Population temporal structure supplements the rate code during sensorimotor transformations

Sensorimotor transformations are mediated by premotor brain networks where individual neurons represent sensory, cognitive, and movement-related information. Such multiplexing poses a conundrum – how does a decoder know precisely when to initiate a movement if its inputs are active at times when a movement is not desired (e.g., in response to sensory stimulation)? Here, we propose a novel hypothesis: movement is triggered not only by an increase in firing rate, but critically by a reliable temporal pattern in the population response. Laminar recordings in the superior colliculus (SC), a midbrain region that plays an essential role in orienting eye movements, indicate that the temporal structure across neurons is a factor governing movement initiation. Specifically, using a measure that captures the fidelity of the population code - here called temporal stability - we show that the temporal structure fluctuates during the visual response but becomes increasingly stable during the movement command, even when the mean population activity is similar between the two epochs. Analyses of pseudo-populations in SC and cortical frontal eye fields (FEF) corroborated this model. We also used spatiotemporally patterned microstimulation to causally test the contribution of population temporal stability to movement initiation and found that stable stimulation patterns were more likely to evoke a movement, even when other features of the patterns such as mean pulse rates and population state subspaces were matched. Finally, a spiking neuron model was able to discriminate between stable and unstable input patterns, providing a putative biophysical mechanism for decoding temporal structure. These findings offer an alternative perspective on the relationship between movement preparation and generation by situating the correlates of movement initiation in the temporal features of activity in shared neural substrates. They also suggest a need to look beyond the instantaneous rate code at the single neuron or population level and consider the effects of short-term population history on neuronal communication and behaviour. Summary Sensorimotor transformations are mediated by premotor brain networks where individual neurons represent sensory, cognitive, and movement-related information. Such multiplexing poses a conundrum - how does a decoder know precisely when to initiate a movement if its inputs are active at times when a movement is not desired (e.g., in response to sensory stimulation)? Here, we propose a novel hypothesis: movement is triggered not only by an increase in firing rate, but critically by a reliable temporal pattern in the population response. Laminar recordings in the macaque superior colliculus (SC), a midbrain hub of orienting control, and pseudo-population analyses in SC and cortical frontal eye fields (FEF) corroborated this hypothesis. Importantly, we used spatiotemporally patterned microstimulation to causally verify the importance of temporal structure and demonstrate its role in gating movement initiation. We also offer a spiking neuron model with dendritic integration as a putative mechanism to decode this temporal information. These findings offer new insights into the long-standing debate on movement generation and highlight the importance of short-term population history in neuronal communication and behavior.