Learning from invariants predicts upcoming behavioral choice from spiking activity in monkey V1

Animals frequently make decisions based on sensory cues. In such a setting, the overlap in the information on the stimulus and on the choice is crucial for the formation of informed behavioral decisions. Yet, how the information on the stimulus and on the choice interact in the brain is poorly understood. Here, we study the representation of a binary decision variable in the primary visual cortex (V1) while macaque monkeys perform delayed match-to-sample task on naturalistic visual stimuli close to psychophysical threshold. Using population vectors, we demonstrate the overlap in decoding spaces on binary stimulus classes "match/non-match" and binary choices "same /different" of the animal. Leveraging this overlap, we use learning from the invariant information across the two classification problems to predict the choice of the animal as a time-dependent population signal. We show the importance of the across-neuron organization and the temporal structure of spike trains for the decision signal and suggest how noise correlations between neurons with similar decoding selectivity are helpful for the accumulation of the decision signal. Finally, we show that decision signal is primarily carried by bursting neurons in the superficial layers of the cortex. Author summaryV1 is necessary for normal visual processing and is known to process features of visual stimuli such as orientation, but whether V1 also encodes behavioral decisions is an unresolved issue, with conflicting evidence. Here, we demonstrate that V1 encodes a mixed variable that contains the information about the stimulus as well as about the choice. We learn the structure of population responses in trials pertaining to the variable "stimulus+choice", and apply the resulting population vectors to trials that differ only about the choice of the animal, but not about the stimulus class. Moreover, we learn structure of population responses on time-averaged data and then apply it on time-dependent (spiking) data. During the late phase of the trial, this procedure allows to predict the upcoming choice of the animal with a time-dependent population signal. The spiking signal of small neural population is sparse, and we hypothesize that positive correlations between neurons in the same decoding pool help the transmission of the decision-related information downstream. We find that noise correlations in the same decoding pool are significantly stronger than across coding pools, which corroborates our hypothesis on the benefit of noise correlations for the read-out of a time-dependent population signal.