Integrative and Comparative Biology Advance Access originally published online on July 12, 2007
Integrative and Comparative Biology 2007 47(4):447-450; doi:10.1093/icb/icm036
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Recent developments in neurobiology: introduction to the symposium to honor Professor Douglas G. Stuart
Department of Biology and Marine Biology and Center for Marine Science, University of North Carolina Wilmington, Wilmington, NC 29409, USA
Correspondence: 1E-mail: satterlier{at}uncw.edu
This year's symposiuim "Recent Developments in Neurobiology" honors Dr Douglas G. Stuart, Regents Professor Emeritus of Physiology at the University of Arizona for his long-time contribution to research in the field of neural control of movement, and for his service to the development of neuroscience research in the State of Arizona and beyond (Fig. 1). In addition to his long list of research accomplishments (summarized subsequently), Professor Stuart served as the Head of Physiology at the University of Arizona, and as Associate Dean of Research at the UA College of Medicine. He was a founding member of the College of Medicine (1967) and was awarded Regents Professor status in 1990. Professor Stuart has over 120 experimental papers in scientific journals, and over 80 chapters, reviews and symposium papers. In the recent years, he provided overviews on motor control and on the history of movement neuroscience.
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| Topical annotated bibliography of Professor Stuart's research Neurophysiology: hypothalamus (1958–1966) |
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Stuart DG, Maxwell DS, Hayward JN, Fairchild MD, Adey WR, Porter RW. 1964. Unit activity in the hypothalamus. In: Escoba E, editor. Feedback mechanisms controlling neural activity. Mexico City: Sociedad Medicana des Ciencias Fisiologicas. p. 226–47.
This review summarizes Professor Stuart's work in 12 refereed articles, which advanced our understanding of single-cell activity in the hypothalamus using techniques that included (1) extracellular unitary and DC-potential recording in anesthetized and unanesthetized preparations, (2) thermal stimulation with self-designed Peltier thermodes, and (3) measurement of temperature gradients between arterial blood and the brain.
| Neurophysiology: segmental motor system (1961–Present) |
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(Note: the term "segmental motor system" refers to (1) properties and central actions of posture-related and movement-related sensory feedback, (2) interneuron and motoneuron discharge properties, motoneuron recruitment, and associations between motoneuron, muscle fiber, and motor-unit properties for graded development of muscle force, and (3) segmental-pattern generation for the elaboration of intrinsic/rhythmic and learned/skillful movements).
Stuart DG, Withey T, Wetzel MC, Goslow GE Jr. 1973. Time constraints for interlimb coordination in the cat during unrestrained locomotion. In: Stein RB, Pearson KG, Smith RS, Redford JB, editors. Control of posture and locomotion. New York: Plenum Press. p. 537–60.
This refereed article is an example of "outside-in" research and thinking, showing how measurement of footfall patterns during walking, trotting and galloping can be used to predict efficacy of spinal reflex activity during low-speed to high-speed quadrupedal cat locomotion.
Jankowska E, Lundberg A, Roberts WJ, Stuart DG. 1974. A long propriospinal system with direct effect on motoneurones and on interneurones in the cat lumbosacral cord. Exp Brain Res 21:169–94.
An example of the use of advanced spinal cord electrophysiological techniques to unravel the details of spinal cord circuitry, which Professor Stuart learned from Anders Lundberg and the still-premier exponent of these techniques, Elzbieta Jankowksa.
Watt DGD, Stauffer EK, Taylor A, Reinking RM, Stuart DG. 1976. Analysis of muscle receptor connections by spike-triggered averaging: 1. Spindle primary and tendon organ afferents. J Neurophysiol 39:1375–92.
A seminal study that used a cross-correlation technique to show how minute monosynaptic and disynaptic EPSPs and IPSPs, attributable to the input of single sensory axons, could be measured in the cat spinal cord.
Windhorst U, Hamm TM, Stuart DG. 1989. On the function of muscle and reflex partitioning. Behav Brain Sci 12:629–81.
A review in an open-peer-reviewed journal, which summarized work (including over 15 of Professor Stuart's refereed articles) on associations between motoneurons, muscle fibers, and motor-unit properties.
Stauffer EK, Stuart DG, McDonagh, JC, Hornby TG, Reinking RM. 2005. After hyperpolarization-firing rate relation of turtle spinal neurons. J Comp Physiol A 191:135–46.
A seminal report, which used data from four other refereed articles by Profesor Stuart's group to compare the detailed, intracellularly recorded properties of motoneurons and ventral interneurons in unanesthetized slices of turtle spinal cord. This work challenged doctrinaire thought on spinal interneuronal properties.
| Technical contributions (1959–1995) |
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Hayward JN, Fairchild MD, Stuart DG, Deemer JA. 1964. A stereotaxic platform for micro-electrode studies in chronic animals. Electroencephalogr Clin Neurophysiol 16:522–4.
This article provides the first-ever extracellularly recorded firing pattern of a hypothalamic cell in an unanesthetized intact mammal (cat). The technique subsequently became widely used on various mammalian species including nonhuman primates.
Reinking RM, Stuart DG. 1974. A servo-regulated electromagnetic device for muscle stretch and vibration. Am J Phys Med 53:1–28.
This article explained how to build a sophisticated device to deliver precise stretches and vibration to anesthetized and unanesthetized animals, including humans. This technique, too, became widely used.
Gorman RB, Reinking RM, Stuart DG. 1995. Characterization of the biophysical properties of spinal neurons: A solution using a graphical programming language. SciTech Journal 5:22–5.
Professor Stuart's laboratory pioneered the use of a graphical programming language with Macintosh computers, as described in this and four other articles. Several laboratories now use this approach.
| Reviews on movement neuroscience (1963–present) |
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Wetzel MC, Stuart DG. 1976. Ensemble characteristics of cat locomotion and its neural control. Prog Neurobiol 7:1–98.
An important review that introduced many Western workers to the post-Bernstein Russian group's seminal work on locomotor control; it became widely used in predoctoral and postdoctoral training programs.
Hasan Z, Stuart DG. 1988. Animal solutions to problems of movement control: the role of proprioceptors. Annu Rev Neurosci 11:199–223.
This review proposed several still-untested functions for proprioceptors on the basis of an "outside-in" approach to movement control, which was applied to work undertaken largely on the crab, cat, and human.
Enoka RM, Stuart DG. 1992. Neurobiology of muscle fatigue. J Appl Physiol 72:1631–48.
A widely quoted article on neural and neuromuscular fatigue mechanisms, which proposed four themes, and guided research for the next decade in several laboratories.
Nordstrom MA, Gorman RB, Laouris Y, Spielmann JM, Stuart DG. 2007. Does motoneuron adaptation contribute to muscle fatigue? Muscle Nerve 35:135–58.
A provocative article that narrows the gap between the firing-rate properties of motoneurons, as studied electrophysiologically ("bottom-up") in animal preparations, and the "top-down" study of the firing patterns of human motor units as fatigue ensues.
| Editing movement neuroscience volumes (1976–present) |
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Herman RM, Grillner S, Stein PSG, Stuart DG, editors. 1976. Neural control of locomotion. New York: Plenum.
Grillner S, Stein PSG, Stuart DG, Forssberg H, Herman RM, editors. 1987. Neurobiology of vertebrate locomotion. London: MacMillan.
Stein PSG, Grillner S, Selverston A, Stuart DG, editors. 1997. Neurons, networks, and motor behavior. Boston: MIT Press.
These three widely read postsymposium volumes are the quintessence of integrative and comparative approaches to the study of locomotion in the world's leading laboratories. The symposia themselves not only promoted international collaborative efforts but were vehicles for advancing the careers of junior scientists including predoctoral and postdoctoral trainees.
| History of movement neuroscience (1998–present) |
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Stuart DG, McDonagh JC. 1998. Reflections on a Bernsteinian approach to systems neuroscience: the controlled treadmill locomotion of high decerebrate cats. In: Latash ML, editor. Progress in motor control: Bernstein's traditions in movement studies. Champaign, IL: Human Kinetics. p 21–49.
This article shows how ideas on the neural control of movement, which were proposed in 1947 by Nicolai Bernstein on the basis of over 20 years of his research on largely human movement, were tested experimentally on high-decerebrate cats in the 1960s and early 1970s by a group of relatively young Russian neuroscientists and thereby considerably advanced our understanding of the neural control of locomotion.
Stuart DG. 2005. Integration of posture and movement: contributions of Sherrington, Hess, and Bernstein. Hum Mov Sci 24:621–43.
A review that compares and contrasts the scientific careers of three neuroscientists who were born in the 19th century and who contributed substantially to 20th century thought on the neural control of movement. One, Sherrington, emphasized an "inside-out" approach whereas the other two preferred an "outside-in" strategy. The article also addresses the need for interdisciplinarity, interphyletic awareness, and transnationalism in the study of movement neuroscience.
Stuart DG, Pierce PA. 2006. The academic lineage of Sir John Carew Eccles (1903–1997). Prog Neurobiol 78: 136–55.
This article reviews the academic lineage of Eccles: who trained him, whom he then trained and with whom he collaborated, and the subsequent impact of his trainees and collaborators on movement neuroscience. This is one of 10 articles on Eccles in a special issue of Progress in Neurobiology that was coedited by Professor Stuart.
| Selected bibliography from Professor Stuart's experimental work |
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1960–1969
Stuart DG, Kawamura Y, Hemingway A. 1961. Activation and suppression of shivering during septal and hypothalamic stimulation. Exp Neurol 4:485–506.
Hayward JN, Fairchild MD, Stuart DG, Deemer JA. 1964. A stereotaxic platform for micro-electrode studies in chronic animals. Electroencephalogr Clin Neurophysiol 16:522–24.
Stuart DG, Ott K, Ishikawa K, Eldred E. 1965. Muscle receptor responses to sinusoidal stretch. Exp Neurol 13:82–95.
Stuart DG, Ott K, Ishikawa K, Eldred E. 1966. The rhythm of shivering III. Central contributions. Am J Phys Med 45:91–104.
Ishikawa K, Ott K, Porter RW, Stuart DG. 1966. Low frequency depression of H waves in normal and spinal man. Exp Neurol 15:140–56.
1970–1979
Goslow GE, Reinking RM, Stuart DG. 1973. The cat step cycle: hind limb joint angles and muscle lengths during unrestrained locomotion. J Morphol 141:1–41.
Jankowska E, Lundberg A, Roberts WJ, Stuart DG. 1974. A long propriospinal system with direct effect on motoneurones and on interneurones in the cat lumbosacral cord. Exp Brain Res 21:169–94.
Wetzel MC, Stuart DG. 1976. Ensemble characteristics of cat locomotion and its neural control. Prog Neurobiol 7:1–98.
Watt DGD, Stauffer EK, Taylor A, Reinking RM, Stuart DG. 1976. Analysis of muscle receptor connections by spike-triggered averaging: 1. Spindle primary and tendon organ afferents. J Neurophysiol 39:1375–92.
Burke D, Skuse NS, Stuart DG. 1979. The regularity of muscle spindle discharge in man. J Physiol (Lond) 291:277–90.
1980–1989
Hasan Z, Enoka RM, Stuart DG. 1985. The interface between biomechanics and neurophysiology in the study of movement: some recent approaches. Exerc Sport Sci Rev 13:169–234.
Hamm TM, Sasaki S, Stuart DG, Windhorst U, Yuan C-S. 1987. The measurement of single motor-axon recurrent inhibitory postsynaptic potentials in the cat. J Physiol (Lond) 388:631–51.
Hasan Z, Stuart DG. 1988. Animal solutions to problems of movement control: the role of proprioceptors. Ann Rev Neurosci 11:199–223.
Nemeth PM, Norris GJ, Lowry OH, Gordon DA, Enoka RM, Stuart DG. 1988. Activation of single muscle fibers in individual motor units revealed by 2-deoxyglucose-6-phosphate. J Neurosci 8:3959–66.
Windhorst U, Hamm TM, Stuart DG. 1989. On the function of muscle and reflex partitioning. Behav Brain Sci 12:629–81.
1990–1999
Bevan L, Laouris Y, Reinking RM, Stuart DG. 1992. The effect of the stimulation pattern on the fatigue of single motor units in adult cats. J Physiol (Lond) 449:85–108.
Enoka RM, Stuart DG. 1992. Neurobiology of muscle fatigue. J Appl Physiol 72:1631–48.
Spielmann JM, Laouris Y, Nordstrom MA, Robinson GA, Reinking RM, Stuart DG. 1993. Adaptation of cat motoneurons to sustained and intermittent extracellular activation. J Physiol (Lond) 464:75–120.
McDonagh JC, Gorman RB, Gilliam EE, Hornby TG, Reinking RM, Stuart DG. 1998. Properties of spinal motoneurons and interneurons in the adult turtle: provisional classification by cluster analysis. J Comp Neurol 400:544–70.
Stuart DG. 1999. The segmental motor system: advances, issues, and possibilities. Prog Brain Res 123:3–28.
2000–Present
Stuart DG. 2002. Reflections on spinal reflexes. Adv Exp Med Biol 508: 249–57.
Hornby TG, McDonagh JC, Reinking RM, Stuart DG. 2002. Effects of excitatory modulation on the intrinsic properties of turtle motoneurons. J Neurophysiol 88: 86–97.
Gorman RB, McDonagh JC, Hornby TG, Reinking RM, Stuart DG. 2005. Measurement and nature of firing rate adaptation in turtle spinal neurons. J Comp Physiol A 191:583–603.
Nordstrom MA, Gorman RB, Laouris Y, Spielmann JM, Stuart DG. 2007. Does motoneuron adaptation contribute to muscle fatigue? Muscle Nerve 35:135–58.
Stauffer EK, McDonagh JC, Hornby TG, Reinking RM, Stuart DG. 2007. Historical reflections on the afterhyperpolarization-firing rate relation of vertebrate spinal neurons. J Comp Physiol A 193:145–58.
| Acknowledgments |
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We are grateful for the support of the National Science Foundation (IOS 0424467) in bringing together the following list of speakers for the Recent Developments in Neurobiology symposium at the 2007 annual meeting of the Society for Integrative and Comparative Biology (Phoenix, AZ): K. Pearson and D. McVea (University of Alberta), R. Levine (University of Arizona), C. Duch (Arizona State University), R. Enoka and B. Barry (University of Colorado), A. Prochazka (University of Alberta), S. Yakovenko (University of Montreal), T. Pirtle (Abilene Christian University), and of course, Professor D. Stuart (University of Arizona).
| Footnotes |
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From the symposium "Recent Developments in Neurobiology—A Tribute to Professor Douglas G. Stuart" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2007, at Phoenix, Arizona.
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