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The significance of supraspinal control of reflex actions
Brain Research Bulletin, Vol. 50, Nos. 5/6, p. 325, 1999 Copyright © 1999 Elsevier Science Inc. Printed in the USA. All rights reserved 0361-9230/99/$–see front matter
PII S0361-9230(99)00150-1
The significance of supraspinal control of reflex actions Robert E. Burke* Laboratory of Neural Control, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA [Received 17 May 1999; Accepted 17 May 1999] superimposing the test stimuli on monosynaptic reflexes to assess the excitability of the target motoneurons, they also used the then new technique of intracellular recordings from individual motoneurons to demonstrate the appearance of inhibitory postsynaptic potentials (IPSPs) after the spinalization. In a later paper with Birgitta Holmqvist [3], Lundberg demonstrated differences in the descending suppression of transmission through spinal interneurons in reflex pathways from muscle, joint, and cutaneous afferents to particular groups of motoneurons that depended on the location of supraspinal lesions in the brainstem. This provided evidence for a previously unsuspected level of specificity in the supraspinal control of interneurons in spinal reflex pathways. A large body of subsequent work, largely by Lundberg and his students, provides clear indications that voluntary movements involve the convergence of a wide variety of descending control systems onto spinal interneurons that also receive information from primary afferents and project to motoneurons, i.e., interneurons in spinal reflex pathways. Thus, many of the commands for voluntary actions arrive at the motoneurons after being filtered through spinal interneurons that also compute the state of affairs in the peripheral plant. Much remains to be done to validate this concept but it represents a major paradigm shift in thinking about the control of movement by the brain.
From the perspective of research on brain function, the 20th Century opened with the triumph of the “Neuron Doctrine” that emerged from a happy marriage of neuroanatomy and neurophysiology, respectively epitomized by Ramo´n y Cajal and Sherrington. The Neuron Doctrine envisioned that the nervous system is composed of discrete neurons, communicating with one another through synaptic contacts and organized into specific pathways with specific functions. The idea of functional specificity was evident in observations on spinal reflexes by Sherrington and his students; reflexes exhibited differences depending on the nature of the stimulated sensory systems and the identity of the motoneurons that were activated (summarized in [1]). This work also produced evidence that neurons inhibit as well as excite one another. The concepts and even the terminology developed by these pioneers now thoroughly permeate what has become the unified field now called “neuroscience.” For centuries, philosophers and their scientific descendants have wrestled with the question of how the brain controls movement. With the Neuron Doctrine perspective, Sherrington focused on motoneurons as the “final common path” upon which reflex circuits and voluntary movement commands converged. He recognized that spinal reflex circuits can interact but his evidence provided little information about how they might be utilized in the control of voluntary movements. Accordingly, for decades reflex and voluntary movements have been thought of as separate entities. This view began to change in the 1950s. This change has been incremental because of the complexity of the issue, and the evidence propelling it is contained in what has become a large literature. However, the beginnings are clear. In a short report that appeared in 1958, Rosamond Eccles and Anders Lundberg [2] showed that spinalization of unanesthetized decerebrate cats released powerful excitatory and inhibitory effects produced by electrical stimulation of muscle afferents, particularly those of relatively high threshold, that were virtually undetectable in the decerebrate state. Although most of their data were obtained by
REFERENCES 1. Creed, R. S.; Denny-Brown, D.; Eccles, J. C.; Liddell, E. G. T.; Sherrington, C. S. Reflex activity of the spinal cord. London: Oxford University Press; 1932. 2. Eccles, R. M.; Lundberg, A. Significance of supraspinal control of reflex actions by impulses in muscle afferents. Experientia 14:197–199; 1959. 3. Holmqvist, B.; Lundberg, A. Differential supraspinal control of synaptic actions evoked by volleys in the flexion reflex afferents in alpha motoneurones. Acta Physiol. Scand. 54 (suppl. 186):1–51; 1961.
* Address for correspondence: Dr. Robert E. Burke, Laboratory of Neural Control, Bldg. 49, Rm. 3A50, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892-4455, USA. Fax: 301-402-4836; E-mail: [email protected]
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PII S0361-9230(99)00150-1
The significance of supraspinal control of reflex actions Robert E. Burke* Laboratory of Neural Control, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD, USA [Received 17 May 1999; Accepted 17 May 1999] superimposing the test stimuli on monosynaptic reflexes to assess the excitability of the target motoneurons, they also used the then new technique of intracellular recordings from individual motoneurons to demonstrate the appearance of inhibitory postsynaptic potentials (IPSPs) after the spinalization. In a later paper with Birgitta Holmqvist [3], Lundberg demonstrated differences in the descending suppression of transmission through spinal interneurons in reflex pathways from muscle, joint, and cutaneous afferents to particular groups of motoneurons that depended on the location of supraspinal lesions in the brainstem. This provided evidence for a previously unsuspected level of specificity in the supraspinal control of interneurons in spinal reflex pathways. A large body of subsequent work, largely by Lundberg and his students, provides clear indications that voluntary movements involve the convergence of a wide variety of descending control systems onto spinal interneurons that also receive information from primary afferents and project to motoneurons, i.e., interneurons in spinal reflex pathways. Thus, many of the commands for voluntary actions arrive at the motoneurons after being filtered through spinal interneurons that also compute the state of affairs in the peripheral plant. Much remains to be done to validate this concept but it represents a major paradigm shift in thinking about the control of movement by the brain.
From the perspective of research on brain function, the 20th Century opened with the triumph of the “Neuron Doctrine” that emerged from a happy marriage of neuroanatomy and neurophysiology, respectively epitomized by Ramo´n y Cajal and Sherrington. The Neuron Doctrine envisioned that the nervous system is composed of discrete neurons, communicating with one another through synaptic contacts and organized into specific pathways with specific functions. The idea of functional specificity was evident in observations on spinal reflexes by Sherrington and his students; reflexes exhibited differences depending on the nature of the stimulated sensory systems and the identity of the motoneurons that were activated (summarized in [1]). This work also produced evidence that neurons inhibit as well as excite one another. The concepts and even the terminology developed by these pioneers now thoroughly permeate what has become the unified field now called “neuroscience.” For centuries, philosophers and their scientific descendants have wrestled with the question of how the brain controls movement. With the Neuron Doctrine perspective, Sherrington focused on motoneurons as the “final common path” upon which reflex circuits and voluntary movement commands converged. He recognized that spinal reflex circuits can interact but his evidence provided little information about how they might be utilized in the control of voluntary movements. Accordingly, for decades reflex and voluntary movements have been thought of as separate entities. This view began to change in the 1950s. This change has been incremental because of the complexity of the issue, and the evidence propelling it is contained in what has become a large literature. However, the beginnings are clear. In a short report that appeared in 1958, Rosamond Eccles and Anders Lundberg [2] showed that spinalization of unanesthetized decerebrate cats released powerful excitatory and inhibitory effects produced by electrical stimulation of muscle afferents, particularly those of relatively high threshold, that were virtually undetectable in the decerebrate state. Although most of their data were obtained by
REFERENCES 1. Creed, R. S.; Denny-Brown, D.; Eccles, J. C.; Liddell, E. G. T.; Sherrington, C. S. Reflex activity of the spinal cord. London: Oxford University Press; 1932. 2. Eccles, R. M.; Lundberg, A. Significance of supraspinal control of reflex actions by impulses in muscle afferents. Experientia 14:197–199; 1959. 3. Holmqvist, B.; Lundberg, A. Differential supraspinal control of synaptic actions evoked by volleys in the flexion reflex afferents in alpha motoneurones. Acta Physiol. Scand. 54 (suppl. 186):1–51; 1961.
* Address for correspondence: Dr. Robert E. Burke, Laboratory of Neural Control, Bldg. 49, Rm. 3A50, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892-4455, USA. Fax: 301-402-4836; E-mail: [email protected]
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