Feedforward amplification in recurrent networks underlies paradoxical neural coding

Abstract The activity of single neurons encodes behavioral variables, such as sensory stimuli (Hubel & Wiesel 1959) and behavioral choice (Britten et al. 1992; Guo et al. 2014), but their influence on behavior is often mysterious. We estimated the influence of a unit of neural activity on behavioral choice from recordings in anterior lateral motor cortex (ALM) in mice performing a memory-guided movement task (H. K. Inagaki et al. 2018). Choice selectivity grew as it flowed through a sequence of directions in activity space. Early directions carried little selectivity but were predicted to have a large behavioral influence, while late directions carried large selectivity and little behavioral influence. Consequently, estimated behavioral influence was only weakly correlated with choice selectivity; a large proportion of neurons selective for one choice were predicted to influence choice in the opposite direction. These results were consistent with models in which recurrent circuits produce feedforward amplification (Goldman 2009; Ganguli et al. 2008; Murphy & Miller 2009) so that small amplitude signals along early directions are amplified to produce low-dimensional choice selectivity along the late directions, and behavior. Targeted photostimulation experiments (Daie et al. 2021b) revealed that activity along the early directions triggered sequential activity along the later directions and caused predictable behavioral biases. These results demonstrate the existence of an amplifying feedforward dynamical motif in the motor cortex, explain paradoxical responses to perturbation experiments (Chettih & Harvey 2019; Daie et al. 2021b; Russell et al. 2019), and reveal behavioral relevance of small amplitude neural dynamics.