Central control of information transmission through the intraspinal arborizations of sensory fibers examined 100 years after Ramón y Cajal

Abstract

About 100 years ago, Santiago Ramón y Cajal reported that sensory fibers entering the spinal cord have ascending and descending branches, and that each of them sends collaterals to the gray matter where they have profuse ramifications. To him this was a fundamental discovery and proposed that the intraspinal branches of the sensory fibers were "centripetal conductors by which sensory excitation is propagated to the various neurons in the gray matter". In addition, he assumed that "conduction of excitation within the intraspinal arborizations of the afferent fibers would be proportional to the diameters of the conductors", and that excitation would preferentially flow through the coarsest branches. The invariability of some elementary reflexes such as the knee jerk would be the result of a long history of plastic adaptations and natural selection of the safest neuronal organizations. There is now evidence suggesting that in the adult cat, the intraspinal branches of sensory fibers are not hard wired routes that diverge excitation to spinal neurons in an invariable manner, but rather dynamic pathways where excitation flow can be centrally addressed to reach specific neuronal targets. This central control of information flow is achieved by means of specific sets of GABAergic interneurons that produce primary afferent depolarization (PAD) via axo-axonic synapses and reduce transmitter release (presynaptic inhibition). The PAD produced by single, or by small groups of GABAergic interneurons in group I muscle afferents, can remain confined to some sets of intraspinal arborizations of the afferent fibers and not spread to nearby collaterals. In muscle spindle afferents this local character of PAD allows cutaneous and descending inputs to differentially inhibit the PAD in segmental and ascending collaterals of individual fibers, which may be an effective way to decouple the information flow arising from common sensory inputs. This feature appears to play an important role in the selection of information flow in muscle spindles that occurs at the onset of voluntary contractions in humans.