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Correlation Between BOLD fMRI and Theta-Band Local Field Potentials in the Human Hippocampal Area

¹Center for Cognitive Neuroscience, Semel Institute, Department of Psychiatry and Biobehavioral Sciences, ³Department of Neurology, Seizure Disorder Center, and ⁵Division of Neurosurgery, David Geffen School of Medicine and Semel Institute For Neuroscience and Human Behavior, University of California, Los Angeles, California; ²Center for Neuroscience, University of California, Davis, California; ⁴Keck School of Medicine at University of Southern California, Comprehensive Epilepsy Program, Los Angeles, California; and ⁶Functional Neurosurgery Unit, Tel-Aviv Medical Center and Sackler School of Medicine, Tel-Aviv University, Tel-Aviv, Israel

Submitted 24 November 2008; accepted in final form 20 February 2009

The relation between the blood-oxygen-level-dependent (BOLD) signal, which forms the basis of functional magnetic resonance imaging (fMRI), and underlying neural activity is not well understood. We performed high-resolution fMRI in patients scheduled for implantation with depth electrodes for seizure monitoring while they navigated a virtual environment. We then recorded local field potentials (LFPs) and neural firing rate directly from the hippocampal area of the same subjects during the same task. Comparing BOLD signal changes with 396 LFP and 185 neuron recordings in the hippocampal area, we found that BOLD signal changes correlated positively with LFP power changes in the theta-band (4–8 Hz). This correlation, however, was largely present for parahippocampal BOLD signal changes; BOLD changes in the hippocampus correlated weakly or not at all with LFP power changes. We did not find a significant relationship between BOLD activity and neural firing rate in either region, which could not be accounted for by a lesser tendency for neurons to respond or a greater tendency for neurons to habituate to the task. Strengthening the idea of a dissociation between LFP power and neural firing rate in their relation to the BOLD signal, simultaneously recorded LFP power and neural firing rate changes were uncorrelated across electrodes. Together, our results suggest that the BOLD signal in the human hippocampal area has a more heterogenous relationship with underlying neural activity than has been described previously in other brain regions.

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