Scaling of sensorimotor control in terrestrial mammals

Abstract

Sensorimotor control is greatly affected by two factors-the time it takes for an animal to sense and respond to stimuli (responsiveness), and the ability of an animal to distinguish between sensory stimuli and generate graded muscle forces (resolution). Here, we demonstrate that anatomical limitations force a necessary trade-off between responsiveness and resolution with increases in animal size. To determine whether responsiveness is prioritized over resolution, or resolution over responsiveness, we studied how size influences the physiological mechanisms underlying sensorimotor control. Using both new electrophysiological experiments and existing data, we determined the maximum axonal conduction velocity (CV) in animals ranging in size from shrews to elephants. Over the 100-fold increase in leg length, CV was nearly constant, increasing proportionally with mass to the 0.04 power. As a consequence, larger animals are burdened with relatively long physiological delays, which may have broad implications for their behaviour, ecology and evolution, including constraining agility and requiring prediction to help control movements.

Scaling of sensorimotor delays in terrestrial mammals

“…This hypothesized scaling is not inevitable, because distinct physiological processes underlie the component delays. Consequently, their contributions to total delay may scale differently than what we previously observed for nerve conduction delay [13], offsetting or adding to its effect. We focused on two characteristic movement durations: stride duration, because it is the maximum time available for the nervous system to make adjustments for the next step [20]; and stance duration, because it is the maximum time available to respond to a disturbance within the same step.…”

“…To conduct information along a nerve fibre, an electrical current flows quickly down the fibre in areas insulated by myelin, slowing only periodically at gaps in the myelin to regenerate itself by triggering action potentials [30]. We previously found that the conduction velocity of nerve fibres is relatively constant regardless of animal size [13], making nerve conduction delay almost entirely dependent on conduction distance. In the case of the hindlimb stretch reflex, increases in animal size lead to longer legs, which increases conduction distance and thereby lengthens nerve conduction delay.…”

“…An animal's size may have a substantial effect on its sensorimotor delays. For example, we previously found that one sensorimotor delay-nerve fibre conduction velocity-remains nearly constant across the full size range of terrestrial mammals, indicating that the time required for a nerve fibre to transmit information increases in direct proportion to the length of the fibre [13]. Larger animals have longer peripheral nerve fibres due to their longer limbs and thus are faced with longer nerve conduction delays.…”

“…But movement durations do not increase as sharply as nerve conduction delay, changing only with the square root of limb length [14][15][16]. Consequently, the ratio between nerve conduction delay and movement duration is about 10 times higher in an elephant than in a shrew [13]. The scaling of other sensorimotor delays with animal size has not previously been studied, but if they were all size-independent, our observed scaling of nerve conduction delay would result in total delays that increase strongly with animal size and outpace increases in movement duration.…”

Swing-Leg Trajectory of Running Guinea Fowl Suggests Task-Level Priority of Force Regulation Rather than Disturbance Rejection

“…Neuromuscular delays (synaptic, conduction, electromechanical and force development) can represent a large fraction of the step cycle in animals [10], [31], and therefore limit the rate of feedback in both stance and swing. These neural delays are likely to be especially problematic at the swing-stance transition, when small changes in landing conditions have large influence on stance leg loading and body dynamics [9]–[11].…”