Estimates of the Contribution of Single Neurons to Perception Depend on Timescale and Noise Correlation

The sensitivity of a population of neurons, and therefore the amount of sensory information available to an animal, is limited by the sensitivity of single neurons in the population and by noise correlation between neurons. For decades, therefore, neurophysiologists have devised increasingly clever and rigorous ways to measure these critical variables (Parker and Newsome, 1998). Previous studies examining the relationship between the responses of single middle temporal (MT) neurons and direction-discrimination performance uncovered an apparent paradox. Sensitivity measurements from single neurons suggested that small numbers of neurons may account for a monkey's psychophysical performance (Britten et al., 1992), but trial-to-trial variability in activity of single MT neurons are only weakly correlated with the monkey's behavior, suggesting that the monkey's decision must be based on the responses of many neurons (Britten et al., 1996). We suggest that the resolution to this paradox lies (1) in the long stimulus duration used in the original studies, which led to an overestimate of neural sensitivity relative to psychophysical sensitivity, and (2) mistaken assumptions (because no data were available) about the level of noise correlation in MT columns with opposite preferred directions. We therefore made new physiological and psychophysical measurements in a reaction time version of the direction-discrimination task that matches neural measurements to the actual decision time of the animals. These new data, considered together with our recent data on noise correlation in MT (Cohen and Newsome, 2008), provide a substantially improved account of psychometric performance in the direction-discrimination task.