Functional Imaging And Correlates Of Neural Activity

It has been known for more than 100 years that blood flow to the brain increases in a regionally specific manner, according to mental activity. The father of modern psychology, William James, was aware of observations relating regional brain pulsation to mental activity (James 1890). Paul Broca, known primarily for his observations on the effects of left frontal lesions on language, performed several experiments relating regional brain temperature to cognitive function (Broca 1879). But it was not until the 1950s, when Seymour Kety and Louis Sokoloff developed the autoradiographic technique for quantitatively measuring regional blood flow, that specific cognitive functions could be directly mapped in the living brain (Kety 1965).

Both PET and fMRI rely on the fact that blood flow increases in areas where neuronal activity increases, and most studies implicitly assume the validity of this relationship. It is easy to see the link in terms of an increased metabolic demand. The activation of a neural circuit is a complex network of electrochemical processes that requires energy. The most demanding processes, in terms of energy expenditure, are those related to synaptic activity, which results in breakdown of energy stores in the neuron in the form of adenosine triphosphate (ATP) molecules. To replace the ATP energy stores degraded by the increased metabolic demand, a surge in the concentration of glucose and oxygen is necessary, which results in increased blood flow to the activated region. It is this vascular or hemodynamic response to neural activity—that is, the variation in regional cerebral blood flow (rCBF)—that is the quantity actually measured in the majority of brain activation studies with fMRI and PET/SPECT (Arthurs and Boniface 2002; Jueptner and Weiller 1995). Thus, the hemodynamic response represents an indirect assay of neural activity (Villringer and Dirnagl 1995). It is important to note that the hemodynamic response lags behind the actual neural activity by a few seconds. The hemodynamic response is also blurred in the spatial domain compared with the underlying neural activity. This imposes limits on the spatiotemporal resolution of blood flow methods, independently of technology improvement.

A special caveat should be noted concerning the interpretation of rCBF results. The measurement of task-related variations of rCBF does not provide any clear indication about the nature of the underlying neural activity (i.e., whether it is excitatory or inhibitory), although hypotheses have been proposed for and argued against a bias favoring excitatory contributions (Heeger et al. 1999; Tagamets and Horwitz 2001; Waldvogel et al. 2000). The construction of specific inferences about the actual state of activity —actively excited or actively inhibited—of brain regions showing an increase in rCBF during an experimental task would require the integration of information from many different sources (e.g., electrophysiology, neurochemistry, cytoarchitectonics).

In summary, despite the fact that the physiological and biochemical processes linking the neural activity and the hemodynamic response have not been clarified yet, the empirical relationship between these parameters appears both reliable and reproducible in a variety of contexts. The validity of fMRI measurements of signal change as an assay of neural activity has been documented using electrophysiological techniques such as neuronal field potentials (Logothetis et al. 2001).

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