Internal feedback in the cortical perception-action loop enables fast and accurate behavior

Jing Shuang (Lisa) Lia, Anish A. Sarmaa, Terrence J. Sejnowskic, and John C. Doyle, Internal feedback in the cortical perception-action loop enables fast and accurate behavior, PNAS, September 22, 2023 120 (39) e2300445120 https://doi.org/10.1073/pnas.2300445120, asXiv: https://arxiv.org/abs/2211.05922

Significance

Internal feedback projections—signals flowing from motor areas or late sensory processing regions back to early sensory processing regions such as primary visual and auditory areas—are ubiquitous in the sensorimotor nervous system and are as or more numerous than feedforward projections. However, the function of internal feedback is poorly understood, particularly in the context of task performance. We leverage control theory and simple models to demonstrate that internal feedback facilitates good task performance when there are communication limitations such as internal time delays and speed–accuracy trade-offs, which motivate compensatory feedback signals to counter self-generated and predictable movements. Control theory explains why motor-related signals are found throughout the sensory cortex and why the motor cortex is dominated by internal dynamics.

Abstract

Animals move smoothly and reliably in unpredictable environments. Models of sensorimotor control, drawing on control theory, have assumed that sensory information from the environment leads to actions, which then act back on the environment, creating a single, unidirectional perception–action loop. However, the sensorimotor loop contains internal delays in sensory and motor pathways, which can lead to unstable control. We show here that these delays can be compensated by internal feedback signals that flow backward, from motor toward sensory areas. This internal feedback is ubiquitous in neural sensorimotor systems, and we show how internal feedback compensates internal delays. This is accomplished by filtering out self-generated and other predictable changes so that unpredicted, actionable information can be rapidly transmitted toward action by the fastest components, effectively compressing the sensory input to more efficiently use feedforward pathways: Tracts of fast, giant neurons necessarily convey less accurate signals than tracts with many smaller neurons, but they are crucial for fast and accurate behavior. We use a mathematically tractable control model to show that internal feedback has an indispensable role in achieving state estimation, localization of function (how different parts of the cortex control different parts of the body), and attention, all of which are crucial for effective sensorimotor control. This control model can explain anatomical, physiological, and behavioral observations, including motor signals in the visual cortex, heterogeneous kinetics of sensory receptors, and the presence of giant cells in the cortex of humans as well as internal feedback patterns and unexplained heterogeneity in neural systems.