Use of Behavioral Responses

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The use of behavioral responses in fMRI-based studies began as a comforting demonstration that subjects were doing what the experimenter had asked them to do. However, behavioral measures can be much more useful. Two studies of memory, for example, made use of behavioral data collected after the MRI scanning session was over and the subject was out of the magnet to retroactively specify the data analytic process. One study of the effects of a drug used the subject's behaviorally reported mental state to obtain a temporal function that could be correlated with the brain imaging data.

The two memory studies each made use of the visual presentation of stimuli during the fMRI scanning session. In one case the stimuli were pictures; in the other case they were words. In both cases the subjects had an irrelevant task to perform related to these stimuli. After the scanning session was over, the subjects were given a memory task (without prior warning) to determine which of the test stimuli they recalled seeing. The key idea here was to group the imaging data according to whether the data were collected during the presentation of stimuli that were subsequently remembered versus the presentation of stimuli that were subsequently forgotten. The expectation (which was confirmed) was that various parts of the brain associated with long-term memory and encoding would have been more active on those trials in which the stimulus was subsequently recalled.

The drug study used behavioral measures more directly in analyzing the fMRI data. The study involved the challenging task of measuring fMRI changes during the administration of a psychoactive drug, cocaine. Subjects were regular cocaine users who had declined treatment but who had volunteered for a study. During the course of an imaging session they were given either a placebo or an injection of cocaine. (There were two imaging runs, so each subject received the cocaine on one run and the placebo on the other.) During the runs subjects regularly reported on their subjective state of ''high,'' "low," ''rush,'' and ''craving''—terms that were known to be associated with cocaine experiences.

Note that there are unique technical challenges in this study. In addition to being a psychoactive drug, cocaine is also a cardiovascular stimulant. Therefore, before considering the possible effects of cocaine in its psychoactive and addicting role, it was necessary to demonstrate that such effects would not be masked by the circulatory effects of the drug. To accomplish this, the investigators used a standard stimulus (flashing light) to calibrate neuronally triggered hemodynamic responses. Also, they used two imaging pulse sequences: one that was sensitive to BOLD effects and

Figure 5 Voluntary attention modulates activity in human visual cortex. This collection of images summarizes an early fMRI-based experiment demonstrating the detection of neural modulation due to the exertion of voluntary attention. Subjects viewed a continuous movie consisting of a cross in the middle of the visual vield (on which they were instructed to fixate) and moving black dots and stationary white dots in the periphery. The cartoon at the upper right represents one frame of this movie, with arrows indicating the direction of motion. In the actual stimuli, of course, there were no arrows present—only moving, stationary dots and the fixation cross. The motion was always radial, toward the fixation point, to make it easy for the subjects to maintain fixation. Additional testing with an MR-compatible eyetracker revealed that subjects could maintain fixation. While looking at this movie for several minutes, subjects received verbal instructions to attend to one collection of colored dots or the other. These instructions alternated every 20 sec, as indicated in the figure by the black ("attend black'') and white ("attend white'') arrows on the timeline, below the visual stimulus. When the subjects heard "attend black,'' they would continue to fixate the central cross, but they were supposed to pay more attention to the black (moving) dots than the white (stationary) dots during that time. Similarly, when they heard "attend white,'' they were supposed to attend more to the white (stationary) dots. The imaging data were collected with a small coil of wire (about 13 cm in diameter) placed near the occipital cortex (the back of the head). This yielded a stronger signal in the brain regions of interest for the experiment, but it yielded weak signals from the rest of the brain, as indicated in the structural image shown at the upper left and the functional image shown in the lower left. Data for five slices, oriented parallel to the calcarine fissure (primary visual cortex), were collected (as indicated by the lines in the upper left). Data from one of those slices is shown in the lower left. As described for Fig. 4, a pseudocolor representation of the results of a statistical test comparing the MR data collected during one condition ("attend black'') versus the other condition ("attend white'') is displayed. There was a clear increase in activity on both the left and the right sides of this brain, in a region that corresponds anatomically to a known visual motion processing area of the cortex. Data from the voxels of the brain whose statistic exceeded the threshold used to specify the color map were averaged; the results are plotted as a function of time in the graph in the lower right. Data collected during the time that subjects were attending to moving stimuli (light background portions of the graph) were clearly higher in amplitude than the data collected during the time that subjects were attending to the stationary stimuli (dark background), even though the visual stimulus was unchanged throughout the entire scanning period. This experiment represents a simple, dramatic demonstration of the ability of fMRI to detect the neural consequences of changes in cognitive state (data and analysis courtesy of Kathleen O'Craven).

one that was sensitive to flow effects. This combination allowed them to demonstrate that cocaine influenced the flow-dependent MR signal changes but not the BOLD MR signal changes.

Thus, they could use the BOLD changes to study the effects of cocaine in its role as a psychoactive stimulant relatively independent of its role as a cardiovascular stimulant. Using the time course profile obtained from the behavioral ratings (specifically, the temporal modulation of craving and rush) they could find brain areas whose activity followed a similar profile, allowing them to conclude that those areas were implicated in the experience of these sensations.

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