Spinal reflexes, mechanisms and concepts: From Eccles to Lundberg and beyond
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).
Section snippets
Development of conceptual views during the last century on the role of the spinal cord in “reflex” and “voluntary” motor activities
I wish to begin with a citation from Sir Michael Foster (1836–1907) in his renowned textbook of physiology (Foster, 1879). There he wrote that “… reflex action may be said to be, par excellence, the function of the spinal cord” (quoted on p. 98 in Liddell, 1960), but added that “the cord contains a number of more or less complicated mechanisms capable of producing, as reflex results, coordinated movement altogether similar to those which are called forth by the will. Now it must be an economy
Development during the last century of experimental tools and techniques for the investigation of spinal cord circuitry
Sherrington's important contributions on spinal reflexes were to a large extent the result of careful observation, using vision and palpation. The experimental techniques were relatively simple, using natural stimulation or electrical stimulation of nerves while recording reflex responses as changes in muscle length or force. The optical isometric myograph was improved during his collaboration with Eccles (Eccles and Sherrington, 1929) and EMG recording of individual motor units was used in
Five examples of the analysis of neurons and circuits in the spinal cord—from connectivity to function
During his 13+ years in Canberra, Eccles had no less than 74 visiting scientists from 20 different countries (Curtis and Andersen, 2001, Stuart and Pierce, 2006). Looking through the publications related to spinal reflexes from this period, five different pathways stand out as exemplary in a discussion of Eccles’ contribution to the field: (1) recurrent inhibition; (2) the reflexes from muscles spindles; (3) Golgi tendon organs; (4) the flexor reflex; and (5) presynaptic inhibition. As already
Summary and concluding thoughts on future possibilities
I have exemplified above how the analysis of a number of spinal networks has developed throughout almost a century. Sherrington's important contributions on spinal reflexes were to a large extent the result of careful observation, using vision and palpation. The experimental techniques were relatively simple, using natural stimulation or electrical stimulation of nerves, while recording the response as changes in muscle length or force. EMG recording of individual motor units was used in
Acknowledgements
Preparation of this article was supported, in part, by the Danish Medical Research Council and the Ludvig and Sara Elsass Foundation. I would also like to thank Lillian Grondahl and Lisbeth Causse for their technical assistance. During the course of writing this chapter I was concerned about my lack of direct knowledge on Eccles’ “golden years” in Canberra. I had several telephone discussions with my mentor, Anders Lundberg, both on the scientific life in Canberra during that period, and on the
References (172)
Inhibitory circuits in the thalamus and hippocampus—an appraisal after 40 years
Prog. Neurobiol.
(2006)- et al.
Cognitive neural prosthetics
Trends Cogn. Sci.
(2004) - et al.
Selecting the signals for a brain-machine interface
Curr. Opin. Neurobiol.
(2004) Beginning at the end: repetitive firing properties in the final common pathway
Prog. Neurobiol.
(2006)John Eccles’ pioneering role in understanding central synaptic transmission
Prog. Neurobiol.
(2006)- et al.
Electrophysiology of sensory and sensorimotor processing in mice under general anesthesia
Brain Res. Brain Res. Protoc.
(2003) - et al.
Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling
Cell
(1997) - et al.
In humans Ib facilitation depends on locomotion while suppression of Ib inhibition requires loading
Brain Res.
(2006) - et al.
Activity of interneurons mediating reciprocal 1a inhibition during locomotion
Brain Res.
(1975) - et al.
Descending control of reflex pathways in the production of voluntary isolated movements in man
Brain Res.
(1983)
The formation of sensorimotor circuits
Curr. Opin. Neurobiol.
Development of circuits that generate simple rhythmic behaviors in vertebrates
Curr. Opin. Neurobiol.
Cerebellar circuitry as a neuronal machine
Prog. Neurobiol.
Interneuronal relay in spinal pathways from proprioceptors
Prog. Neurobiol.
In vivo recordings of bulbospinal excitation in adult mouse forelimb motoneurons
J. Neurophysiol.
John C. Eccles (1903–1997)
Trends Neurosci.
Presynaptic inhibitory action of cerebral cortex on the spinal cord
Nature
Integration in spinal neuronal systems
Analysis of the fast afferent impulses from thigh muscles
J. Physiol. (Lond.)
Homeobox gene Nkx2.2 and specification of neuronal identity by graded sonic hedgehog signalling
Nature
Experimental investigations on the afferent fibres of muscle nerves
Proc. R. Soc. Lond. B
The nature of the monosynaptic excitatory and inhibitory processes in the spinal cord
Proc. R. Soc. Lond. B
Cell depletion due to diphtheria toxin fragment A after Cre-mediated recombination
Mol. Cell Biol.
The intrinsic factors in the act of progression in the mammal
Proc. R. Soc. Lond. B.
On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression and a theory of the evolution of function in the nervous system
J. Physiol. (Lond.)
Inhibition of human motoneurons, probably of Renshaw origin, elicited by an orthodromic motor discharge
J. Physiol.
Stable ensemble performance with single-neuron variability during reaching movements in primates
J. Neurosci.
Primary afferent depolarization evoked from the sensorimotor cortex
Acta Physiol. Scand.
The distribution of monosynaptic exciation from the pyramidal tract and from primary spindle afferents to motoneurons of the baboon's hand and forearm
J. Physiol. (Lond.)
Proprioceptive input resets central locomotor rhythm in the spinal cat
Exp. Brain Res.
Reflex Activity of the Spinal Cord
Spinal mechanisms in man contribution to reciprocal inhibition during voluntary dorsiflexion of the foot
J. Physiol. (Lond.)
Reciprocal Ia inhibition between ankle flexors and extensors in man
J. Physiol.
Disynaptic reciprocal inhibition of ankle extensors in spastic patients
Brain
Appearance of reciprocal facilitation of ankle extensors from ankle flexors in patients with stroke or spinal cord injury
Brain
Reciprocal inhibition and corticospinal transmission in the arm and leg in patients with autosomal dominant pure spastic paraparesis (ADPSP)
Brain
Two kinds of recurrent inhibition of cat spinal alpha-motoneurones as differentiated pharmacologically
J. Physiol. (Lond.)
John Carew Eccles 1903–1997
Hist. Rec. Aust. Sci.
Pharmacology and nerve endings
Proc. R. Soc. Med.
Reciprocal inhibition between the muscles of the human forearm
J. Physiol. (Lond.)
Short-latency autogenic inhibition in patients with Parkinsonian rigidity
Ann. Neurol.
Regulation of bipedal stance: dependency on “load” receptors
Exp. Brain Res.
Contribution of sensory feedback to ongoing ankle extensor activity during the stance phase of walking
Can. J. Physiol. Pharmacol.
The Neurophysiological Basis of Mind
The Physiology of Nerve Cells
The Physiology of Synapses
Sherrington, His Life and Thought
The rhythmic discharge of motoneurones
Proc. R. Soc. Lond. B
Improved bearing for the torsion myograph
J. Physiol. (Lond.)
Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones
J. Physiol. (Lond.)
Cited by (129)
Phrenic-to-intercostal reflex activity in response to high frequency spinal cord stimulation (HF-SCS)
2022, Respiratory Physiology and NeurobiologyTemporal modulation of H-reflex in young and older people: Acute effects during Achilles tendon vibration while standing
2022, Experimental GerontologyCentral pattern generator and human locomotion in the context of referent control of motor actions
2021, Clinical NeurophysiologyDevelopment of motor circuits: From neuronal stem cells and neuronal diversity to motor circuit assembly
2021, Current Topics in Developmental BiologySense of verticality and Neurointegrated Orthopaedic Manual Therapy in pediatric physiotherapy
2020, Motricite Cerebrale