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The Journal of Neuroscience, January 5, 2005, 25(1):68-77; doi:10.1523/JNEUROSCI.2823-04.2005

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Neurobiology of Disease
Temporal Dependence in Uncoupling of Blood Volume and Oxygenation during Interictal Epileptiform Events in Rat Neocortex

Minah Suh, Sonya Bahar, Ashesh D. Mehta, and Theodore H. Schwartz

Department of Neurological Surgery, Weill Medical College of Cornell University, New York, New York 10021

We investigated the dynamic spatiotemporal relationships of cerebral blood volume (CBV), deoxygenated hemoglobin (Hbr), and light scatter (LS) associated with interictal epileptiform events with multiwavelength optical recording of intrinsic signals and simultaneous field potential recording. Interictal spikes (IISs) were induced with iontophoresis of bicuculline methiodide in rat neocortex. Intrinsic signal changes appeared as early as 100 msec after the IIS at all wavelengths and could be appreciated after only a single IIS. Initially, the largest signal arose from a focal increase in deoxygenation, which lasted for 2 sec, consistent with an "initial dip." An equally early focal increase in CBV had a smaller amplitude than the Hbr signal until >2 sec after the IIS, when its amplitude surpassed that of the Hbr signal but also spread to a larger, less focal area. The most spatially restricted and smallest amplitude signal was produced by LS. A later hyperoxygenation, or increase in blood oxygenation level-dependent signal, was often seen in the draining veins but inconsistently seen in the IIS focus. An inverted optical signal was recorded at all wavelengths from multiple regions in the surrounding cortex within 100 msec of the IIS. We therefore conclude that the IIS induces a rapid increase in metabolic demand, which cannot be met by a rapid, initially focal but small increase in CBV that results in a prolonged increase in Hbr (epileptic dip in oxygenated hemoglobin). The inverted optical signal in the surround arises from a decrease in CBV and a decrease in Hbr, likely resulting from a combination of shunting of CBV to the focus and decreased metabolic demand resulting from decreased neuronal activity, consistent with "surround inhibition."

Key words: bicuculline; epilepsy; neocortex; rat; interictal spike; optical imaging; intrinsic signal; hemoglobin; initial dip; cerebral blood volume; BOLD; fMRI

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Received March 26, 2004; revised October 1, 2004; accepted October 1, 2004.

This article has been cited by other articles:

				H. Ma, M. Zhao, M. Suh, and T. H. Schwartz Hemodynamic Surrogates for Excitatory Membrane Potential Change During Interictal Epileptiform Events in Rat Neocortex J Neurophysiol, May 1, 2009; 101(5): 2550 - 2562. [Abstract] [Full Text] [PDF]

				M. Zhao, H. Ma, M. Suh, and T. H. Schwartz Spatiotemporal Dynamics of Perfusion and Oximetry during Ictal Discharges in the Rat Neocortex J. Neurosci., March 4, 2009; 29(9): 2814 - 2823. [Abstract] [Full Text] [PDF]

				E. A. Allen, B. N. Pasley, T. Duong, and R. D. Freeman Transcranial Magnetic Stimulation Elicits Coupled Neural and Hemodynamic Consequences Science, September 28, 2007; 317(5846): 1918 - 1921. [Abstract] [Full Text] [PDF]

				M. Fukuda, C.-H. Moon, P. Wang, and S.-G. Kim Mapping Iso-Orientation Columns by Contrast Agent-Enhanced Functional Magnetic Resonance Imaging: Reproducibility, Specificity, and Evaluation by Optical Imaging of Intrinsic Signal. J. Neurosci., November 15, 2006; 26(46): 11821 - 11832. [Abstract] [Full Text] [PDF]

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