A model for self-organization of sensorimotor function: the spinal monosynaptic loop

Recent spinal cord literature abounds with descriptions of genetic preprogramming and the molecular control of circuit formation. In this paper, we explore to what extent circuit formation based on learning rather than preprogramming could explain the selective formation of the monosynaptic projections between muscle spindle primary afferents and homonymous motoneurons. We adjusted the initially randomized gains in the neural network according to a Hebbian plasticity rule while exercising the model system with spontaneous muscle activity patterns similar to those observed during early fetal development. Normal connectivity patterns developed only when we modeled β motoneurons, which are known to innervate both intrafusal and extrafusal muscle fibers in vertebrate muscles but were not considered in previous literature regarding selective formation of these synapses in animals with paralyzed muscles. It was also helpful to correctly model the greatly reduced contractility of extrafusal muscle fibers during early development. Stronger and more coordinated muscle activity patterns such as observed later during neonatal locomotion impaired projection selectivity. These findings imply a generic functionality of a musculoskeletal system to imprint important aspects of its mechanical dynamics onto a neural network, without specific preprogramming other than setting a critical period for the formation and maturation of this general pattern of connectivity. Such functionality would facilitate the successful evolution of new species with altered musculoskeletal anatomy, and it may help to explain patterns of connectivity and associated reflexes that appear during abnormal development. NEW & NOTEWORTHY A novel model of self-organization of early spinal circuitry based on a biologically realistic plant, sensors, and neuronal plasticity in conjunction with empirical observations of fetal development. Without explicit need for guiding genetic rules, connection matrices emerge that support functional self-organization of the mature pattern of Ia to motoneuron connectivity in the spinal circuitry.