Dynamic Excitatory and Inhibitory Gain Modulation Can Produce Flexible, Robust and Optimal Decision-making

Behavioural and neurophysiological studies in primates have increasingly shown the involvement of urgency signals during the temporal integration of sensory evidence in perceptual decision-making. Neuronal correlates of such signals have been found in the parietal cortex, and in separate studies, demonstrated attention-induced gain modulation of both excitatory and inhibitory neurons. Although previous computational models of decision-making have incorporated gain modulation, their abstract forms do not permit an understanding of the contribution of inhibitory gain modulation. Thus, the effects of co-modulating both excitatory and inhibitory neuronal gains on decision-making dynamics and behavioural performance remain unclear. In this work, we incorporate time-dependent co-modulation of the gains of both excitatory and inhibitory neurons into our previous biologically based decision circuit model. We base our computational study in the context of two classic motion-discrimination tasks performed in animals. Our model shows that by simultaneously increasing the gains of both excitatory and inhibitory neurons, a variety of the observed dynamic neuronal firing activities can be replicated. In particular, the model can exhibit winner-take-all decision-making behaviour with higher firing rates and within a significantly more robust model parameter range. It also exhibits short-tailed reaction time distributions even when operating near a dynamical bifurcation point. The model further shows that neuronal gain modulation can compensate for weaker recurrent excitation in a decision neural circuit, and support decision formation and storage. Higher neuronal gain is also suggested in the more cognitively demanding reaction time than in the fixed delay version of the task. Using the exact temporal delays from the animal experiments, fast recruitment of gain co-modulation is shown to maximize reward rate, with a timescale that is surprisingly near the experimentally fitted value. Our work provides insights into the simultaneous and rapid modulation of excitatory and inhibitory neuronal gains, which enables flexible, robust, and optimal decision-making.Author Summary: Perceptual decision-making involves not only simple transformation of sensory information to a motor decision, but can also be modulated by high-level cognition. For example, the latter may include strategic allocation of limited attentional resources over time in a decision task to improve performance. At the neurophysiological level, there is evidence supporting attention-induced neuronal gain modulation of both excitatory and inhibitory cortical neurons. In the context of perceptual discrimination tasks performed by animals, we make use of a biologically inspired computational model of decision-making to understand the computational capabilities of such co-modulation of neuronal gains. We find that dynamic co-modulation of both excitatory and inhibitory neurons is important for flexible, and cognitively demanding decision-making while also enhancing robustness in the decision circuit's functions. Our model captures the neuronal activity and behavioural data in the animal experiments remarkably well. Decision performance in a reaction time task can be optimized, maximizing the rate of receiving reward by using fast gain recruitment. Our experimentally fitted timescale is near the optimal one, suggesting that the animals performed almost optimally. By providing both computational simulations and theoretical analyses, our computational model sheds light into the multiple functions of rapid co-modulation of neuronal gains during decision-making.