Ready…Go: Amplitude of the fMRI Signal Encodes Expectation of Cue Arrival Time

Abstract

What happens when the brain awaits a signal of uncertain arrival time, as when a sprinter waits for the starting pistol? And what happens just after the starting pistol fires? Using functional magnetic resonance imaging (fMRI), we have discovered a novel correlate of temporal expectations in several brain regions, most prominently in the supplementary motor area (SMA). Contrary to expectations, we found little fMRI activity during the waiting period; however, a large signal appears after the “go” signal, the amplitude of which reflects learned expectations about the distribution of possible waiting times. Specifically, the amplitude of the fMRI signal appears to encode a cumulative conditional probability, also known as the cumulative hazard function. The fMRI signal loses its dependence on waiting time in a “countdown” condition in which the arrival time of the go cue is known in advance, suggesting that the signal encodes temporal probabilities rather than simply elapsed time. The dependence of the signal on temporal expectation is present in “no-go” conditions, demonstrating that the effect is not a consequence of motor output. Finally, the encoding is not dependent on modality, operating in the same manner with auditory or visual signals. This finding extends our understanding of the relationship between temporal expectancy and measurable neural signals. Like the sprinter waiting for the starting pistol, all animals develop expectations about when events will occur in time. We explored the neural correlates of readiness and expectation using functional magnetic resonance imaging (fMRI), and found areas of the brain in which the fMRI signal remains at baseline during the waiting period and rises sharply after a cue to react (a “go” cue). Strikingly, the amplitude of the rise reflects a function of the probability of an event occurring at that time. The dependence on probability remains even in the absence of a motor act (that is, not pressing a button when the go cue appears). When the arrival time of the go cue is known in advance, the expectation-dependent signal disappears, indicating that this brain response reflects expectation, not simply elapsed time. These results match up with prior studies of expectation in the brain, with one important difference: previously, electrophysiology experiments showed that expectation is encoded by a build-up of spiking activity as the waiting period progresses, while our fMRI data reveal a signature of expectation that becomes apparent after the waiting concludes. We discuss the apparent mismatch between these different technologies for measuring expectation-related activity in the brain.