Spinal reflexes, mechanisms and concepts: From Eccles to Lundberg and beyond

Abstract

This review focuses on investigations by Sir John Eccles and co-workers in Canberra, AUS in the 1950s, in which they used intracellular recordings to unravel the organization of neuronal networks in the cat spinal cord. Five classical spinal reflexes are emphasized: recurrent inhibition of motoneurons via motor axon collaterals and Renshaw cells, pathways from muscle spindles and Golgi tendon organs, presynaptic inhibition, and the flexor reflex. To set the scene for these major achievements I first provide a brief account of the understanding of the spinal cord in “reflex” and “voluntary” motor activities from the beginning of the 20th century. Next, subsequent work is reviewed on the convergence on spinal interneurons from segmental sensory afferents and descending motor pathways, much of which was performed and inspired by Anders Lundberg's group in Gothenburg, SWE. This work was the keystone for new hypotheses on the role of spinal circuits in normal motor control. Such hypotheses were later tested under more natural conditions; either by recording directly from interneurons in reduced animal preparations or by use of indirect non-invasive techniques in humans performing normal movements. Some of this latter work is also reviewed. These developments would not have been possible without the preceding work on spinal reflexes by Eccles and Lundberg. Finally, there is discussion of how Eccles’ work on spinal reflexes remains central (1) as new techniques are introduced on direct recording from interneurons in behaving animals; (2) in experiments on plastic neuronal changes in relation to motor learning and neurorehabilitation; (3) in experiments on transgenic animals uncovering aspects of human pathophysiology; and (4) in evaluating the function of genetically identified classes of neurons in studies on the development of the spinal cord.

Introduction

Three of the chapters in this series of articles describing the lasting importance of the work by Sir John Carew Eccles (1903–1997) are authored by his co-workers from Eccles’ “golden period” in Canberra, AUS from 1952–1966 (Andersen, 2006, Ito, 2006, Willis, 2006). This is not the case for my chapter, although I am of proud of being a member of Eccles’ “scientific lineage”. I had the privilege to meet him at several scientific meetings; mainly after his move to Contra, CHE in 1976. In June 1986, Eccles made a short visit to Copenhagen, with his wife Helena, where he gave a lecture to the Medical Faculty, University of Copenhagen under the auspices of the newly formed Danish Society for Neuroscience. We enjoyed having both of them for lunch at the Faculty Club, and at my home for a private dinner that night. Eccles was relaxed, and he enjoyed entertaining the young scientists who were present in my laboratory not long after I had moved to Copenhagen from Anders Lundberg's group in Gothenburg.

Most of the articles from Eccles’ time in Canberra are so well-known, and reviewed so many times, that the description of these results here will be kept rather short and concise. Rather, more emphasis is focused here on what Eccles’ contributions meant for subsequent steps in the scientific development of the field of “spinal cord and motor control”.

In order to give an idea of the background for Eccles’ contribution to and impact on the field, I begin by describing the development during the last century of conceptual views on central motor control and relevant methodological advancements. The major part of this review then covers the analysis of five specific spinal neuronal pathways, where Eccles’ contributions during his Canberra period have been of particular importance. In Section 4, the development of ideas from the time before Eccles entered the scene will be described, and then followed up to the present. I end with some comments on future potential advancements and possibilities in the field (Section 5).