An investigation of hypofrontality in an animal model of schizophrenia using real-time microelectrochemical sensors for glucose, oxygen, and nitric oxide

ACS Chemical Neuroscience

Volumn 4, Issue 5, 2013, Pages 825-831

  Finnerty, Niall J ^a   Bolger, Fiachra B ^a   Paìšlsson, Erik ^b   Lowry, John P ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

brain; electrochemical sensors; Hypofrontality; metabolism; real time monitoring; schizophrenia

Indexed keywords

GLUCOSE; NITRIC OXIDE; OXYGEN; PHENCYCLIDINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; ELECTROCHEMISTRY; IN VIVO STUDY; MALE; MOTOR PERFORMANCE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SCHIZOPHRENIA;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; ELECTROCHEMICAL TECHNIQUES; GLUCOSE; HALLUCINOGENS; MALE; NITRIC OXIDE; OXYGEN; PHENCYCLIDINE; PREFRONTAL CORTEX; RATS; RATS, WISTAR; SCHIZOPHRENIA;

EID: 84877792037     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn4000567     Document Type: Article

References (56)

1. Ingvar, D. H. and Franzén, G. (1974) Abnormalities of cerebral blood flow distribution in patients with chronic schizophrenia Acta Psychiatr. Scand. 50, 425-462
2. Buchsbaum, M. S., Nuechterlein, K. H., Haier, R. J., Wu, J., Sicotte, N., Hazlett, E., Asarnow, R., Potkin, S., and Guich, S. (1990) Glucose metabolic rate in normals and schizophrenics during the continuous performance test assessed by positron emission tomography Br. J. Psychiatry 156, 216-227
3. Bullmore, E., Brammer, M., Williams, S. C., Curtis, V., McGuire, P., Morris, R., Murray, R., and Sharma, T. (1999) Functional MR imaging of confounded hypofrontality Hum. Brain Mapping 8, 86-91
4. Hill, K., Mann, L., Laws, K. R., Stephenson, C. M. E., Nimmo-Smith, I., and McKenna, P. J. (2004) Hypofrontality in schizophrenia: a meta-analysis of functional imaging studies Acta Psychiatr. Scand. 110, 1-14
5. Reif, A., Schecklmann, M., Eirich, E., Jacob, C. P., Jarczok, T. A., Kittel-Schneider, S., Lesch, K.-P., Fallgatter, A. J., and Ehlis, A.-C. (2011) A functional promoter polymorphism of neuronal nitric oxide synthase moderates prefrontal functioning in schizophrenia Int. J. Neuropsychopharmacol. 14, 887-897
6. Walter, H., Wunderlich, A. P., Blankenhorn, M., Schäfer, S., Tomczak, R., Spitzer, M., and Grön, G. (2003) No hypofrontality, but absence of prefrontal lateralization comparing verbal and spatial working memory in schizophrenia Schizophr. Res. 61, 175-184
7. Gur, R. C. and Gur, R. E. (1995) Hypofrontality in schizophrenia: RIP Lancet 345, 1383-1384
8. Stamford, J. A. and Justice, J. B. (1996) Probing brain chemistry Anal. Chem. 68, A359-A363
9. O'Neill, R. D., Lowry, J. P., and Mas, M. (1998) Monitoring brain chemistry in vivo: voltammetric techniques, sensors and behavioral applications Crit. Rev. Neurobiol. 12, 69-127
10. Lowry, J. P. and O'Neill, R. D. (2005) Neuroanalytical chemistry in vivo using biosensors. In Encyclopedia of Sensors (Grimes, C. A. and Dickey, E. C., Eds.), pp 501-524, American Scientific Publishers, Stevenson Ranch, CA.
11. Lowry, J. P. and O'Neill, R. D. (1993) Partial characterization in vitro of glucose oxidase-modified poly(phenylenediamine)-coated electrodes for neurochemical analysis in vivo Electroanalysis 6, 369-379
12. 2: Implications for biomedical applications J. Chem. Soc., Chem. Commun. 21, 2483-2484
13. Lowry, J. P., McAteer, K., El Attash, S. S., Duff, A., and O'Neill, R. D. (1994) Characterization of glucose oxidase-modified poly(phenylenediamine)- coated electrodes in vitro and in viv o: Homogeneous interference by ascorbic acid in hydrogen peroxide detection Anal. Chem. 66, 1754-1761
14. Lowry, J. P., Boutelle, M. G., O'Neill, R. D., and Fillenz, M. (1996) Characterisation of carbon paste electrodes in vitro for simultaneous amperometric measurement of changes in oxygen and ascorbic acid concentrations in viv o Analyst 121, 761-766
15. Bolger, F. B., McHugh, S. B., Bennett, R., Li, J., Ishiwari, K., Francois, J., Conway, M. W., Gilmour, G., Bannerman, D. M., Fillenz, M., Tricklebank, M., and Lowry, J. P. (2011) Characterisation of carbon paste electrodes for real-time amperometric monitoring of brain tissue oxygen J. Neurosci. Methods 195, 135-142
16. Brown, F. O. and Lowry, J. P. (2003) Microelectrochemical Sensors for In Vivo Brain Analysis: An Investigation of Procedures for Modifying Pt Electrodes Using Nafion Analyst 128, 700-705
17. Brown, F. O., Finnerty, N. J., and Lowry, J. P. (2009) Nitric oxide monitoring in brain extracellular fluid: Characterisation of Nafion-modified Pt electrodes in vitro and in vivo Analyst 134, 2012-2020
18. Lowry, J. P., Miele, M., O'Neill, R. D., Boutelle, M. G., and Fillenz, M. (1998) An amperometric glucose-oxidase/poly(o -phenylenediamine) biosensor for monitoring brain extracellular glucose: In vivo characterization in the striatum of freely-moving rats J. Neurosci. Methods 79, 65-74
19. Finnerty, N. J., O'Riordan, S. L., Brown, F. O., Serra, P. A., O'Neill, R. D., and Lowry, J. P. (2011) In vivo characterisation of a Nafion-modified Pt electrode for real-time nitric oxide monitoring in brain extracellular fluid Anal. Methods 4, 550-557
20. Lowry, J. P., O'Neill, R. D., Boutelle, M. G., and Fillenz, M. (1998) Continuous monitoring of extracellular glucose concentrations in the striatum of freely moving rats with an implanted glucose biosensor J. Neurochem. 70, 391-396
21. Fillenz, M. and Lowry, J. P. (1998) Studies of the source of glucose in the extracellular compartment of the rat brain Dev. Neurosci. (Basel, Switz.) 20, 365-368
22. Lowry, J. P. and Fillenz, M. (1997) Evidence for uncoupling of oxygen and glucose utilisation during neuronal activation in rat striatum J. Physiol. (London, U.K.) 498, 497-501
23. PàŠlsson, E., Finnerty, N., Fejgin, K., Klamer, D., Wass, C., Svensson, L., and Lowry, J. (2009) Increased Cortical Nitric Oxide Release After Phencyclidine Administration Synapse 63, 1083-1088
24. McHugh, S. B., Fillenz, M., Lowry, J. P., Rawlins, N. P., and Bannerman, D. M. (2010) Brain tissue oxygen amperometry in behaving rats demonstrates functional dissociation of dorsal and ventral hippocampus during spatial processing and anxiety Eur. J. Neurosci. 33, 322-37
25. Lowry, J. P., Boutelle, M. G., and Fillenz, M. (1997) Measurement of brain tissue oxygen at a carbon paste electrode can serve as an index of increases in regional cerebral blood flow J. Neurosci. Methods 71, 177-182
26. Lowry, J. P., Griffin, K., McHugh, S. B., Lowe, A. S., Tricklebank, M., and Sibson, N. R. (2010) Real-time electrochemical monitoring of brain tissue oxygen: a surrogate for functional magnetic resonance imaging in rodents NeuroImage 52, 549-55
27. Piilgaard, H. and Lauritzen, M. (2009) Persistent increase in oxygen consumption and impaired neurovascular coupling after spreading depression in rat neocortex J. Cereb. Blood Flow Metab. 29, 1517-27
28. Forstner, H. and Gnaiger, E. (2010) Calculation of equilibrium oxygen concentration. In Polarographic oxygen sensors. Aquatic and physiological applications (Gnaiger, E. and Forstner, H., Eds.), pp 321-336, Springer-Verlag, Berlin, Heidelberg.
29. Francois, J., Conway, M. W., Lowry, J. P., Tricklebank, M., and Gilmour, G. (2012) Changes in reward-related signals in the rat nucleus accumbens measured by in vivo oxygen amperometry are consistent with fMRI BOLD responses in man NeuroImage 60, 2169-2181
30. McHugh, S. B., Marques-Smith, A., Li, J., Rawlins, J. N., Conway, M., Gilmour, G., Tricklebank, M., and Bannerman, D. M. (2013) Hemodynamic responses in amygdala and hippocampus distinguish between aversive and neutral cues during Pavlovian fear conditioning in behaving rats Eur. J. Neurosci. 37, 498-507
31. Farkas, T., Wolf, A. P., Jaeger, J., Brodie, J. D., Christman, D. R., Fowler, J. S., MacGregor, R. R., deLeon, M. J., deFina, P., Goldman, A., Yonekura, Y., Brill, A. B., Schwartz, M., Logan, J., and Cancro, R. (1984) Regional brain glucose metabolism in chronic schizophrenia. A positron emission transaxial tomographic study Arch. Gen. Psychiatry 41, 293-300
32. Wolkin, A., Jaeger, J., Brodie, J. D., Wolf, A. P., Fowler, J., Rotrosen, J., Gomez-Mont, F., and Cancro, R. (1985) Persistence of cerebral metabolic abnormalities in chronic schizophrenia as determined by positron emission tomography Am. J. Psychiatry 142, 564-571
33. Buchsbaum, M. S. (1990) The frontal lobes, basal ganglia, and temporal lobes as sites for schizophrenia Schizophr. Bull. 16, 379-389
34. Gur, R. E., Skolnick, B. E., Gur, R. C., Caroff, S., Rieger, W., Obrist, W. D., Younkin, D., and Reivich, M. (1983) Brain function in psychiatric disorders. I. Regional cerebral blood flow in medicated schizophrenics Arch. Gen. Psychiatry 40, 1250-1254
35. Ebmeier, K. P., Lawrie, S. M., Blackwood, D. H. R., Johnstone, E. C., and Goodwin, G. M. (1995) Hypofrontality revisited: a high resolution single photon emission computed tomography study in schizophrenia J. Neurosurg. Psychiatry 58, 452-456
36. Andreasen, N. C., Rezai, K., Alliger, R., Swayze, V. W., 2nd, Flaum, M., Kirchner, P., Cohen, G., and O'Leary, D. S. (1992) Hypofrontality in neuroleptic-naive patients and in patients with chronic schizophrenia Arch. Gen. Psychiatry 49, 943-958
37. Hoshi, Y., Shinba, T., Sato, C., and Doi, N. (2006) Resting hypofrontality in schizophrenia: A study using near-infrared time-resolved spectroscopy Schizophr. Res. 84, 411-420
38. Steinberg, J. L., Devous, M. D., Sr., and Paulman, R. G. (1996) Wisconsin card sorting activated regional cerebral blood flow in first break and chronic schizophrenic patients and normal controls Schizophr. Res. 19, 177-187
39. Callicott, J. H., Bertolino, A., Mattay, V. S., Langheim, F. J. P., Duyn, J., Coppola, R., Goldberg, T. E., and Weinberger, D. R. (2000) Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited Cereb. Cortex 10, 1078-1092
40. Lowry, J. P. and Fillenz, M. (2001) Real-Time Monitoring of Brain Energy Metabolism In Vivo using Microelectrochemical Sensors: The Effects of Anesthesia Bioelectrochemistry 54, 39-47
41. Vahabzadeh, A. and Fillenz, M. (1994) Comparison of stress-induced changes in noradrenergic and serotonergic neurons in the rat hippocampus using microdialysis Eur. J. Neurosci. 6, 1205-1212
42. Freed, W. J., Bing, L. A., and Wyatt, R. J. (1984) Effects of neuroleptics on phencyclidine (PCP)-induced locomotor stimulation in mice Neuropharmacology 23, 175-81
43. Bristow, L. J., Hutson, P. H., Thorn, L., and Tricklebank, M. D. (1993) The glycine/NMDA receptor antagonist, R-(+)-HA-966, blocks activation of the mesolimbic dopaminergic system induced by phencyclidine and dizocilpine (MK-801) in rodents Br. J. Pharmacol. 108, 1156-1163
44. Magistretti, P. J. and Pellerin, L. (1996) Cellular bases of brain energy metabolism and their relevance to functional brain imaging: evidence for a prominent role of astrocytes Cereb. Cortex 6, 50-61
45. Fillenz, M., Lowry, J. P., Boutelle, M. G., and Fray, A. E. (1999) The role of astrocytes and noradrenaline in neuronal glucose metabolism Acta Physiol. Scand. 167, 275-284
46. Weissman, A. D., Dam, M., and London, E. D. (1987) Alterations in local cerebral glucose utilization induced by phencyclidine Brain Res. 435, 29-40
47. Gao, X. M., Shirakawa, O., Du, F., and Tamminga, C. A. (1993) Delayed regional metabolic actions of phencyclidine Eur. J. Pharmacol. 241, 7-15
48. Duncan, G. E., Leipzig, J. N., Mailman, R. B., and Lieberman, J. A. (1998) Differential effects of clozapine and haloperidol on ketamineinduced brain metabolic activation Brain Res. 812, 65-75
49. Homayoun, H. and Moghaddam, B. (2007) NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurones and pyramidal neurones J. Neurosci. 27, 11496-11500
50. Pratt, J. A., Winchester, C., Egerton, A., Cochran, S. M., and Morris, B. J. (2008) Modelling prefrontal cortex deficits in schizophrenia: implications for treatment Br. J. Pharmacol. 153, S465-S470
51. Fejgin, K., PàŠlsson, E., Wass, C., Svensson, L., and Klamer, D. (2008) Nitric oxide signaling in the medial prefrontal cortex is involved in the biochemical and behavioral effects of phencyclidine Neuropsychopharmacology 33, 1874-1883
52. B receptor activation attenuates phencyclidine-induced impairments of prepulse inhibition: involvement of nitric oxide Neuropsychopharmacology 34, 1673-1684
53. Wultsch, T., Chourbaji, S., Fritzen, S., Kittelt, S., Grünblatt, E., Gutknecht, L., Chizat, F., Golfier, G., Schmitt, A., Gass, P., Lesch, K. P., and Reif, A. (2007) Behavioural and expressional phenotyping of nitric oxide synthase-I knockdown animals J. Neural Transm., Suppl. 72, 69-85
54. Harooni, H. E., Naghdi, N., Sepehri, H., and Rohani, A. H. (2009) The role of hippocampal nitric oxide (NO) on learning and immediate, short- and long-term memory retrieval in inhibitory avoidance task in male adult rat Behav. Brain Res. 201, 166-172
55. Jentsch, J. D., Tran, A., Le, D., Youngren, K. D., and Roth, R. H. (1997) Subchronic phencyclidine administration reduces mesoprefrontal dopamine utilization and impairs prefrontal cortical-dependent cognition in the rat Neuropsychopharmacology 17, 92-99
56. Morton, D. B. and Griffiths, P. H. M. (1985) Guidelines on the recognition of pain and discomfort in experimental animals and an hypothesis for assessment Vet Rec. 116, 431-6