Hemodynamic signals not predicted? Not so: a comment on Sirotin and Das (2009)

In their 2009 Nature article: "Anticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity," Yevginiy Sirotin and Aniruddha Das suggest that hemodynamic signals, the basis of functional MRI (fMRI), can arise without any measurable neuronal activity. They report that hemodynamic signals in visual cortex were associated with and time-locked to the anticipation of a visual stimulus, and importantly, without any associated neuronal activity as measured with direct electrophysiological recordings. In this commentary, we demonstrate, using an assessment of their own data, that their claims are not strongly supported. In fact, we found that specific LFP frequency ranges predicted with a high degree of accuracy, the "dark" or "anticipatory" hemodynamic response. For other frequency ranges, we found differences in phase but not magnitude of the measured and predicted hemodynamic response. Importantly, when comparing simply the magnitude as well as the time series standard deviation of the electrophysiological recordings with those of the measured hemodynamic responses, we found a direct correspondence of the dark/stimulated magnitude and standard deviation between the electrophysiological recordings and the hemodynamic responses. All of these analyses strongly imply that anticipatory hemodynamic responses are, in fact, accurately predicted in phase and magnitude by several LFP frequency bands, and are predicted in standard deviation and magnitude by the standard deviation and magnitude of even a wider range of LFP frequencies. We argue that rather than casting doubt on fMRI signal changes, these studies open up an interesting window into exploring more subtle neurovascular relationships.