D. J., Zahniser, N. R., Hoffer, B. J., and Gerhardt, G. A. (1998) In Vivo Electrochemical Studies of Dopamine Clearance in Subregions of Rat Nucleus Accumbens: Differential Properties of the Core and Shell Exp. Neurol. 153, 277-286
51. Wightman, R. M., Heien, M. L. A. V., Wassum, K. M., Sombers, L. A., Aragona, B. J., Khan, A. S., Ariansen, J. L., Cheer, J. F., Phillips, P. E. M., and Carelli, R. M. (2007) Dopamine release is heterogeneous within microenvironments of the rat nucleus accumbens Eur. J. Neurosci. 26, 2046-2054
52. Valentini, V., Frau, R., Bordi, F., Borsini, F., and Di Chiara, G. (2011) A microdialysis study of ST1936, a novel 5-HT6 receptor agonist Neuropharmacology 60, 602-608
53. Watson, C. J., Venton, B. J., and Kennedy, R. T. (2006) In Vivo Measurements of Neurotransmitters by Microdialysis Sampling Anal. Chem. 78, 1391-1399
54. Justice, J. B., Jr (1993) Quantitative microdialysis of neurotransmitters J. Neurosci. Methods 48, 263-276
55. Engleman, E. A., Keen, E. J., Tilford, S. S., Thielen, R. J., and Morzorati, S. L. (2011) Ethanol drinking reduces extracellular dopamine levels in the posterior ventral tegmental area of nondependent alcohol-preferring rats Alcohol 45, 549-557
56. Crippens, D., Camp, D. M., and Robinson, T. E. (1993) Basal extracellular dopamine in the nucleus accumbens during amphetamine withdrawal: a "no net flux" microdialysis study Neurosci. Lett. 164, 145-148
57. Smith, A. D. and Weiss, F. (1999) Ethanol Exposure Differentially Alters Central Monoamine Neurotransmission in Alcohol-Preferring versus -Nonpreferring Rats J. Pharmacol. Exp. Ther. 288, 1223-1228
58. Katner, S. N. and Weiss, F. (2001) Neurochemical Characteristics Associated With Ethanol Preference in Selected Alcohol-Preferring and -Nonpreferring Rats: A Quantitative Microdialysis Study Alcohol.: Clin. Exp. Res. 25, 198-205
59. Chen, N. N. H., Lai, Y.-J., and Pan, W. H. T. (1997) Effects of different perfusion medium on the extracellular basal concentration of dopamine in striatum and medial prefrontal cortex: a zero-net flux microdialysis study Neurosci. Lett. 225, 197-200
60. Sam, P. M. and Justice, J. B. (1996) Effect of General Microdialysis-Induced Depletion on Extracellular Dopamine Anal. Chem. 68, 724-728
61. Tao, R., Ma, Z., and Auerbach, S. B. (2000) Differential Effect of Local Infusion of Serotonin Reuptake Inhibitors in the Raphe versus Forebrain and the Role of Depolarization-Induced Release in Increased Extracellular Serotonin J. Pharmacol. Exp. Ther. 294, 571-579
62. Redgrave, P. (1977) A modified push-pull system for the localised perfusion of brain tissue Pharmacol., Biochem. Behav. 6, 471-474
63. Paxinos, G. and Watson, C. (2008) The Rat Brain in Stereotaxic Coordinates, Academic Press, San Diego, CA.