Abstract
For stimuli near perceptual threshold, the trial-by-trial activity of single neurons in many sensory areas is correlated with the animal's perceptual report. This phenomenon has often been attributed to feedforward readout of the neural activity by the downstream decision-making circuits. The interpretation of choice-correlated activity is quite ambiguous, but its meaning can be better understood in the light of population-wide correlations among sensory neurons. Using a statistical nonlinear dimensionality reduction technique on single-trial ensemble recordings from the middle temporal (MT) area during perceptual-decision-making, we extracted low-dimensional latent factors that captured the population-wide fluctuations. We dissected the particular contributions of sensory-driven versus choice-correlated activity in the low-dimensional population code. We found that the latent factors strongly encoded the direction of the stimulus in single dimension with a temporal signature similar to that of single MT neurons. If the downstream circuit were optimally utilizing this information, choice-correlated signals should be aligned with this stimulus encoding dimension. Surprisingly, we found that a large component of the choice information resides in the subspace orthogonal to the stimulus representation inconsistent with the optimal readout view. This misaligned choice information allows the feedforward sensory information to coexist with the decision-making process. The time course of these signals suggest that this misaligned contribution likely is feedback from the downstream areas. We hypothesize that this non-corrupting choice-correlated feedback might be related to learning or reinforcing sensory-motor relations in the sensory population.
Highlights
Sensory cortical neurons exhibit substantial variability to repeated presentations of the same stimulus [1, 2]
The correlation between variability in sensory neurons and perceptual decisions is sometimes explained by a causal, feedforward role of sensory noise in behavior
This variability depends on the specifics of the sensory stimulus and task being performed [3,4,5,6,7], and is often correlated with the trial-by-trial perceptual report of the animal [8,9,10,11]. This trial-by-trial correlation between neural responses and perceptual reports, often quantified as choice probability (CP), has long been of interest for its potential to reveal the mechanisms by which downstream areas read out the response of relevant population of sensory neurons [12,13,14]
Summary
Sensory cortical neurons exhibit substantial variability to repeated presentations of the same stimulus [1, 2]. This trial-by-trial correlation between neural responses and perceptual reports, often quantified as choice probability (CP), has long been of interest for its potential to reveal the mechanisms by which downstream areas read out the response of relevant population of sensory neurons [12,13,14] This interpretation is complicated by the presence of interneuronal correlations [15], top-down feedback [9, 16] and depends on assumptions about the readout mechanisms of downstream brain areas [12, 14, 16, 17]. Why would the brain bother to feedback a choice or decision that corrupts the sensory information and make it do worse on the task? Here, we propose an alternative hypothesis: the feedback can be non-corrupting, effectively multiplexing choice signals in a sensory population without diminishing information about the stimulus
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