Dynamical systems theory of spatial orientation – a tale of two negative feedback systems

Ning Chang¹, Hsuan-Pei Huang^3,1, Chung-Chuan Lo^1,2*

¹Institute of Systems Neuroscience, National Tsing Hua University, Hsinchu, Taiwan
²Brain Research Center, National Tsing Hua University, Hsinchu, Taiwan
³Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan

* Presenter:Chung-Chuan Lo, email:cclo@mx.nthu.edu.tw

Spatial orientation memory plays a crucial role in the navigation of animals as they need to maintain a stable sense of the direction of heading regardless of the availability of external cues or landmarks. Recent studies have revealed stunning details about the neural circuits that encode a fruit fly's head direction and confirmed the ring attractor theory proposed decades ago. The theory suggests that the neural activity that encodes the head direction during navigation results from a stable equilibrium state formed by coupled positive and negative feedback. However, the latest connectomic data of the head-direction system reveal a network pattern that is much more complex than the classical theory requires, and this complexity led to various inconsistent modeling implementations. To address this issue, we construct a detailed neural network model of the fruit fly head-direction system based on the connectomic data and perform systematic tests. Our result suggests that the head-direction system is potentially modulated by two, but not one, negative feedback circuits. Each circuit exhibits different functional features, and a combination of the two provides more stability and flexibility than the classical theory can provide. Furthermore, the resulting model exhibits improved performance over the existing models. Our work provides insights into how brains maintain spatial orientation and its underlying mechanisms.

Keywords: neural network, spatial orientation, brain, dynamical systems, attractor