A spiking neural network model for fractional proprioceptive encoding of limb posture and movement in insects

Proprioception is key to all behaviours that involve the control of force, posture or movement. Computationally, many proprioceptive afferents share three features: First, their strictly local encoding of stimulus magnitudes causes range fractionation in sensory arrays. As a result, encoding of large joint angle ranges requires convergence of afferent information onto first-order interneurons. Second, their phasic-tonic response properties lead to fractional encoding of the fundamental sensory magnitude and its derivatives (e.g., joint angle and angular velocity). Third, the distribution of disjunct sensory arrays across the body implies that complex movements involve information from multiple joints or limbs. The present study proposes a multi-layer spiking neural network for distributed computation of whole-body posture and movement. The first part of the study models strictly local, phasic-tonic encoding of joint angle by proprioceptive hair field afferents by use of Adaptive Exponential Integrate-and-Fire neurons. Fractionally encoded afferent information about single-joint posture and movement converges on two types of first-order interneurons, tuned to encode either joint angle or velocity across the entire working range with high accuracy. In velocity-encoding interneurons, spike rate increases linearly with angular velocity. The companion paper exploits this distributed position/velocity encoding in second- and third-order interneurons, using combinations of two or three position/velocity inputs from disjunct arrays. The encoding properties of all interneuron layers are evaluated with experimental data on whole-body kinematics of unrestrained stick insect locomotion, comprising concurrent joint angle time courses of [Formula: see text] leg joints. The hierarchical model allows increasingly complex encoding of posture and movement, from angular velocity of a single joint, to movement cycle phases of an entire limb, to parameters of overall body posture.