Serial microPET measures of the metabolic reaction to a microdialysis probe implant

Despite the widespread use of chronic brain implants in experimental and clinical settings, the effects of these long-term procedures on brain metabolism and receptor expression remain largely unknown. Under the hypothesis that intracerebral microdialysis transiently alters tissue metabolism, we performed a series of 18FDG microPET scans prior to and following surgical implantation of microdialysis cannulae. Parallel microPET measures using the competitive dopamine (DA) D2 receptor antagonist, 11C-raclopride, provided an assay of DA stability in these same animals. 18FDG scans were performed prior to microdialysis cannulation and again at 2, 12, 24, 48, 120, 168, 360 and 500 h (0.2, 0.5, 1, 2, 5, 7, 15 and 25 days). Separate animals received a sham surgery and the control group had no surgical intervention. For the first 24 h (scans at 2, 12 and 24 h post-surgery) uptake was reduced in both hemispheres. However, by 48 h, contralateral uptake had returned to pre-surgical levels. The striking finding was that from 48 to 500 h, the microdialysis cannulation produced widespread ipsilateral reductions in 18FDG uptake that encompassed the entire hemisphere. Despite the extent and persistence of these reductions, 11C-raclopride binding and ECF DA concentrations remained stable.

[1]  R. Ratcheson,et al.  Effects of Focal Cortical Freezing Lesion on Regional Energy Metabolism , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[2]  S. Nelson,et al.  Effects of microdialysis on brain metabolism in normal and seizure states , 1990, Neuroscience.

[3]  R R MacGregor,et al.  GABAergic inhibition of endogenous dopamine release measured in vivo with 11C-raclopride and positron emission tomography , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  H. Akaike A new look at the statistical model identification , 1974 .

[5]  R. Ratcheson,et al.  Delayed Changes in Regional Brain Energy Metabolism following Cerebral Concussion in Rats , 2002, Metabolic Brain Disease.

[6]  Jean Logan,et al.  Reproducibility of 11C-raclopride binding in the rat brain measured with the microPET R4: effects of scatter correction and tracer specific activity. , 2003, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[7]  A. Osmont,et al.  Determination of 18F-fluoro-2-deoxy-d-glucose rate constants in the anesthetized baboon brain with dynamic positron tomography , 1993, Journal of Neuroscience Methods.

[8]  K. Kiening,et al.  Neuromonitoring: Brain oxygenation and microdialysis , 2003, Current neurology and neuroscience reports.

[9]  R Myers,et al.  Dedicated small animal scanners: a new tool for drug development? , 2002, Current pharmaceutical design.

[10]  D. Alexoff,et al.  Topiramate selectively attenuates nicotine‐induced increases in monoamine release , 2001, Synapse.

[11]  J. Luthman,et al.  Tissue and microdialysate changes after repeated and permanent probe implantation in the striatum of freely moving rats , 1993, Brain Research Bulletin.

[12]  H. Benveniste,et al.  Regional Cerebral Glucose Phosphorylation and Blood Flow After Insertion of a Microdialysis Fiber Through the Dorsal Hippocampus in the Rat , 1987, Journal of neurochemistry.

[13]  B. Westerink,et al.  Brain microdialysis and its application for the study of animal behaviour , 1995, Behavioural Brain Research.

[14]  D. Hovda,et al.  Dynamic changes in local cerebral glucose utilization following cerebral concussion in rats: evidence of a hyper- and subsequent hypometabolic state , 1991, Brain Research.

[15]  L. Hillered,et al.  Microdialysis for Neurochemical Monitoring of the Human Brain , 2003, Scandinavian cardiovascular journal : SCJ.

[16]  S R Cherry,et al.  Quantitative Assessment of Longitudinal Metabolic Changes In Vivo after Traumatic Brain Injury in the Adult Rat using FDG-MicroPET , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[17]  Jeih-San Liow,et al.  Evaluation of anesthesia effects on [18F]FDG uptake in mouse brain and heart using small animal PET. , 2004, Nuclear medicine and biology.

[18]  B. Siesjö,et al.  Mechanisms of secondary brain injury. , 1996, European journal of anaesthesiology.

[19]  L. Hernández,et al.  Simultaneous brain and blood microdialysis study with a new removable venous probe. Serotonin and 5-hydroxyindolacetic acid changes after D-norfenfluramine or fluoxetine. , 1996, Life sciences.

[20]  H. Benveniste,et al.  Cellular reactions to implantation of a microdialysis tube in the rat hippocampus , 2004, Acta Neuropathologica.

[21]  S. Carmichael,et al.  Evolution of Diaschisis in a Focal Stroke Model , 2004, Stroke.

[22]  H. Pappius,et al.  Local cerebral glucose utilization in thermally traumatized rat brain , 1981, Annals of neurology.

[23]  Jurgen Seidel,et al.  Measurement of cerebral glucose metabolic rates in the anesthetized rat by dynamic scanning with 18F-FDG, the ATLAS small animal PET scanner, and arterial blood sampling. , 2004, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[24]  Simon R. Cherry,et al.  In vivo imaging of neuronal activation and plasticity in the rat brain by high resolution positron emission tomography (microPET) , 2000, Nature Biotechnology.

[25]  Simon R. Cherry,et al.  Deficits in Striatal Dopamine D2 Receptors and Energy Metabolism Detected by in Vivo MicroPET Imaging in a Rat Model of Huntington's Disease , 2000, Experimental Neurology.

[26]  P F Morrison,et al.  Steady-state theory for quantitative microdialysis of solutes and water in vivo and in vitro. , 1990, Life sciences.

[27]  A. Marmarou,et al.  Functional compartmentalization of energy production in neural tissue , 1992, Brain Research.

[28]  C. Redies,et al.  In vivo measurement of [18f]fluorodeoxyglucose rate constants in rat brain by external coincidence counting , 1987, Neuroscience.

[29]  L. Colle,et al.  Correlation between behavioral status and cerebral glucose utilization in rats following freezing lesion , 1986, Brain Research.

[30]  S. Dewey,et al.  Sub-chronic low dose γ-vinyl GABA (vigabatrin) inhibits cocaine-induced increases in nucleus accumbens dopamine , 2003, Psychopharmacology.

[31]  R. Ackermann,et al.  Regional comparison of the lumped constants of deoxyglucose and fluorodeoxyglucose , 1989, Metabolic Brain Disease.

[32]  H. Killackey,et al.  Organization of corticocortical connections in the parietal cortex of the rat , 1978, The Journal of comparative neurology.

[33]  S. Hume,et al.  Modulatory effects of L-DOPA on D2 dopamine receptors in rat striatum, measured using in vivo microdialysis and PET , 1998, Journal of Neural Transmission.

[34]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[35]  M. Chesselet,et al.  Metabolic correlates of lesion-specific plasticity: an in vivo imaging study , 2004, Brain Research.

[36]  L. Widén,et al.  Journal of Cerebral Blood Flow and Metabolism Rapid Feasibility Studies of Tracers for Positron Emission Tomography: High-resolution Pet in Small Animals with Kinetic Analysis , 2022 .

[37]  R. Busto,et al.  Uncoupling of local cerebral glucose metabolism and blood flow after acute fluid-percussion injury in rats. , 1997, The American journal of physiology.

[38]  R. Leahy,et al.  High-resolution 3D Bayesian image reconstruction using the microPET small-animal scanner. , 1998, Physics in medicine and biology.

[39]  M. Reivich,et al.  THE [14C]DEOXYGLUCOSE METHOD FOR THE MEASUREMENT OF LOCAL CEREBRAL GLUCOSE UTILIZATION: THEORY, PROCEDURE, AND NORMAL VALUES IN THE CONSCIOUS AND ANESTHETIZED ALBINO RAT 1 , 1977, Journal of neurochemistry.

[40]  Anat Biegon,et al.  Dynamic changes in N-methyl-D-aspartate receptors after closed head injury in mice: Implications for treatment of neurological and cognitive deficits. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Arthur W. Toga,et al.  A 3D digital map of rat brain , 1995, Brain Research Bulletin.

[42]  G. Sedvall,et al.  Quantitative analysis of D2 dopamine receptor binding in the living human brain by PET. , 1986, Science.

[43]  C. Hamani,et al.  Microdialysis in the human brain: review of its applications. , 1997, Neurological research.

[44]  William H. Press,et al.  Numerical recipes in C , 2002 .

[45]  N. Reynolds,et al.  Extracellular perfusion of rat brain nuclei using microdialysis: a method for studying differential neurotransmitter release in response to neurotoxins. , 1999, Brain research. Brain research protocols.

[46]  M. Reivich,et al.  Cerebral hemodynamic and metabolic alterations in stroke. , 1977, Advances in experimental medicine and biology.

[47]  J. Brodie,et al.  GABAergic blockade of cocaine-associated cue-induced increases in nucleus accumbens dopamine. , 2001, European journal of pharmacology.

[48]  N. Volkow,et al.  Distribution Volume Ratios without Blood Sampling from Graphical Analysis of PET Data , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[49]  H. Benveniste,et al.  Microdialysis—Theory and application , 1990, Progress in Neurobiology.

[50]  N. Volkow,et al.  Selegiline potentiates cocaine‐induced increases in rodent nucleus accumbens dopamine , 2003, Synapse.

[51]  Jean Logan,et al.  Development of a simultaneous PET/microdialysis method to identify the optimal dose of 11C-raclopride for small animal imaging , 2005, Journal of Neuroscience Methods.

[52]  Sanjiv Sam Gambhir,et al.  AMIDE: a free software tool for multimodality medical image analysis. , 2003, Molecular imaging.

[53]  J. Brodie,et al.  Stereoselective inhibition of dopaminergic activity by gamma vinyl-GABA following a nicotine or cocaine challenge: a PET/microdialysis study. , 2000, Life sciences.