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The Journal of Neuroscience, August 16, 2006, 26(33):8409-8416; doi:10.1523/JNEUROSCI.4615-05.2006

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Behavioral/Systems/Cognitive
Differential Effects of NMDA and AMPA Glutamate Receptors on Functional Magnetic Resonance Imaging Signals and Evoked Neuronal Activity during Forepaw Stimulation of the Rat

Willy Gsell,^1,2,3 * Michael Burke,^1,4 Dirk Wiedermann,¹ Gilles Bonvento,⁵ Afonso C. Silva,⁶ François Dauphin,^2,7 Christian Bührle,^1,8 Mathias Hoehn,¹ and Wolfram Schwindt^1,9 *

¹Max Planck Institute for Neurological Research, 50931 Cologne, Germany, ²Centre National de la Recherche Scientifique, Unité Mixte de Recherche 6551, University of Caen, 14032 Caen, France, ³7T MR Facility, Wellcome Surgical Institute, University of Glasgow, Glasgow 6G1 1QH, United Kingdom, ⁴Faculty of Psychology, Section for Experimental and Biological Psychology, Universität Marburg, 35032 Marburg, Germany, ⁵Commissariat à l’Energie Atomique, Unité de Recherche Associée, Centre National de la Recherche Scientifique 2210, Service Hospitalier Frédéric Joliot, 91401 Orsay, France, ⁶Laboratory of Functional and Molecular Imaging, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland 20892, ⁷Pharmacology, Centre d’Etudes et de Recherche sur le Médicament de Normandie, University of Caen, 14032 Caen, France, ⁸Department of Stereotactic and Functional Neurosurgery, University of Cologne, 50923 Cologne, Germany, and ⁹Department of Clinical Radiology, University Hospital Münster, 48129 Münster, Germany

Correspondence should be addressed to Dr. Wolfram Schwindt, Department of Clinical Radiology, University Hospital Münster, D-48129 Münster, Germany. Email: wschwindt{at}uni-muenster.de

Most of the currently used methods for functional brain imaging do not visualize neuronal activity directly but rather rely on the elicited hemodynamic and/or metabolic responses. Glutamate, the major excitatory neurotransmitter, plays an important role in the neurovascular/neurometabolic coupling, but the specific mechanisms are still poorly understood. To investigate the role of the two major ionotropic glutamate receptors [NMDA receptors (NMDA-Rs) and AMPA receptors (AMPA-Rs)] for the generation of functional magnetic resonance imaging (fMRI) signals, we used fMRI [measurements of blood oxygenation level-dependent (BOLD), perfusion-weighted imaging (PWI), and cerebral blood volume (CBV)] together with recordings of somatosensory evoked potentials (SEPs) during electrical forepaw stimulation in the -chloralose anesthetized rat. Intravenous injection of the NMDA-R antagonist MK-801 [(+)-5-methyl-10,11-dihydro-5H-dibenzo [a,d] cyclohepten-5,10-imine maleate] (0.06 mg/kg plus 3.6 µg · kg^–1 · h^–1) significantly decreased BOLD (–51 ± 19%; n = 5) and PWI (–57 ± 26%; n = 5) responses but reduced the SEPs only mildly (approximately –10%). Systemic application of the AMPA-R antagonist GYKI-53655 [1-(4-aminophenyl)-3-methylcarbamyl-4-methyl7,8-methylenedioxy-3,4-dihydro-5H-2,3-benzodiazepine] significantly decreased both the hemodynamic response (BOLD, –49 ± 13 and –65 ± 15%; PWI, –22 ± 48 and –68 ± 4% for 5 and 7 mg/kg, i.v., respectively; CBV, –80 ± 7% for 7 mg/kg; n = 4) and the SEPs (up to –60%). These data indicate that the interaction of glutamate with its postsynaptic and/or glial receptors is necessary for the generation of blood flow and BOLD responses and illustrate the differential role of NMDA-Rs and AMPA-Rs in the signaling chain leading from increased neuronal activity to the hemodynamic response in the somatosensory cortex.

Key words: glutamate; AMPA receptors; NMDA receptors; functional magnetic resonance imaging; evoked potentials; somatosensory cortex; rat

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Received June 3, 2004; revised June 27, 2006; accepted June 28, 2006.

Correspondence should be addressed to Dr. Wolfram Schwindt, Department of Clinical Radiology, University Hospital Münster, D-48129 Münster, Germany. Email: wschwindt{at}uni-muenster.de

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