Energetics of neuronal signaling and fMRI activity

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 104; no. 51; pp. 20546 - 20551
• Main Authors: Maandag, Natasja J.G, Coman, Daniel, Sanganahalli, Basavaraju G, Herman, Peter, Smith, Arien J, Blumenfeld, Hal, Shulman, Robert G, Hyder, Fahmeed
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 18-12-2007; National Acad Sciences
• Subjects: Anesthesia; Anesthesiology; Anesthetics; Animals; Biological Sciences; Brain; Electric Stimulation; Electrophysiology; Histograms; M region; Magnetic Resonance Imaging; Male; Neural Conduction; Neurons; Neurons, Afferent - physiology; Neuroscience; NMR; Nuclear magnetic resonance; Oxidation; Rats; Rats, Sprague-Dawley; Rodents; Signal Transduction; Somatosensory Cortex - cytology; Somatosensory Cortex - physiology
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.0709515104

Energetics of resting and evoked fMRI signals were related to localized ensemble firing rates (ν) measured by electrophysiology in rats. Two different unstimulated, or baseline, states were established by anesthesia. Halothane and α-chloralose established baseline states of high and low energy, respectively, in which forepaw stimulation excited the contralateral primary somatosensory cortex (S1). With α-chloralose, forepaw stimulation induced strong and reproducible fMRI activations in the contralateral S1, where the ensemble firing was dominated by slow signaling neurons (SSN; ν range of 1-13 Hz). Under halothane, weaker and less reproducible fMRI activations were observed in the contralateral S1 and elsewhere in the cortex, but ensemble activity in S1 was dominated by rapid signaling neurons (RSN; ν range of 13-40 Hz). For both baseline states, the RSN activity (i.e., higher frequencies, including the γ band) did not vary upon stimulation, whereas the SSN activity (i.e., α band and lower frequencies) did change. In the high energy baseline state, a large majority of total oxidative energy [cerebral metabolic rate of oxygen consumption (CMRO₂)] was devoted to RSN activity, whereas in the low energy baseline state, it was roughly divided between SSN and RSN activities. We hypothesize that in the high energy baseline state, the evoked changes in fMRI activation in areas beyond S1 are supported by rich intracortical interactions represented by RSN. We discuss implications for interpreting fMRI data where stimulus-specific ΔCMRO₂ is generally small compared with baseline CMRO₂.