Causal evidence of a line attractor encoding an affective state

Line attractors are emergent population dynamics hypothesized to encode continuous variables such as head direction and internal states1-4. In mammals, direct evidence of neural implementation of a line attractor has been hindered by the challenge of targeting perturbations to specific neurons within contributing ensembles2,3. Linear dynamical systems modeling has revealed that neurons in the hypothalamus exhibit approximate line attractor dynamics in male mice during aggressive encounters5. We have previously hypothesized that these dynamics may encode the variable intensity of an aggressive internal motive state. Here, we report that these neurons also showed line attractor dynamics in head-fixed mice observing aggression6. We identified and perturbed line attractor-contributing neurons using 2-photon calcium imaging and holographic optogenetic perturbations. On-manifold perturbations yielded integration and persistent activity that drove the system along the line attractor, while transient off-manifold perturbations were followed by rapid relaxation back into the attractor. Furthermore, single-cell stimulation and imaging revealed selective functional connectivity among attractor-contributing neurons. Intriguingly, individual differences among mice in line attractor stability were correlated with the degree of functional connectivity among attractor neurons. Mechanistic RNN modelling indicated that dense subnetwork connectivity and slow neurotransmission7 best recapitulate our empirical findings. Our work bridges circuit and manifold levels3, providing causal evidence of continuous attractor dynamics encoding an affective internal state in the mammalian hypothalamus.