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Integration of posture and movement: Contributions of Sherrington, Hess, and Bernstein


Douglas G. Stuart
*
Department of Physiology, University of Arizona College of Medicine, Tucson, AZ 85724-5051, United States

Abstract Neural mechanisms that integrate posture with movement are widespread throughout the central nervous system (CNS), and they are recruited in patterns that are both task- and context-dependent. Scientists from several countries who were born in the 19th century provided essential groundwork for these modern-day concepts. Here, the focus is on three of this group with each selected for a somewhat dierent reason. Charles Sherrington (18571952) had innumerable contributions that were certainly needed in the subsequent study of posture and movement: inhibition as an active coordinative mechanism, the functional anatomy of spinal cord-muscle connectivity, and helping set the stage for modern work on the sensorimotor cortex and the corticospinal tract. Sadly, however, by not championing the work of his trainee and collaborator, Thomas Graham Brown (18821965), he delayed progress on two key motor control mechanisms: central programming and pattern generation. Walter Hess (18811973), a self-taught experimentalist, is now best known for his work on CNS coordination of autonomic (visceral) and emotional behavior. His contributions to posture and movement, however, were also far-reaching: the coordination of eye movements and integration of goal-directed and framework (anticipatory set) motor behavior. Nikolai Bernstein (18961966), the quintessence of an interdisciplinary, self-taught movement neuroscientist, made far-reaching contributions that were barely recognized by Western workers prior to the 1960s. Today, he is widely praised for showing that the CNSs hierarchy of control mechanisms for posture and movement is organized hand-in-hand with distributed and parallel processing, with all three subject to evolutionary pressures. He also made important observations, like those of several previous workers, on the goal focus of voluntary movements. The contributions of Sherrington, Hess, and Bernstein are enduring. They prompt thought on the philosophical axioms that appear to have driven their

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research, and the continual need for emphasis on interdisciplinary, comparative, and transnational approaches to advance movement neuroscience. 2005 Elsevier B.V. All rights reserved.
PsycINFO classication: 2330 Keywords: Posture; Movement; History of movement neuroscience

1. Introduction It is now well accepted that neural mechanisms involved in the integration of posture with movement in humans, other vertebrates, and invertebrates are widespread throughout the central nervous system (CNS), and they are recruited in patterns that are both task- and context-dependent (Mori, Stuart, & Wiesendanger, 2004). Two possibilities are on the forefront of current mammalian research on this topic. One proposes two separate, albeit parallel and coordinated, control systems, one for postural adjustment and the other for movement (see, e.g., Fig. 1 in Massion, Alexandrov, & Frolov, 2004). The other possibility is that a single coordinated control system exists, achieving simultaneously the movement and its obligatory anticipatory and reactive postural adjustments (see, e.g., Fig. 19.9 in Latash, 1998a). The purpose of this article is not to debate the relative merits of these two models. Rather, it is to reect on some of the ideas and results of earlier workers, which have bearing on the models current evaluation. This article focuses on three such workers who were born in the 19th century (Fig. 1): Charles Sherrington, Walter Hess, and Nikolai Bernstein. Hess and Bernstein were selected for their holistic, functionally oriented approaches to posture and movement, which still guide research in this eld. Sherrington was chosen for a somewhat dierent reason. Despite his many essential and indeed Herculean contributions, his reex focus and inside-out approach (see below) were not conducive to the study of movement, in general, and the integration of posture and movement, in particular. The article concludes with some thoughts on the philosophical axioms that appear to have driven the research eorts of these three stellar neuroscientists, and the continual need for emphasis on interdisciplinary, comparative, and transnational approaches to advance movement neuroscience. 2. Charles Sherrington (18571953) Few neuroscientists achieved in their lifetime the visibility, inuence, and accolades bestowed upon Sherrington for his humanistic nature, mentoring success, scientic accomplishments, and broad intellectual abilities and interests (Eccles & Gibson, 1979; Granit, 1966; Liddell, 1952; Stuart, Pierce, Callister, Brichta, & McDonagh, 2001; Swazey, 1969). Sherrington began medical training at St. Thomass Hospital Medical School (London, Great Britain) in 1877, but he switched to the University of Cambridge in 1879, where he graduated in 1883 with a degree in natural science (including botany, zoology, and human anatomy and physiology), followed by a medical degree in 1885. While at Cambridge, he received thorough neuroscience mentoring from two prominent and experienced physiologists, John Langley (18521925) and Walter Gaskell (18471914), the latter emphasizing

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Fig. 1. The three subjects of this article. Top-left: Charles S. Sherrington (18571953) at about 45 years of age. (From Granit, 1966, Plate 8) Top-right: Walter Hess (18811973) when 55 years of age. (From Worden et al., 1992, p. 490, Fig. 27.7. Reprinted with permission from Springer-Verlag.) Bottom: Nikolai Bernstein (18961966) at the age of 55 years. (From Latash, 1998, p. viii. Reprinted with permission from M.L. Latash.)

comparative issues. Sherringtons postdoctoral training included 12 months (1884) with Eduard Puger (18291900) at the University of Bonn, a year (18841885) with Friedrich Goltz (18341902) at the University of Strasbourg, 2 months (1886) with Rudolph Virchow (18211902) at the University of Berlin and a year (18861887) with Robert Koch (18431910) at the same institution. While these European experiences were largely in neurohistology and pathology, Sherrington also strengthened his hand in the all-round study of the CNS (pgs. 914 in Swazey, 1969). Subsequently, Sherrington made substantial contributions to overall neuroscience and movement neuroscience in his own laboratory, with the majority of his post-training work undertaken at the Universities of Cambridge (18871895), Liverpool (18951912) and Oxford (19131936).

Fizkultura I Sport 1998

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For neuroscience, in general, Sherringtons writings on overall aspects of CNS function (rather than his own extensive personal research ndings) helped emphasize the validity and signicance of the synapse in CNS circuitry and function. His experimental prowess is possibly best revealed and remembered in work showing that inhibition is an active process in the CNS and a co-partner of excitation in brain function. (For details, see Stuart et al., 2001, which chapter has specic reference to 52 of Sherringtons most signicant articles.) For the integration of posture and movement, Sherringtons major contributions were to delineate the functional organization of the sensorimotor cortex and the corticospinal tract (Fig. 2), and advance understanding of the segmental convergence of descending command signals and sensory feedback signals (Stuart et al., 2001). The former work (Grunbaum & Sherrington, 1901, 1903; Leyton & Sherrington, 1917) has been rightly lauded in modern accounts of voluntary movement (e.g., pgs. 59 in Porter & Lemon, 1993). In retrospect, work undertaken in the same era on the extrapyramidal pathways, a term coined in an 1898 article on epilepsy by Johann Prus (18581926),1 was of equal signicance. Vogt and Vogt (19061907, 19191920) pioneered this work. It is rarely cited, however, in modern accounts of posture and movement. Sherringtons segmental (spinal cord and peripheral neuromuscular) contributions were his most substantial: the functional anatomy of spinal cord-muscle connectivity, about which there had been much prior inaccuracy, uncertainty and confusion, and the reex play of one muscles (and/or one dermatomes) sensory input upon another muscles activity and/or movement. The latter work, which required much experimental and theoretical skill, yielded many concepts that are still in the forefront of thought on spinal cord function: central excitatory vs. inhibitory state, discharge zone and subliminal fringe, spatiotemporal summation, disynaptic reex pathways, reex afterdischarge, integrative reex action, and the nal common path. He also provided de novo ndings on motor units and wrote extensively on modulation of movement by sensory feedback. Clearly, Sherrington fully deserved his 1932 Nobel Prize! He provided few, if any, direct contributions to ideas on the integration of posture and movement, however: i.e., as based on his own research. Admittedly, as . . . the great integrator of knowledge of the central nervous system . . . (pg. ix in Eccles & Gibson, 1979), he is widely quoted on what he wrote about posture and movement. For example, Sherrington is recognized, along in particular with Rudolph Magnus (18731927; see Magnus, 1924), for the view espoused in his classic 1906 text (pgs. 336344 in 1947 edition) that the bodys orientation with respect to gravity was determined by a group of reexes that sets the body segments collective orientation and stabilizes the orientation against external disturbances (pg. 13 in Massion et al., 2004). Subsequently, however, he said little about this topic in terms of overall body posture during movement. In his 1932 summing up chapter on his major area of research, spinal reex coordination, he did comment briey on the aphorism posture accompanies movement like its shadow (pgs. 147148 in Creed, Denny-Brown, Eccles, Liddell, &

1 It is generally thought in English-speaking countries that the British neurologist, S.A. Kinnear Wilson (1848 1937) coined the term extrapyramidal paths (pg. 394 in Wilson, 1924). This came 26 years after Prus (1898), however.

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Fig. 2. A Sherrington nding on the morphology of the corticospinal tract. It shows the longitudinal distribution of corticospinal axons after a unilateral lesion in the arm area of the motor cortex of a chimpanzee. The cross sections are at the upper (up.py.dec.) and mid (mid.py.dec.) levels of the pyramidal decussation in the lower brainstem and at C2 (2c), C8 (8c), T6 (6th) and T12 (12th) levels of the spinal cord. This gure demonstrated that the corticospinal innervation is uncrossed at the upper level of the pyramidal decussation, largely crossed and mostly limited to the cervical level of the spinal cord, and near-exclusively crossed and much thinned out at the thoracic level. No degeneration was observed at the lumbar level of the spinal cord (for further details on the signicance of this nding and its electrophysiological. counterpart, see pgs. 510 in Porter and Lemon, 1993). (From Leyton and Sherrington, 1917, p. 184, Fig. 20. Reprinted with permission from Blackwell Publishing.)

Sherrington, 1932). The overall thrust of this chapter, however, precluded further discussion of this point. Some believe that Sherrington moved away from the neural control of body posture because he wished to encourage Magnus to be on the forefront in this line of work (pg. 95 in Granit, 1966). This viewpoint is dicult to document. There is clear-cut evidence,

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however, that Magnus began his postural work on experimental animals while working in Sherringtons laboratory in 1908 (pg. 218 in Fulton, 1955; also pg. 62 in Granit, 1966). At the spinal level of motor control, Sherrington contributed important examples of how sensory input from the proprioceptors could enhance the quality of rhythmic movements. He chose to deemphasize, however, the existence and nature of the essentially spinal origin of locomotor pattern generation. Like his well-respected Belgian peer, Maurice Philippson (18771938), he chose to emphasize the role of interlocking spinal reexes in the elaboration of locomotion (see, e.g., plate X in Philippson, 1905), while also conceding the possibility of a central control of locomotor movements. For example, Sherrington sometimes emphasized the signicance of pioneering 19111922 work on the spinal origin of locomotor rhythmicity by his former trainee and subsequent collaborator, Thomas Graham Brown (18821965; see Brown, 1916). Sherringtons ambivalence about Graham Browns work was seemingly lifelong, however. As emphasized previously (pg. 334 in Stuart et al., 2001) he did include important comments on Graham Browns work on spinal pattern generation in his 1931 Hughlings Jackson Lecture (pg. 25) and the inuential Creed et al. (1932) text (pg. 146), and he did mention Graham Brown in his Nobel lecture (see endnotes 2830). Also, in the foreword to the 1947 edition of Sherrington (1906) he concedes at the outset that the role of spinal reex action in motor control should not be overstated. Later in this foreword, however, there appears . . . A train of motor acts results therefore from a train of external situations. This one caveat about Sherringtons contributions is emphasized because it is now known that the spinal (rather than sensory input) origin of locomotor pattern generation is an essential component of the overall neural control of movement.2 with equivalent circuitry extending to the forebrain and coming into play in the integration of posture and a wide variety of movements; from the most rudimentary to the most skilled and learning dependent (Grillner & Wallen, 2004). Sherrington wrote much on why he favored a single-cell/single-reex approach to the study of CNS control mechanisms. In modern-day parlance, Sherrington used an inside-out approach to movement neuroscience, in which the starting point is the property of single cells within the CNS and peripheral neuromuscular system and then its extension into the behavior of CNS microcircuits, single reexes, groups of reexes, followed by theorizing on the function of CNS regions like the motor cortex and spinal cord, and nally overall motor behavior. The majority of Sherringtons British peers, including his co-Nobel Laureate, Edgar Adrian (18891977), also favored this approach. It was a key, indeed essential, precedent to the iterative late 1930-early 1950 renement and use of the intracel-

2 Graham Browns prescient work on spinal rhythm generation languished in near-total obscurity until Lundbergs widely read 1969 report. Graham Brown appears to have remained a good friend and active colleague of Sherrington despite their dierent views on the control of locomotion (see pgs. 333334 in Stuart et al., 2001). It remains puzzling why Graham Brown published so little on movement neuroscience after WWI (see Adrian, 1966). In 1941, however, he demonstrated an intriguing lm on the treadmill locomotion of the decerebrate cat at an unpublished 1941 meeting of the Physiological Society in London, UK. This lm had no captions and its availability remained relatively unknown until Lundberg and Phillips (1973) wrote a short account about it. (This lm is now available upon request to The Physiological Society.) Interestingly, Graham Brown, at the age of 80 years, wrote to Anders Lundberg and oered to sail his yacht across the North Sea from Scotland to Goteborg, Sweden, to provide Lundberg with appropriate captions for his 1941 lm. (His letter, dated February 17, 1962, is available upon request from AL or DGS.) Sadly, however, Graham Browns subsequent ill-health prevented this adventuresome and demanding trip, which would have been much appreciated by Lundberg and the movement neuroscience eld, as a whole!

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lular microelectrode to study single neurons within the CNS and the peripheral neuromuscular system (Bretag, 1983; Hoyle, 1983). Some would argue that the inside-out approach is, to at least some extent, an example of elementalism (the analysis of an entity by consideration of its separate elements), this being a central theme in British empiricist philosophy, from John Locke (16321704) to Bertrand Russell (18721970). In the 1920s1940s, important conceptual advances in movement neuroscience were being made in Switzerland, Germany, and Russia, using an outside-in approach. For this, the starting point is consideration of the problems posed by the moving mechanical system, which are solved by the CNS and its circuitry and pathways, with subsequent theorizing extending down nally the level of single neurons (see, e.g., Hasan & Stuart, 1988; Loeb, 1987). It seems likely that the initial usage of an outside-in approach was inuenced by holism (the idea that an entity has properties greater than the sum of its parts), as championed in continental Europe by the prominent German philosopher, Georg Hegel (17701831). Despite his wide reading and broad cultural interests (see Eccles & Gibson, 1979), Sherringon appears to have been unaware of, or perhaps impervious to an outside-in, holistic approach to the study of movement neuroscience. This is again revealed in his foreword to the 1947 edition of Sherrington (1906). Admittedly, Sherrington was 91 years of age in 1947, and he had essentially stopped his neuroscience research in 1935. Nonetheless, taking all factors into account, great as Sherringtons contributions were, his legacy in movement neuroscience would have been more far-reaching if he had actively promulgated Graham Browns results and been more interdisciplinary and transnational in his overall thought about posture and movement. 3. Walter Hess (18811973) Hess was a remarkably well-rounded, self-taught systems-oriented researcher who . . . made pioneering contributions in the eld of hemodynamics, physiological optics, oculomotor diagnostics, regulation of circulation, respiration and temperature, and nally on the somatomotor, visceral and emotional functions of the diencephalon (pg. vii in Akert, 1981; see also Akert, 1999; Hess, 1942, 1943, 1949, 1965; Hess, Burgi, & Bucher, 1946; Jung, 1981, 1992; Wiesendanger, 1997). In English-speaking countries, Hess was and remains best known for the work for which he received a 1949 Nobel Prize: the functional organization of the diencephalon as the primary coordinator of the activities of visceral organs (Gloor, 1954). Here, however, the focus is on his contributions to movement neuroscience which were also farreaching. Hess was an essentially a self-taught physiologist and neuroscientist, with a quantitative bent (Hess, 1963). He studied medicine in Lausanne and Bern in Switzerland, and Berlin and Kiel in Germany. Subsequently, he graduated with an MD degree in 1905 from the University of Zurich. While a medical student, he performed his rst research, a theoretical analysis of blood vessels. With his MD degree in hand, Hess rst decided to become an ophthalmologist. While in such training (19061908), he developed a new device to measure quantitatively oculomotor coordination in diplopic patients. After four years in private practice as an ophthalmologist (19081912), he returned to the University of Zurich as an assistant in the Physiology Institute. In 1917, at the age of 36 years, he became Chair of Physiology, a position he held until 1951. In all, Hess published original work and

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thoughts for 70 years (19031973), thereby slightly exceeding the 69-year span of Sherringtons publications (18841953)! Even in the early 1920s, Hess recognized that neural circuitry in the brainstem coordinates a variety of autonomic functions. To advance this idea, he pioneered the study of CNS function in intact, freely moving mammalian preparations, in which he chronically implanted tripolar stimulating electrodes to activate brainstem axons and neurons (see Fig. 27.8 in Jung, 1992). The responses he noted included not only vegetative changes in blood pressure, heart rate, and respiratory activity, but also behavioral aspects of emotion (e.g., increased and deceased alertness, aggressiveness, anger, ight, sleep). Less widely known is that throughout the above work, Hess became increasingly interested in the principles of motor organization. He observed that electrical stimulation in certain motor structures of the brainstem and basal ganglia could elicit directed movements that were accompanied with appropriate postural changes. This prompted him to model goal-oriented movements and their accompanying postural adjustments. Contrary to the then prevailing inuence of Sherrington (1906) and Magnus (1924), Hess held the view that without anticipation of postural adaptations (a component of his framework ereismatic system), goal-directed movements (his teleokinetic system) were doomed to failure; the eects of reexes were too slow to compensate for self-induced disturbances produced by voluntary movements. In order to transmit this notion to his students, Hess used a very eective human model of volitional goal-oriented movements, which is shown in Fig. 3. Fig. 3 shows that the goal of voluntary movement (teleokinetic motility) in Hesss model was represented by a student who was to jump from the shoulders of another student to a dened target on the oor. The supporting student represented the framework (postural support) of the movement. The demonstration showed that the intentional movement was only correctly performed if a third student was behind the back of the postural student providing anticipatory set (bereitschaft). Possibly, both postural framework and anticipatory set can be considered to comprise Hesss ereismatic motility. In evaluating the signicance of the model in Fig. 3, which is central to modern ideas on the integration of posture and movement, it is important to emphasize its sharp distinction from the above-described inside-out approach of Sherringon and his colleagues. For example, the distinguished and imaginative German neurologist, Richard Jung (1911 1986), commented in an inspirational memoir that while he was most impressed with the scientic rigor of the pre-World War II Oxford and Cambridge neuroscientists, he was pleased with his own personal change from . . . fact-oriented (i.e., unitary cellular) British physiology to the systems-oriented physiology of W. R. Hess . . . (who) considered single facts (i.e., single-cell and isolated reex results) only in their context with functional systems or in their signicance for the organism (i.e., the outside-in approach, as dened above). In his later years, Hess strongly advocated the need to integrate neurophysiology with psychology, as had been the practice in the late 19th century (see below). For example, his last book (Hess, 1962) and article (Hess & Fischer, 1973) are still relevant to psychological aspects of movement neuroscience. Hesss modern-day relevance for ideas on the integration of posture and movement are emphasized by his concluding remarks in the chapter on intentional movements in Hess (1962), which were summarized in a shortened version by Wiesendanger (1997, pg. 131):

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Fig. 3. Hesss concept of the need for integration of goal-directed movement (Hesss teleokinetic motility) and its framework anticipatory and supportive postural support (ereismatic motility). Three medical students represent the actions and simultaneous reactions involved in a voluntary movement. The goal directed (teleokinetic) leaper (1) makes use of a postural frameworker (2) who also requires a supporter (3) for postural anticipatory set. Both (2) and (3) likely comprise Hesss ereismatic motility. The leap (goal) is achieved appropriately (ac) when (1), (2) and (3) are highly coordinated. The leap is unsuccessful (df) when there is a lack of coordination between the three simultaneous needs of the performance. Jung redrew these sketches from an unpublished motion picture made by Hess in 1943 for use in his medical school teaching. Similar sketches appeared in Hess (1965). Preceding still pictures from the motion picture were provided in Hess (1943). (From Field et al., 1960; Jung and Hassler, 1960, p. 904, Fig. 13. Reprinted with permission from The American Physiological Society.)

. . . (1) An intentional action is induced by a conscious drive and set. (2) The perception of the object in a goal-oriented movement3 and its memorized content contribute to the drive and motivation for prehension. (3) A manifold of innervation patterns characterizes the probing of a limb. (4) Goal achievement reinforces the used innervation pattern, thus

3 Action is possibly a better term than movement because active perception can occur without overt movement.

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steadily improving the performance by learning. (5) Disturbances of central coordination are compensated adaptively. Clearly, modern-day movement neuroscientists owe much to Hess! 4. Nikolai Bernstein (18961966) In sharp contrast to Sherringon and Hess, Bernsteins life and career had some tragic elements, particularly in his later years (Feigenberg & Latash, 1996). Sadly, it was only after his death that he received the well-deserved, international accolades for movement neuroscience contributions that have made him pre-eminent in this eld. These accolades actually began the year of his death (Gelfand, Gurnkel, Fomin, & Tsetlin, 1966) and have thereafter increased progressively (see, e.g., Bernstein, 2003; Bongaardt, 2001; Feigenberg, 2004; Latash, 1998b, 2005; Latash & Turvey, 1996; Whiting, 1984). It is likely that he would receive even more renown if his 1947 book, which was his most detailed exposition on movement neuroscience, was translated into English. Bernstein received a Stalin Prize Award for this book in 1948. Wastefully, however, he was dismissed from his Moscow position at the USSR Academy of Sciences in 1950 for his scientic viewpoints, particularly those that argued against some of Pavlovs views. Bernsteins reinstatement was initiated after Stalins death in 1953. This was a relatively slow process, however, and it was due at least in part to his ill health. He was again reasonably active and certainly locally inuential throughout the early 1960s until his death in 1966 (for further details, see Feigenberg, 2004; Feigenberg & Latash, 1996). Bernstein was born into a stellar academic family, with parents and close relatives particularly strong in the ne arts, humanities, medicine, and mathematics (Feigenberg & Latash, 1996). After completing his MD degree in 1919 at the University of Moscow in the USSR and a 3-year stint in the Soviet army, he was given the opportunity in 1922 to develop a motor control laboratory at the Moscow Central Institute of Labor. In the 1920s, he was also aliated with the Moscow Institute of Psychology. It is well to remember that the Soviet regime was reasonably supportive of, albeit somewhat ambivalent, about the scientic intelligentsia and their research up to 1929 (see pgs. 72122 in Vucinich, 1984). In this usually supportive, but always highly charged, environment Bernstein initially ourished as an innovative investigator. . . . At dierent times, he created laboratories of motor control at the Labor Protection Institute, All-Union Institute of Sports, Institute of Musical Science, All-Union Institute of Experimental Medicine, Institute of Neurology (Academy of Medical Sciences), and the Moscow Institute of Prosthetic Appliances (pg. 2 in Gurnkel & Cordo, 1998). Bernstein seems unique in the extent of his self-taught, eclectic approach to movement neuroscience. His remarkable insight into movement found one of its fullest expressions in his essays on the origins and construction of movements (Essays 3 and 4, respectively, in Latash & Turvey, 1996), which should be essential initial reading for trainees in movement neuroscience. Bernsteins research career spanned four decades (19221967), with his 1967 book published a few months after his death. His contributions to movement neuroscience extended for a much longer period, however, given the eventual 1991 (in Russian) and 1996 (in English; Latash & Turvey, 1996) publication of a treatise on dexterity. This work was actually in galley proof form in 1950 when Bernstein was subject to particularly harsh treatment from the Soviet power structure (Feigenberg & Latash, 1996). Similarly, Bernstein (1992) is a recapitulation of his career-long contributions to prosthetics. Also, a book

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he wrote for publication in 1936 has only recently been published (Bernstein, 2003)4 in Russian, and its translation into English is not yet forthcoming. Today, Bernstein is perhaps most widely known for his work on self-controlling biological systems. His work in this area, which must surely have been assisted by several German precedents (Wiesendanger, 1997, 1998), paralleled that of Arturo Rosenblueth (19001970) and Norbert Wiener (18941964; see Wiener, 1948). Among movement neuroscientists, Bernstein is also given great credit for combining quantitative cyclographic kinesiology, in which area he made several technical improvements, with imaginative ideas on the neural control of movement. The latter were based on evolutionary, fundamental neuroscience, and applied (clinical) neuroscience concepts and ndings. Indeed, he achieved a synthesis of movement neuroscience and biomechanics that has rarely been equaled subsequently. Bernstein employed this synthesis in a remarkable theoretical description of simple to complex movements in a wide variety of animal species (his Essay 3 in Latash & Turvey, 1996). Most of his work, however, involved quantitative experimental and theoretical studies on the intact and brain-damaged human and in the development of prosthetic devices for the latter. For the present purposes, it is sucient to focus on three Bernstein concepts: movement as a structure, his denition of motor coordination, and his hierarchical theory of motor coordination. The rst of these concepts was developed, in part, in Bernstein (1929) and progressively rened up to Bernstein (1940/1967), in which article it is stated that . . . movements are not chains of details but structures which are dierentiated into details; they are structurally whole, simultaneously exhibiting a high degree of dierentiation of elements and diering in the particular forms of the relations between elements (pg. 69 in Bernstein, 1967). The second Bernstein concept of relevance here, which was elaborated in part in Bernstein (1935), is his denition of motor coordination as . . . overcoming excessive degrees of freedom of our movement organs, that is, turning the movement organs into controllable systems . . . the degrees of freedom can be both kinematic and dynamic (Essay 2, pg. 41 in Latash & Turvey, 1996). The third concept also began to develop in Bernstein (1935/1967): . . . there exist in the central nervous system exact formulae of movement (Bewegungsformeln) or their engrams, and that these formulae or engrams contain in some form of brain trace the whole process of the movement in its entire course of time (pg. 37 in Bernstein, 1967; i.e., the English translation of Bernstein, 1935). Later, in Bernstein (1947), he provided a far fuller and complete (V.S. Gurnkel, personal communication) account of this concept with the idea that . . . The higher sections of the nervous system determine the chains of motor activity, the lower level ties movements to spatial coordinates. Still lower levels solve the motor problem as such by organizing the necessary interaction of elements (muscle, joints, limbs) and by operatively controlling their work (quotation on pg. 756 of Shik, Severin, & Orlovsky, 1966).
4

This book was written far earlier and entitled Current research in the physiology of nervous processes a critical review of the main problems of brain function (in Russian). The book contained criticisms of the work of Ivan Pavlov (18491936). It was in galley proof form and ready for printing in 1936 by the State Publishing House of Biological and Medical Literature. Bernstein insisted that it be withdrawn, however, because Pavlovs death in 1936 denied the latter, whom Bernstein respected greatly, the opportunity to counter Bernsteins points (personal communication from Anatol Feldman; also pg. 249 in Feigenberg & Latash, 1996).

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Gurnkel and Cordo (1998) have summarized Bernsteins ideas on the functional anatomy of the above concept, which accommodated distributed and parallel processing throughout the CNS, with all three subject to evolutionary pressures. Today, it is well known that the testing of this third concept led to major advances in current understanding of the neural control of locomotion. This began with work undertaken in Moscow in the 1960s,5 which then spread to an international eort (summarized in Fig. 4) that con tinues to this day (Grillner & Wallen, 2004; Orlovsky, Deliagina, & Grillner, 1999; Stuart & McDonagh, 1998). Fig. 4 brings out the salient features of the role of Bernsteins third concept in subsequent delineation of the tripartite interactions between descending command signals, sensory feedback, and spinal pattern generators in an overall control program for locomotion. Over 30 years ago, a relatively unread albeit important article by Gurnkel and Shik (1973) proposed that the same Bernstein concept might mean that gravity-containing postures are organized and controlled similarly. Surprisingly, this provocative concept has commanded little subsequent attention. If Bernsteins above three concepts are considered as one, however, then it is worth testing the possibility that posture (in all its forms) and movement are one and the same type of Bernsteinian structure. This idea has yet to be tested, however. It has been said with authority that . . . Bernstein was highly familiar with the physiological and neurological literature, which is clearly evident in his unpublished (1936) book . . . (pg. 2 in Gurnkel & Cordo, 1998). In this now published book, Bernstein (2003)4 discussed Western work from Flourens to Lashley (V.S. Gurnkel, personal communication). Nonetheless, a potential blot on Bernsteins otherwise impeccable scholarly escutcheon is that he did not always acknowledge the Western precedents to some of his ideas. For example, the above-mentioned Bewegungsformeln had precedents in the work of Liepman (1900), Brown (1916), Lashley (1917), Head (1920), and Wachholder (1928), and presumably several others. It seems likely, however, that Bernsteins wealth of personally generated movement data and analysis provided the primary basis for his Bewegungsformeln proposition (Gurnkel & Cordo, 1998). It is also surprising that Lashleys work appears not to have inuenced Bernstein, even though they came to many similar conclusions while using dierent methods. For example, Lashleys (1929) observations on brain-injured rats and Bernsteins on the kinemetics of human movements led to the same conclusion, invariant goal achievement by variable means: i.e., the same motor task accomplished using dierent muscle and joints, an idea that dates back to at least Kohnstamm (1901) and Foerster (1902). In other words, Lashleys principle of motor equivalence (Lashley, 1933) and Bernsteins principle of equal simplicity (Fig. 3 in Bernstein, 1935/1967) are virtually one and the same phenomenon. Note also the near-identical

5 The seminal 1960s locomotion work of Y. Arshavsky, M.L. Shik, G.N. Orlovsky, and their collaborators owed much to the ideas of Bernstein, even though they had virtually no direct contact with him (personal communication from G.N. Orlovsky). These gifted interdisciplinary movement neuroscientists were also stimulated by the enlightened leadership and quantitative contributions of two mathematician/physicists, Israel Gelfand (1913; see Berkinblit, Vasilev, & Shik, 1974) and Mikhail Tsetlin (19241966; see Editors Obituary, 1966), Institute of Problems of Information Transmission (formerly called the Institute of Biological Physics), USSR Academy of Sciences, Moscow, USSR.

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Fig. 4. An important nding that emerged from testing a key Bernstein concept. This diagram summarizes current understanding of the control of vertebrate locomotion, and it owes much to the testing of ideas presented by Bernstein (1947) (for review of these developments, see Bernstein, 1947; Orlovsky et al., 1999; Stein, 1999; Stuart and McDonagh, 1998). (A) Tripartite interactions between descending command signals, spinal cord pattern generators (CPGs), and sensory feedback. (The quoted material that follows is from pg. 5 in Grillner and Wallen, 2004.) The locomotor CPGs in the spinal cord are turned on from the brainstem via reticulospinal pathways. Disinhibition of the basal ganglias output to the mesencephalic (mesopontine, MLR) and diencephalic (DLR) locomotor centers results in increased activity in reticulospinal neurons (RS), which, in turn, cooperate with sensory feedback, activate the central spinal network, which, in turn, produces the locomotor pattern . . . Experimentally, locomotion can also be elicited pharmacologically by administration of excitatory amino acid agonists combined with sensory input. (B) Gait transitions during locomotion. With increased activation of the locomotor centers, the speed of locomotion increases. In quadrupeds, this also leads to shifts in interlimb coordination, from walk to trot and, nally, to gallop. (C) An asymmetric activation of SR neurons gives rise to an asymmetric output of the left (L) and right (R) sides. This will result in a turning movement from one side to the other. Note that the thrust of the Grillner and Wallen (2004) article was that it is misleading to draw a distinction between innate and learned movements across vertebrates, a viewpoint that extends on some thoughts previously espoused by Bernstein (see his Essay 3 in Latash and Turvey, 1996). (From Mori et al., 2004; Grillner and Wallen, 2004, p. 5, Fig. 2. Reprinted with permission from Elsevier.)

principle of exible coupling of Albrecht Bethe (18721954: for review of this point, see Wiesendanger, 1997, 1998). This issue is even more puzzling because in his 1935 article, Bernstein took Lashley to task for overstating the case for CNS equipotentiality in the neural basis for memory (pgs. 3435 in Bernstein, 1967) while in the very same article he failed to acknowledge the existence of Lashleys 1933 report! In defense of Bernstein, he was certainly a victim of his times in the repressive Soviet regime that developed after 1929, when Stalin came into full power. This Soviet era (192153) was noted for its widespread (Vucinich, 1984), albeit with isolated exceptions (see pgs. 337380 in Bailes, 1978), political intrusion into the conduct of science. As a result, by the 1930s and subsequently, Bernstein presumably had few, if any, contacts with Western scientists. Also, his work was mostly published in Russian journals and by Russian publishing houses (Gurnkel & Cordo, 1998), information that was rarely read in the West. This is presumably one of the reasons that his Western peers ignored his work until

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the mid 1960s. It remains puzzling, however, that the same fate did not befall the Russian writings of Pavlov, which certainly created much interest in the West well before the awarding of his 1904 Nobel Prize. Another reason is that at least in English-speaking countries up to the late 1960s, the inside-out approach to CNS control mechanisms for posture and movement was far more favored than the outside-in strategy of Bernstein and Hess. 5. Summary thoughts It should not be construed from the above that Sherringtons inside-out approach to his own experimental work was any less valuable than the outside-in approach of Hess and Bernstein. To the contrary, both are absolutely essential to advance movement neuroscience, as is the case in all the biological sciences. By the early 20th century, however, it would have been extremely dicult for any single investigator or any single laboratory to give equal emphasis to the two approaches. This problem grew progressively after WWII, particularly with the advent of the techniques of molecular biology in the midto-late 1970s. To oset this problem, much emphasis has been placed in recent years on the need for movement neuroscientists to (1) display an appreciation of and contribute to interdisciplinary research (interdisciplinarity), (2) have knowledge of comparative advances (interphyletic awareness), and (3) adopt transnational approaches to advance movement neuroscience. The current state-of-the-play in these three areas is commented upon below with due consideration to their historical precedents. 5.1. Interdisciplinarity In the eld of movement science, it certainly appears that even in the 19th century . . . many concepts, originating in one discipline, soon found their way into other disciplines (pg. 103 in Wiesendanger, 1997). It would seem that such cross-fertilization declined in the rst half of the 20th century, and then progressively increased up to the present day. If Bernsteins interdisciplinary prowess had been understood in the West in the 1920 1950s, this process may well have been further accelerated. For example, the interdisciplinary composition of his own and his immediate successors laboratories in the Academy of Science of the USSR became much more visible to Western workers with the 1955 publication of the Russian journal, Biozika, and its English translation, Biophysics. In the West, theoretical and applied advances in electrical and mechanical engineering and the 1950s step jump in computer science possibilities matched these developments after WWII. These developments, together with a wide variety of international symposia on movement neuroscience, had much to do with the post 1980s emergence in the West of interdisciplinary pre- and postdoctoral training programs that provide substantial interactions between the life and physical sciences. The power of this approach is exemplied in Fig. 5, which shows how modern engineering control theory now contributes to a particularly dicult problem in movement neuroscience: making sense of the wealth of intricate spinal circuitry involved in the elaboration of movement. Prochazka (1993) used this gure as an example of both interphyletic awareness (dened below) and how nite state (conditional), adaptive (self organizing) predictive control, neural networks, and fuzzy logic are now being used to understand spinal circuitry and advance prosthetics research (see also Prochazka, 1996).

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Fig. 5. An example of both the interface between neuroscience and engineering, and interphyletic awareness. The gure demonstrates the proposed use of nite state control in the elaboration of a stepping movement. Shown are schematics of a stick insect, locust, lobster, cat, active leg prosthesis, and a human with a functional electrical stimulation device. In each case, pairs of sensory variables are indicated when used in a conditional way to initiate the swing phase of the step. That is, if displacement exceeds threshold and force has declined below threshold, exion is then initiated. Approximate positions of identied sensors (natural and articial) are shown. (From Prochazka, 1993, p. 8, Fig. 1. Reprinted with permission from IEEE).

The above developments have precedents in the eorts of many scientists born in the 19th century (including Hess and Bernstein to much greater extent than Sherrington). Also, the interface between movement neuroscience and psychology had a promising

IEEE 1993

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start in the 19th century due to the eorts of the two founders of modern-day psychology: Wilhelm Wundt (18321920) and William James (18421910). They both were originally trained as clinicians and then became active in physiology and its interface with psychology. For movement neuroscience, the contributions of subsequent psychologists born in the 19th century were also profound: e.g., the work of Narziss Ach (18711946), Wilhelm Wirth (18721952), Robert Woodworth (18691962), and Karl Lashley (1890 1958). Innumerable later-born psychologists and scientists trained in other disciplines (again including Hess and Bernstein) further advanced the interface between psychology and movement neuroscience (for examples, see: Paillard, 1960, 1986; Whiting, 1984; Worringham, 1992). Sherringtons role was somewhat dierent. He certainly championed the study of both, but as relatively separate entities (see, e.g., Sherrington, 1940). Despite the extent and quality of the eort of those who initially advanced the interface between psychology and movement neuroscience, the current interaction between these two areas is weaker than that between biological and physical science approaches, at least in N. American movement neuroscience. This problem is likely to be short-lived, however, given the recent interdisciplinary impact of the theory and techniques of cognitive science (e.g., Hommel, 2003; Hommel, Ridderinkof, & Theewes, 2002; Rushworth, Walton, Kennerley, & Bannerman, 2004). 5.2. Interphyletic awareness This term was coined in the mid-1980s (Stuart, 1985) to emphasize the signicance for movement neuroscience of considering selected neural control mechanisms and strategies that are applicable to invertebrates, non-mammalian vertebrates, and mammalian vertebrates, including humans (for review: Pearson, 1993). Furthermore, a synthesis of inside-out and outside-in approaches is more readily achievable in invertebrate and non-mammalian vertebrate species than in mammalian vertebrates. Such a comparative emphasis in movement neuroscience dates back to at least the 19th and early 20th century: e.g., the research strategy and interests of Etienne-Jules Marey (18301904), August Forel (18481931), Jacob von Uexku (18641944), Albrecht Bethe (18721954), James Gray ll (18911975), Paul Weiss (18981989), and Erich von Holst (19081962). Among the three subjects of this article, Bernstein seems to have been the most strongly inuenced by comparative ndings. Sherrington and Hess may well have kept up with relevant comparative literature but they, themselves, wrote no articles with the interphyletic interest and insight displayed in Essay 3 of Bernsteins 1991/1996 book on dexterity (see pgs. 4596 in Latash & Turvey, 1996). In retrospect, this is somewhat surprising considering the respect Sherrington held for his comparative mentor, Walter Gaskell (see pgs. 1113 in Granit, 1966) and the early (childhood) interests of Hess in botany and zoology (pg. 401 in Hess, 1963). Even today, interphyletic awareness is better accepted for molecular (e.g., genes, ion channels, myosin isoforms, Ca2+ binding proteins) and cellular (e.g., mitosis, metabolic pathways, synaptic transmission) mechanisms than for the systems and organismic levels of enquiry. Nonetheless, the case for the latter two is no less compelling. For example, it has been particularly prominent in studies on the neural control of locomotion since at least the early 1970s (for various aspects of this point, see Clarac, 1991; Delcomyn, 1980; Grillner, Stein, Stuart, Forrsberg, & Herman, 1986; Herman, Grillner, Stein, & Stuart, 1976; Stein, 1999; Stein, Grillner, Selverston, & Stuart, 1997; Stuart & McDonagh,

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1998). Its value is just as evident in other areas, too, like olfaction (Hildebrand & Shepherd, 1997) and visually guided head-neck movements (Strausfeld, 1997). If the English neurophysiologist, Keith Lucas (18791916), had survived a 1916 plane crash and gone on with his stellar career (Fletcher, 1934), the British, and indeed Western European and North American, pre-WWII research on posture and movement may have emphasized far more work on non-mammalian vertebrates and invertebrates (Stuart et al., 2001). Lucas sought to change . . . the lack of interaction between evolutionary concepts and physiological research . . . Lucas emphasized that . . . the primary problem of comparative physiology. . .[is] the question to what extent and along what lines the functional capabilities of animal cells have been changed by evolution (pg. 534 in Gillespie, 1973; citing pg. 325 in Lucas, 1909). 5.3. Transnationalism Since WWII, advances in movement neuroscience have been paralleled by the eld becoming progressively more transnational, with scientists often working for several years in foreign countries, attending international symposia in a wide variety of countries, and contributing to the activities of organizations that promulgate international training and collaboration. Such activities were also evident in the 19th century, but slowed in the rst part of the 20th century by events leading to WWs I and II, and a post-WWII (if not postWWI) seeming aversion in English-speaking countries to the rich tradition of German movement neuroscience (Wiesendanger, 1997, 1998). Sherrington proted greatly from the steady inux of Rhodes Scholars and other likemotivated trainees from Australia, Canada, New Zealand, South Africa, and the USA. In return, he gave these colonials the very best of counseling, irrespective of the biomedical area to which they were subsequently attracted (e.g., pgs. 9294 in Eccles & Gibson, 1979). He had great empathy for Canada and the USA, which countries he visited several times, and even came close to accepting a position at the University of Toronto in the early 1900s (pgs. 2122 in Eccles & Gibson, 1979). Sherringtons laboratory at the Universities of Liverpool and Oxford also attracted neuroscientists from Europe. They came either for periods of research (see Table 1 in Stuart et al., 2001) or a day or two of discussion. In most cases, it appears that both they and Sherrington enjoyed and proted from their exchanges (e.g., pg. 88 in Granit, 1966), an exception being a visit by Hess in 19171918 (pg. 413 in Hess, 1963). In return, Sherrington traveled widely throughout Europe, including a 1914 trip to St. Petersburg to see Pavlov (pg. 56 in Brazier, 1959). In view of the above, it is bothersome that Sherrington gave no credit to, nor even cited, the seminal ndings on human spinal reexes of the German physiologist, Paul Homann (18841962). These ndings included the Eigenreex, which Homann proposed was a monosynaptic pathway (Homann, 1910, 1922, 1934). This was later proven, and it became known as the H-reex in Homans honor (for further details, see Jung, 1992; Wiesendanger, 1997). This blind spot of Sherrington is even more troubling because Homann worked with him at the University of Liverpool in 1912, at least two years after Homans rst major article on spinal reexes (Homann, 1910). It is also puzzling why Sherrington paid virtually no attention to the outside-in ndings and viewpoints of outstanding German movement neuroscientists like Liepman

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(1900), Kohnstamm (1901), Foerster (1902), and later, von Holst (1932).6 In my opinion, Sherringtons 1885-onwards, outspoken opposition to Prussian militarism (Granit, 1966; Eccles & Gibson, 1979) was not a factor. Note, for example, Granit (1966; pg. 60) comment that . . . Important studies on the spinal animal were performed in Goltzs laboratory in the nineties [i.e., 1890s] and Sherrington visited it several times. Rather, it would appear that Sherringtons adherence to inside-out ndings in movement neuroscience outweighed his intrinsic transnationalism! In sharp contrast to Sherrington, Hess had limited international opportunities despite his enthusiasm for them (Hess, 1963). In his case, albeit living in neutral Switzerland, both his publishing largely in German and WWII denied him the opportunity to train foreign workers. This was also to the detriment of international movement neuroscience. It remains unknown to Western workers if Bernstein would have liked to interact with his international peers. Certainly, both he and they would have proted from the one-onone exchange of ideas. The power structure of his country throughout his adult life, however, did not favor internationalism in science, thereby diminishing the inuence of USSR science at the international level, and reducing the visibility of innumerable outstanding scientists, including Bernstein. In nal summary, modern movement neuroscience stands on the shoulders of many giants, who were trained in several countries and in several dierent elds. In this article, three of them are discussed and many more deserve the same consideration. Hopefully, an increased emphasis in training programs on historical aspects of the discipline will convince the next generation of movement neuroscientists that interdisciplinarity, interphyletic awareness, and transnationalism can continue to open new doors in this everintriguing eld. Acknowledgements Presented, in part, as oral presentations at (1) the international symposium Higher Nervous Control of Posture and Locomotion: Parallel and Centralized Control Systems (organizer/director, Shigemi Mori), National Institute for Physiological Sciences, Okazaki, Japan, March 1820, 2001 and (2) the 7th Motor Control and Human Skill Conference (convener, Jan Piek), Freemantle, Western Australia, February 37, 2005. Note that the former symposium was followed by a research volume: Mori, S., Stuart, D.G., and Wiesendanger, M. (2003). Brain mechanisms for the integration of posture and movement, Volume 143, Progress in Brain Research. Amsterdam: Elsevier. I would like to thank Roger Enoka, Sten Grillner, Shigemi Mori, Mark Latash, and Mario Wiesendanger for reviewing a draft of this article. Understandably, their viewpoints do not necessarily coincide with those expressed in this report. Also thanked are Patricia Pierce for her editorial assistance, Nga Nguyen for her library research, and Mario Wiesendanger and Wulla Gronenberg for their help with the translated titles of several German articles and books.

6 The published contributions of Erich von Holst (19081962) span 1932 to his untimely death in 1962. Much of his work is summarized in a two-volume collection (von Holst, 1969).

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References
Adrian, E. T. (1966). Thomas Graham Brown. Biographical Memoirs of Fellows of the Royal Society, 12, 2333. Akert, K. (Ed.). (1981). Biological order and brain organization. Selected works of W.R. Hess. Berlin: Springer. Akert, K. (1999). Walter Rudolf Hess (18811973) and his contribution to neuroscience. Journal of the History of the Neurosciences, 8, 248263. Bailes, K. E. (1978). Technology and society under Lenin and Stalin. Princeton: Princeton University Press. Berkinblit, M. B., Vasilev, J. M., & Shik, M. L. (1974). The work of I.M. Gelfand in biology. Russian Mathematical Surveys, 29, 4553. Bernstein, N. A. (1929). Klinitcheskie puty sovremenoi biomechaniki [Clinical ways of modern biomechanics]. Sbornik trudov Gos. in-ta usovershenstvovaniya vratchey v Kazany (Vol. 1, pp. 249270). Kazan, Russia: Glavnauka (This book is a collection of papers of the Institute for Medical Improvement). Bernstein, N. A. (1940/1967). Issledovaniya po biodynamike chodby, bega, prizhka [Studies on the biodynamics of walking, running and jumping]. Moscow: Physical Culture and Sport (For English translation, see chap. III in Bernstein, 1947). Bernstein, N. A. (1935/1967). Problema vzaimootnosheniya koordinazii i lokalizazii [The problem of the interrelation of coordination and localization]. Arkhiv Biologicheskikh Nauk, 38, 138 (For English translation, see chap. II in Bernstein, 1967). Bernstein, N. A. (1947). O postroenii dvizhenii [On the construction of movements]. Moscow: Medzig. Bernstein, N. A. (1967). On the co-ordination and regulation of movements. New York: Pergamon (A collection of English-translated papers published previously in Russian and German journals and monographs). Bernstein, N. A. (1992). Biomechanika i protezirovanie. No. 1 [Biomechanics and prosthetics. No. 1]. Moscow: Central Institute for Prosthetic Appliances. Bernstein, N. A. (2003). In I. M. Feigenberg & I. E. Sirotkina (Eds.), Sovremennie iskania v ziologii nervnogo processa [Modern research in the physiology of neural processes]. Moscow: Smysl [Sense] (See footnote 4). Bongaardt, R. (2001). How Bernstein conquered movement. In M. L. Latash & V. Zatsiorsky (Eds.), Classical papers in movement science (pp. 5984). Champaign, IL: Human Kinetics. Brazier, M. A. B. (1959). The historical development of neurophysiology. In J. Field, H. W. Magoun, & V. E. Hall (Eds.). Handbook of physiology, neurophysiology (Vol. I, pp. 158). Washington, DC: American Physiological Society. Bretag, A. (1983). Who did invent the intracellular microelectrode? Trends in Neuroscience, 6, 365. Brown, T. G. (1916). Die Reex Funktionen des Zentralnervensystems mit besonderer Berucksichtigung der rhythmischen Tatigkeiten bei Saugetieren [Reex functions of the central nervous system with particular consideration of rhythmic activities in mammals]. Ergebnisse der Physiologie, 15, 480490. Clarac, F., Humphrey, D. R., & Freund, H. J. (1991). How do sensory and motor signals interact during locomotion? A comparative point of view. In Dahlem workshop on motor control: Concepts and issues (pp. 199201). Chichester, UK: John Wiley and Sons. Creed, R. S., Denny-Brown, D., Eccles, J. C., Liddell, E. G. T., & Sherrington, C. S. (1932). Reex activity of the spinal cord. Oxford, UK: Clarendon Press (Note: This books chap. 7 [p. 55] was written solely by Sherrington and it may be considered . . . his last purely scientic writing and . . . the crowning achievement of the Oxford School . . . [pages 6566 in Eccles and Gibson, 1979]). Delcomyn, F. (1980). Neural basis of rhythmic behavior in animals. Science, 210, 492498. Eccles, J. C., & Gibson, W. C. (1979). Sherrington: His life and thought. Berlin: Springer-Verlag. Editors Obituary (1966). Mikhail, LVovich Tsetlin. Biophysics, 11, 10801082 (Translation from the Russian journal Biophysika). Feigenberg, I. M. (2004). Nikolai Bernstein. Ot reeksa k modeli buduschego [Nikolai Bernstein. From the reex to the model of the future]. Moscow: Smysl [Sense]. Feigenberg, I. M., Latash, L. P., Latash, M. L., & Turvey, M. T. (1996). N.A. Bernstein: The reformer of neuroscience. In Dexterity and its development (pp. 247275). Mahwah, NJ: Lawrence Erlbaum. Fletcher, W. M. (Ed.). (1934). Keith Lucas. Cambridge, UK: Heer (Note: Originally written in 1916; published after Fletchers death). Foerster, O. (1902). Die Physiologie und Pathologie der Coordination; eine Analyse der Bewegungsstorungen bei den Erkrankungen des Centralnervensystems und ihre rationelle Therapie [Physiology and pathology of coordination an analysis of movement disorders occurring with diseases of the central nervous system and their rational therapy]. Jena, Germany: Fischer. Fulton, J. F. (1955). A textbook of physiology. Philadelphia: W.B. Saunders.

640

D.G. Stuart / Human Movement Science 24 (2005) 621643

Gelfand, I. M., Gurnkel, V. S., Fomin, S. V., & Tsetlin, M. L. (1966). Models of the structural-functional organization of certain biological systems. Moscow: Academy of Science of the USSR [in Russian] (English translation by C. R. Beard and edited by J. S. Barlow, Boston: MIT Press). Gillespie, C. C. (Ed.). (1973). Lucas, Keith. Dictionary of Scientic Biography (Vol. VIII, pp. 532535). New York: Charles Scribners Sons. Gloor, P. (1954). Autonomic functions of the diencephalon; a summary of the experimental work of Prof. W.R. Hess. Archives of Neurology and Psychiatry, 71, 773790. Granit, R. (1966). Charles Scott Sherrington: An appraisal. London: Thomas Nelson and Sons. Grillner, S., Stein, P. S. G., Stuart, D. G., Forrsberg, H., & Herman, R. M. (Eds.). (1986). Neurobiology of vertebrate locomotion. London, UK: Macmillan Press. Grillner, S., & Wallen, P. (2004). Innate versus learned movements a false dichotomy? Progress in Brain Research, 143, 312. Grunbaum, A. S. F., & Sherrington, C. S. (1901). Observations on the physiology of the cerebral cortex of some higher apes. Proceedings of the Royal Society of London Series B: Biological Science, 69, 206209 (Note: Grunbaum later changed his name to Leyton). Grunbaum, A. S. F., & Sherrington, C. S. (1903). Observations on the physiology of the cerebral cortex of the higher anthropoid apes. Proceedings of the Royal Society of London Series B: Biological Science, 72, 152155. Gurnkel, V. S., & Cordo, P. J. (1998). The scientic legacy of Nikolai Bernstein. In M. L. Latash (Ed.), Progress in motor control - Bernsteins traditions in movement studies (pp. 119). Champaign, IL: Human Kinetics. Gurnkel, V. S., & Shik, M. L. (1973). The control of posture and locomotion. In A. A. Gydikov, N. T. Tankov, & D. S. Kosarov (Eds.), Motor control (pp. 217234). New York: Plenum. Hasan, Z., & Stuart, D. G. (1988). Animal solutions to problems of movement control: The role of proprioceptors. Annual Reviews of Neuroscience, 11, 199223. Head, H. (1920). Studies in neurology (Vol. 2). London: Frowde, Hodder & Stoughton. Herman, R. M., Grillner, S., Stein, P. S. G., & Stuart, D. G. (Eds.). (1976). Neural control of locomotion. New York: Plenum Press. Hess, W. R. (1942). Biomotorik als Organisationproblem I und II [The biomotor system as an organization problem, I and II]. Naturwissenschaften, 30, 441448, 537541. (For English translation, see chap. 15 in Akert, 1981). Hess, W. R. (1943). Teleokinetische und ereismatische Kraftesysteme in der Biomotorik [Teleokinetic and ereismatic mechanisms and biomotor functions]. Helvetica Physiologica Acta, 1, C62C63 (For English translation see chap. 16 in Akert, 1981). Hess, W. R. (1949). Das Zwischenhirn. Syndrome, Localisationen, Funktionen [Autonomic and extrapyramidal functions]. Basel: Schwabe (English translation in 1954, Diencephalon. New York: Grune & Stratton). Hess, W. R. (1962). Psychologie in biologischer Sicht [A biological approach to psychology]. Stuttgart: Thieme (English translation in 1964, The biology of the mind. Chicago: University of Chicago Press). Hess, W. R. (1963). From medical practice to theoretical medicine. An autobiographic sketch. Perspectives in Biology and Medicine, 6, 400423. Hess, W. R. (1965). Cerebrale Organisation somatomotorischer Leistungen. I. Physikalische Vorbemerkungen und Analyse konkreter Beispiele [Cerebral organization of motor tasks. I. Physical remarks followed by an analysis of concrete examples]. Archiv far Psychiatrie und Nervenkrankheiten, 207, 3344. Hess, W. R., Burgi, S., & Bucher, V. (1946). Motorische Funktionen des Tektal- und Tegment-algebeites [Motor functions of tectal and tegmental areas]. Monatsschrift fur Psychiatrie und Neurologie, 112, 152 (For English translation, see chap. 17 in Akert, 1981). Hess, W. R., & Fischer, H. (1973). Brain and consciousness. A discussion about the function of the brain. Perspectives on Biology and Medicine, 17, 109118. Hildebrand, J. G., & Shepherd, G. M. (1997). Mechanisms of olfactory discrimination: Common principles across phyla. Annual Review of Neuroscience, 20, 595631. Homann, P. (1910). Beitrage zur Kenntnis der menschlichen Reexe mit besonder Berucksichtigung der elektrischen Erscheinungen [Contributions to the knowledge of human reexes with particular reference to electrical phenomena]. Archiv fur Anatomie, Physiologie und wissenschaftliche Medicin, 1910, 223246. Homann, P. (1922). Die Eigenreexe (Sehnenreexe) menschlicher Muskeln [The monosynaptic reexes (tendon reexes) of human muscles]. Berlin: Springer-Verlag. Homann, P. (1934). Die physiologischen Eigenschaften der Eigenreexe [The physiological properties of monosynaptic reexes]. Ergebnisse der Physiologie, 34, 15108. Hommel, B. (2003). Planning and representing intentional action. The Scientic World Journal, 3, 593608.

D.G. Stuart / Human Movement Science 24 (2005) 621643

641

Hommel, B., Ridderinkof, K. R., & Theewes, J. (2002). Cognitive control f attention and action: Issues and trends. Psychological Research, 66, 215219. Hoyle, G. (1983). Origins of intracellular microelectrodes. Trends in Neuroscience, 6, 163. Jung, R. (1981). Walter R. Hess (18811973) [Ditto; an obituary]. Reviews of Physiology, Biochemistry and Pharmacology, 88, 122. Jung, R. (1992). Some European neuroscientists: A personal tribute. In I. F. G. Worden, J. P. Swazey, & G. Adelman (Eds.), The neurosciences: Paths of discovery (pp. 477511). Boston: Birkhauser (First published by MIT Press in 1975). Jung, R., & Hassler, R. (1960). The extrapyramidal motor system. In J. Field, H. W. Magoun, & V. E. Hall (Eds.), Handbook of physiology, Sec. 1. Neurophysiology (Vol. II, pp. 863927). Washington, DC: American Physiological Society. Kohnstamm, O. (1901). Uber Koordination, Tonus und Hemmung [On coordination, muscle tone and inhibition]. Zeitschrift fur Diat und Physikalische Therapie, 4, 112122 [in German]. Lashley, K. S. (1917). The accuracy of movement in the absence of excitation from a moving organ. American Journal of Physiology, 43, 169194. Lashley, K. S. (1929). Brain mechanisms and intelligence: A quantitative study of injuries to the brain. Chicago: University of Chicago Press. Lashley, K. S. (1933). Integrative functions of the cerebral cortex. Physiological Reviews, 13, 142. Latash, M. (1998a). Neurophysiological basis of movement. Champaign, IL: Human Kinetics. Latash, M. L. (Ed.). (1998b). Progress in motor control Bernsteins traditions in movement studies. Champaign, IL: Human Kinetics. Latash, M. L. (2005). A new biography of Nikolai Bernstein. Motor Control, 9, 12. Latash, M. L., & Turvey, M. T. (1996). Dexterity and its development (including On dexterity and its development by N. A. Bernstein as translated from Russian by M. L. Latash). Mahwah, NJ: Lawrence Erlbaum. Leyton, A. S. F., & Sherrington, C. S. (1917). Observations on the excitable cortex of the chimpanzee, orang-utan and gorilla. Quarterly Journal of Experimental Physiology, 11, 135222. Liepman, H. (1900). Das Krankheitsbild der Apraxia (motorische Asymbolie) auf Grund eines Falles von Apraxie [The clinical picture of apraxia (motor asymboly) based on one case of apraxia]. Monatschrift fur Psychiatrie, 8, 1544, 102132, 188197. Liddell, E. G. T. (1952). Charles Scott Sherrington: 18571952. Obituary Notices of Fellows of the Royal Society, 8, 241270. Loeb, G. E. (1987). Hard lessons in motor control from the mammalian spinal cord. Trends in Neuroscience, 10, 108113. Lucas, K. (1909). The evolution of animal function. Science Progress, 20 cent., London, 3, 472483. Lundberg, A. (1969). Reex control of stepping Nansen memorial lecture to Norwegian Academy of Sciences. Oslo: Universitetsforlarget. Lundberg, A., & Phillips, C. G. (1973). T Graham Browns lm on locomotion in the decerebrate cat. Journal of Physiology (London), 231, 9091. Magnus, R. (1924). Korperstellung [Posture]. Berlin: Springer. Massion, J., Alexandrov, A., & Frolov, A. (2004). Why and how are posture and movement coordinated. Progress in Brain Research, 143, 1327. Mori, S., Stuart, D. G., & Wiesendanger, M. (2004). Brain mechanisms for the integration of posture and movement. Progress in Brain Research (Vol. 143). Amsterdam: Elsevier. Orlovsky, G. N., Deliagina, T. G., & Grillner, S. (1999). Neuronal control of locomotion from mollusc to man. New York: Oxford University Press. Paillard, J. (1960). The pattening of skilled movements. In J. Field, H. W. Magoun, & V. E. Hall (Eds.), Handbook of physiology, Sec. 1. Neurophysiology (Vol. III, pp. 1671708). Washington, DC: American Physiological Society. Paillard, J. (1986). Development and acquisition of motor skills: A challenging prospect for neuroscience. In M. G. Wade & H. T. A. Whiting (Eds.), Motor development in children: Aspects of coordination and control (pp. 415441). Ordrecht: Martinus Nijho Publishers. Pearson, K. G. (1993). Common principles of motor control in vertebrates and invertebrates. Annual Review of Neuroscience, 16, 265297. ` Philippson, M. (1905). Lautonomie et la centralisation dans le systeme nerveux des animaux: etude de physiologie experimentale et compare [Autonomy and centralization in the nervous system of animals: Studies in experimental and comparative physiology]. Brussels: Falk.

642

D.G. Stuart / Human Movement Science 24 (2005) 621643

Porter, R., & Lemon, R. (1993). Corticospinal function and voluntary movement. New York: Oxford University Press. Prochazka, A. (1993). Comparison of natural and articial movement control of movement. IEEE Transactions on Rehabilitation Engineering, 1, 717. Prochazka, A. (1996). Proprioceptive feedback and movement regulation. In L. B. Rowell & J. T. Shepherd (Eds.), Handbook of physiology, Sec. 12, Exercise: Regulation and integration of multiple systems (pp. 89127). New York: Oxford University Press. Prus, J. (1898). Ueber die Leitungsbahnen und Pathogenese der Rindenepilepsie [Pathways and pathogenesis of cortical epilepsy]. Wiener klinische Wochenschrift, 11, 857863. Rushworth, M. F., Walton, M. E., Kennerley, S. W., & Bannerman, D. M. (2004). Action sets and decisions in the medial frontal cortex. Trends in Cognitive Science, 8(9), 410417. Sherrington, C. S. (1906). The integrative action of the nervous system. New Haven, CT: Yale University Press (Republished by Cambridge University Press, UK in 1947). Sherrington, C. S. (1931). Quantitative management of contraction in lowest level co-ordination. Hughlings Jackson Lecture. Brain, 54, 148. Sherrington, C. S. (1932). Inhibition as a coordinative factor. Nobel Lecture, December 12, 1932. In Les Prix Nobel (pp. 278289). Stockholm: Nobel Foundation. Sherrington, C. S. (1940). Man on his nature. The Giord lectures, Edinburgh, 193738. Cambridge, UK: Cambridge University Press. Shik, M. L., Severin, F. V., & Orlovsky, G. N. (1966). Organization of locomotor synergism. Biophysics, 11, 10111019. Stein, P. S. G. (1999). Central pattern generators and interphyletic awareness. Progress in Brain Research, 123, 259271. Stein, P. S. G., Grillner, S., Selverston, A. I., & Stuart, D. G. (Eds.). (1997). Neurons, networks, and motor behavior. Boston, MA: MIT Press. Strausfeld, N. J. (1997). Oculomotor control in insects: From muscles to elementary motion detectors. In P. S. G. Stein, S. Grillner, A. I. Selverston, & D. G. Stuart (Eds.), Neurons, networks, and motor behavior (pp. 277284). Boston: MIT Press. Stuart, D. G. (1985). Summary and challenges for future work. In P. S. G. Stein (Ed.), Short course syllabus Motor control: From movement trajectories to neural mechanisms (pp. 95105). Bethesda, MD: Society for Neuroscience. Stuart, D. G., & McDonagh, J. C. (1998). Reections on a Bernsteinian approach to systems neuroscience: The controlled locomotion of high-decerebrate cats. In M. L. Latash (Ed.), Progress in motor control Bernsteins traditions in movement studies (pp. 2149). Champaign, IL: Human Kinetics. Stuart, D. G., Pierce, P. A., Callister, R. J., Brichta, A., & McDonagh, J. C. (2001). Sir Charles Sherrington: Humanist, mentor, and movement neuroscientist. In M. L. Latash & V. Zatsiorsky (Eds.), Classical papers in movement science (pp. 317374). Champaign, IL: Human Kinetics. Swazey, J. P. (1969). Reexes and motor integration: Sherringtons concept of integrative action. Cambridge, MA: Harvard University Press. Vogt, C., & Vogt, J. (19061907). Zur Kenntnis der elektrisch erregbaren Hirnindengebiete bei den Saugetieren [About the actual knowledge of the electrically excitable cortical areas in mammals]. Journal fur Psychologie und Neurologie, 8, 277456. Vogt, C., & Vogt, J. (19191920). Allegemeinere Ergebnisse unserer Hirnforschung [General results from our brain research]. Journal fur Psychologie und Neurologie, 25, 279461. von Holst, E. (1932). Untersuchungen uber die Funktionen des Zentralnervensystems beim Regenwurm [Investigations of the function of the central nervous system of the earthworm]. Zoologische Jahrbuecher, Abteilung fuer Allgemeine Zoologie und Physiologie der Tiere, 51, 547588. von Holst, E. (1969). Zur Verhaltensphysiolgie bei Tieren und Menschen. Gesammelte Abhandlungen [The behavioral physiology of animal and man]. Munich: R. Piper (In two volumes, with Vol. 1 translated into English: (1973). Coral Gables, FL, USA: Hillsdale). Vucinich, A. (1984). Empire of knowledge: The Academy of Sciences of the USSR (19171970). Berkeley, CA: University of California Press. Wachholder, K. (1928). Willkurliche Haltung und Bewegung [Volitional standing and moving]. Ergebnisse der Physiologie, 26, 568775. Whiting, H. T. A. (1984). Human motor actions Bernstein reassessed. Amsterdam: North-Holland. Wiener, N. (1948). Cybernetics, or control and communication in the animal and the machine. New York: Wiley.

D.G. Stuart / Human Movement Science 24 (2005) 621643

643

Wiesendanger, M. (1997). Paths of discovery in human motor control: A short historical perspective. In M.-C. Hepp-Reymond & G. Marini (Eds.), Perspectives of motor behavior and its neural basis (pp. 103124). Basel: S. Karger AG. Wiesendanger, M. (1998). Bernsteins principle of equal simplicity and related concepts. In M. L. Latash (Ed.), Progress in motor control Bernsteins traditions in movement studies (pp. 105125). Champaign, IL: Human Kinetics. Wilson, S. A. K. (1924). The old motor system and the new. Archives of Neurology and Psychiatry, 11, 385404. Worringham, C. J. (1992). Some historical roots of phenomena and methods in motor behavior research. In G. E. Stelmach & J. Requin (Eds.), Tutorials in motor behavior II (pp. 807825). Amsterdam: Elsevier B.V.

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