Near-additive temporal dynamics of sub-threshold population responses in macaque V1

Abstract

To study stimulus-evoked dynamics of neuronal signals, a powerful method is to quantify deviations of the measured response dynamics from predictions of a linear system. A linear system can be completely characterized by its impulse response function; deviations from linearity can inform us about the type of nonlinearities that the response dynamics contain. Non-linearities in neuronal responses typically have ecological causes or functional benefits, and are crucial for understanding how our internal representations relate to sensory inputs. Here, we conducted linear system analysis on trial-by-trial data of voltage sensitive dye (VSD) measurements from behaving macaque V1. We used a set of 12 large and high-contrast visual stimuli that varied in duration of a single pulse, and in inter-stimulus interval between two pulses (20 to 640 ms). VSD signals represent membrane potential dynamics pooled from a local neuronal population, which makes it unique and complementary to spike-based signals measured using other methods (e.g. single- or multi-units, LFP, BOLD in fMRI). Unlike other spike-based signals, we found that population membrane potentials measured using VSD are surprisingly close to being additive in time. This near-additivity has not been previously examined, possibly due to challenges to separate stimulus-evoked neuronal signals from other signal sources in VSD time courses. Our new pre-processing algorithm allows us to robustly separate these two components. We further quantified the small but significant deviations from additivity at short stimulus durations, and present a delayed normalization model that accounts for the near-additive temporal summation in population membrane dynamics. The delayed normalization model can also exhibit previously observed contrast-dependent gain change in population membrane potential dynamics. Furthermore, the model provides a platform for testing ways to connect between signals of population membrane potential and other spike-based neuronal population measurements.