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

Human Movement Science 24 (2005) 621–643

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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 centralnervous 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 groundworkfor these modern-day concepts. Here, the focus is on three of this group with each selected for asomewhat different reason. Charles Sherrington (1857–1952) had innumerable contributions thatwere certainly needed in the subsequent study of posture and movement: inhibition as an active coor-dinative mechanism, the functional anatomy of spinal cord-muscle connectivity, and helping set thestage for modern work on the sensorimotor cortex and the corticospinal tract. Sadly, however, bynot championing the work of his trainee and collaborator, Thomas Graham Brown (1882–1965),he delayed progress on two key motor control mechanisms: central programming and pattern gen-eration. Walter Hess (1881–1973), a self-taught experimentalist, is now best known for his work onCNS coordination of autonomic (visceral) and emotional behavior. His contributions to posture andmovement, however, were also far-reaching: the coordination of eye movements and integration ofgoal-directed and ‘‘framework’’ (anticipatory set) motor behavior. Nikolai Bernstein (1896–1966),the quintessence of an interdisciplinary, self-taught movement neuroscientist, made far-reaching con-tributions that were barely recognized by Western workers prior to the 1960s. Today, he is widelypraised for showing that the CNS�s hierarchy of control mechanisms for posture and movement isorganized hand-in-hand with distributed and parallel processing, with all three subject to evolution-ary pressures. He also made important observations, like those of several previous workers, on thegoal focus of voluntary movements. The contributions of Sherrington, Hess, and Bernstein areenduring. They prompt thought on the philosophical axioms that appear to have driven their

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doi:10.1016/j.humov.2005.09.011

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622 D.G. Stuart / Human Movement Science 24 (2005) 621–643

research, and the continual need for emphasis on interdisciplinary, comparative, and transnationalapproaches to advance movement neuroscience.� 2005 Elsevier B.V. All rights reserved.

PsycINFO classification: 2330

Keywords: Posture; Movement; History of movement neuroscience

1. Introduction

It is now well accepted that neural mechanisms involved in the integration of posturewith movement in humans, other vertebrates, and invertebrates are widespread through-out the central nervous system (CNS), and they are recruited in patterns that are bothtask- and context-dependent (Mori, Stuart, & Wiesendanger, 2004). Two possibilitiesare on the forefront of current mammalian research on this topic. One proposes two sep-arate, albeit parallel and coordinated, control systems, one for postural adjustment andthe other for movement (see, e.g., Fig. 1 in Massion, Alexandrov, & Frolov, 2004). Theother possibility is that a single coordinated control system exists, achieving simulta-neously 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 rel-ative merits of these two models. Rather, it is to reflect on some of the ideas and results ofearlier workers, which have bearing on the models� current evaluation. This article focuseson 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 inthis field. Sherrington was chosen for a somewhat different reason. Despite his many essen-tial and indeed Herculean contributions, his reflex focus and ‘‘inside-out’’ approach (seebelow) were not conducive to the study of movement, in general, and the integration ofposture and movement, in particular.

The article concludes with some thoughts on the philosophical axioms that appear tohave driven the research efforts of these three stellar neuroscientists, and the continualneed for emphasis on interdisciplinary, comparative, and transnational approaches toadvance movement neuroscience.

2. Charles Sherrington (1857–1953)

Few neuroscientists achieved in their lifetime the visibility, influence, and accoladesbestowed upon Sherrington for his humanistic nature, mentoring success, scientific accom-plishments, 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. Thomas�s Hospital Medical School (London,Great Britain) in 1877, but he switched to the University of Cambridge in 1879, where hegraduated in 1883 with a degree in natural science (including botany, zoology, and humananatomy and physiology), followed by a medical degree in 1885. While at Cambridge, hereceived thorough neuroscience mentoring from two prominent and experienced physiol-ogists, John Langley (1852–1925) and Walter Gaskell (1847–1914), the latter emphasizing

Fig. 1. The three subjects of this article. Top-left: Charles S. Sherrington (1857–1953) at about 45 years ofage. (From Granit, 1966, Plate 8) Top-right: Walter Hess (1881–1973) when 55 years of age. (From Wordenet al., 1992, p. 490, Fig. 27.7. Reprinted with permission from Springer-Verlag.) Bottom: Nikolai Bernstein(1896–1966) at the age of 55 years. (From Latash, 1998, p. viii. Reprinted with permission from M.L.Latash.)

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comparative issues. Sherrington�s postdoctoral training included 1–2 months (1884) withEduard Pfluger (1829–1900) at the University of Bonn, a year (1884–1885) with FriedrichGoltz (1834–1902) at the University of Strasbourg, 2 months (1886) with Rudolph Vir-chow (1821–1902) at the University of Berlin and a year (1886–1887) with Robert Koch(1843–1910) at the same institution. While these European experiences were largely in neu-rohistology and pathology, Sherrington also strengthened his hand in the all-round studyof the CNS (pgs. 9–14 in Swazey, 1969).

Subsequently, Sherrington made substantial contributions to overall neuroscience andmovement neuroscience in his own laboratory, with the majority of his post-training workundertaken at the Universities of Cambridge (1887–1895), Liverpool (1895–1912) andOxford (1913–1936).


For neuroscience, in general, Sherrington�s writings on overall aspects of CNS function(rather than his own extensive personal research findings) helped emphasize the validityand significance of the synapse in CNS circuitry and function. His experimental prowessis possibly best revealed and remembered in work showing that inhibition is an active pro-cess in the CNS and a co-partner of excitation in brain function. (For details, see Stuartet al., 2001, which chapter has specific reference to 52 of Sherrington�s most significantarticles.)

For the integration of posture and movement, Sherrington�s major contributions wereto delineate the functional organization of the sensorimotor cortex and the corticospinaltract (Fig. 2), and advance understanding of the segmental convergence of descendingcommand signals and sensory feedback signals (Stuart et al., 2001). The former work(Grunbaum & Sherrington, 1901, 1903; Leyton & Sherrington, 1917) has been rightlylauded in modern accounts of voluntary movement (e.g., pgs. 5–9 in Porter & Lemon,1993).

In retrospect, work undertaken in the same era on the extrapyramidal pathways, a termcoined in an 1898 article on epilepsy by Johann Prus (1858–1926),1 was of equal signifi-cance. Vogt and Vogt (1906–1907, 1919–1920) pioneered this work. It is rarely cited, how-ever, in modern accounts of posture and movement.

Sherrington�s segmental (spinal cord and peripheral neuromuscular) contributionswere his most substantial: the functional anatomy of spinal cord-muscle connectivity,about which there had been much prior inaccuracy, uncertainty and confusion, andthe reflex play of one muscle�s (and/or one dermatome�s) sensory input upon anothermuscle�s activity and/or movement. The latter work, which required much experimentaland theoretical skill, yielded many concepts that are still in the forefront of thought onspinal cord function: central excitatory vs. inhibitory state, discharge zone and subli-minal fringe, spatiotemporal summation, disynaptic reflex pathways, reflex after-discharge, integrative reflex action, and the final common path. He also provided denovo findings on motor units and wrote extensively on modulation of movement bysensory feedback.

Clearly, Sherrington fully deserved his 1932 Nobel Prize! He provided few, if any, directcontributions to ideas on the integration of posture and movement, however: i.e., as basedon his own research. Admittedly, as ‘‘. . . the great integrator of knowledge of the centralnervous system . . .’’ (pg. ix in Eccles & Gibson, 1979), he is widely quoted on what hewrote about posture and movement. For example, Sherrington is recognized, along in par-ticular with Rudolph Magnus (1873–1927; see Magnus, 1924), for the view espoused in hisclassic 1906 text (pgs. 336–344 in 1947 edition) that ‘‘the body�s orientation with respect togravity was determined by a group of reflexes that sets the body segments� collective ori-entation and stabilizes the orientation against external disturbances’’ (pg. 13 in Massionet al., 2004). Subsequently, however, he said little about this topic in terms of overall bodyposture during movement. In his 1932 summing up chapter on his major area of research,spinal reflex coordination, he did comment briefly on the aphorism ‘‘posture accompaniesmovement like its shadow’’ (pgs. 147–148 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.

Fig. 2. A Sherrington finding on the morphology of the corticospinal tract. It shows the longitudinal distributionof corticospinal axons after a unilateral lesion in the arm area of the motor cortex of a chimpanzee. The crosssections are at the upper (up.py.dec.) and mid (mid.py.dec.) levels of the pyramidal decussation in the lowerbrainstem and at C2 (2c), C8 (8c), T6 (6th) and T12 (12th) levels of the spinal cord. This figure demonstrated thatthe corticospinal innervation is uncrossed at the upper level of the pyramidal decussation, largely crossed andmostly limited to the cervical level of the spinal cord, and near-exclusively crossed and much thinned out at thethoracic level. No degeneration was observed at the lumbar level of the spinal cord (for further details on thesignificance of this finding and its electrophysiological. counterpart, see pgs. 5–10 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 discus-sion of this point.

Some believe that Sherrington moved away from the neural control of body posturebecause he wished to encourage Magnus to be on the forefront in this line of work (pg.95 in Granit, 1966). This viewpoint is difficult to document. There is clear-cut evidence,


however, that Magnus began his postural work on experimental animals while working inSherrington�s 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 ofhow sensory input from the proprioceptors could enhance the quality of rhythmic move-ments. He chose to deemphasize, however, the existence and nature of the essentiallyspinal origin of locomotor pattern generation. Like his well-respected Belgian peer, Mau-rice Philippson (1877–1938), he chose to emphasize the role of interlocking spinal reflexesin the elaboration of locomotion (see, e.g., plate X in Philippson, 1905), while also conced-ing the possibility of a central control of locomotor movements. For example, Sherringtonsometimes emphasized the significance of pioneering 1911–1922 work on the spinal originof locomotor rhythmicity by his former trainee and subsequent collaborator, ThomasGraham Brown (1882–1965; see Brown, 1916). Sherrington�s ambivalence about GrahamBrown�s work was seemingly lifelong, however. As emphasized previously (pg. 334 in Stu-art et al., 2001) he ‘‘did include important comments on Graham Brown�s work on spinalpattern generation in his 1931 Hughlings Jackson Lecture (pg. 25) and the influentialCreed et al. (1932) text (pg. 146), and he did mention Graham Brown in his Nobel lecture’’(see endnotes 28–30). Also, in the foreword to the 1947 edition of Sherrington (1906) heconcedes at the outset that the role of spinal reflex action in motor control should notbe overstated. Later in this foreword, however, there appears ‘‘. . . A train of motor actsresults therefore from a train of external situations’’. This one caveat about Sherrington�scontributions is emphasized because it is now known that the spinal (rather than sensoryinput) origin of locomotor pattern generation is an essential component of the overall neu-ral control of movement.2 with equivalent circuitry extending to the forebrain and cominginto play in the integration of posture and a wide variety of movements; from the mostrudimentary to the most skilled and learning dependent (Grillner & Wallen, 2004).

Sherrington wrote much on why he favored a single-cell/single-reflex approach to thestudy of CNS control mechanisms. In modern-day parlance, Sherrington used an‘‘inside-out’’ approach to movement neuroscience, in which the starting point is the prop-erty of single cells within the CNS and peripheral neuromuscular system and then its exten-sion into the behavior of CNS microcircuits, single reflexes, groups of reflexes, followed bytheorizing on the function of CNS regions like the motor cortex and spinal cord, and finallyoverall motor behavior. The majority of Sherrington�s British peers, including his co-NobelLaureate, Edgar Adrian (1889–1977), also favored this approach. It was a key, indeedessential, precedent to the iterative late 1930-early 1950 refinement and use of the intracel-

2 Graham Brown�s prescient work on spinal rhythm generation languished in near-total obscurity untilLundberg�s widely read 1969 report. Graham Brown appears to have remained a good friend and active colleagueof Sherrington despite their different views on the control of locomotion (see pgs. 333–334 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 film on the treadmill locomotion of the decerebrate cat atan unpublished 1941 meeting of the Physiological Society in London, UK. This film had no captions and itsavailability remained relatively unknown until Lundberg and Phillips (1973) wrote a short account about it. (Thisfilm is now available upon request to The Physiological Society.) Interestingly, Graham Brown, at the age of 80years, wrote to Anders Lundberg and offered to sail his yacht across the North Sea from Scotland to Goteborg,Sweden, to provide Lundberg with appropriate captions for his 1941 film. (His letter, dated February 17, 1962, isavailable upon request from AL or DGS.) Sadly, however, Graham Brown�s subsequent ill-health prevented thisadventuresome and demanding trip, which would have been much appreciated by Lundberg and the movementneuroscience field, as a whole!


lular microelectrode to study single neurons within the CNS and the peripheral neuromus-cular 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 entityby consideration of its separate elements), this being a central theme in British empiricistphilosophy, from John Locke (1632–1704) to Bertrand Russell (1872–1970).

In the 1920s–1940s, important conceptual advances in movement neuroscience werebeing made in Switzerland, Germany, and Russia, using an ‘‘outside-in’’ approach. Forthis, the starting point is consideration of the problems posed by the moving mechanicalsystem, which are solved by the CNS and its circuitry and pathways, with subsequent the-orizing extending down finally 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 influ-enced 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(1770–1831).

Despite his wide reading and broad cultural interests (see Eccles & Gibson, 1979), Sher-ringon appears to have been unaware of, or perhaps impervious to an ‘‘outside-in’’, holis-tic approach to the study of movement neuroscience. This is again revealed in his forewordto the 1947 edition of Sherrington (1906). Admittedly, Sherrington was 91 years of age in1947, and he had essentially stopped his neuroscience research in 1935. Nonetheless, tak-ing all factors into account, great as Sherrington�s contributions were, his legacy in move-ment neuroscience would have been more far-reaching if he had actively promulgatedGraham Brown�s results and been more interdisciplinary and transnational in his overallthought about posture and movement.

3. Walter Hess (1881–1973)

Hess was a remarkably well-rounded, self-taught systems-oriented researcher who ‘‘. . .made pioneering contributions in the field of hemodynamics, physiological optics, oculo-motor diagnostics, regulation of circulation, respiration and temperature, and finally onthe 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 forwhich he received a 1949 Nobel Prize: the functional organization of the diencephalonas the primary coordinator of the activities of visceral organs (Gloor, 1954). Here, how-ever, the focus is on his contributions to movement neuroscience which were also far-reaching.

Hess was an essentially a self-taught physiologist and neuroscientist, with a quantitativebent (Hess, 1963). He studied medicine in Lausanne and Bern in Switzerland, and Berlinand Kiel in Germany. Subsequently, he graduated with an MD degree in 1905 from theUniversity of Zurich. While a medical student, he performed his first research, a theoret-ical analysis of blood vessels. With his MD degree in hand, Hess first decided to become anophthalmologist. While in such training (1906–1908), he developed a new device to mea-sure quantitatively oculomotor coordination in diplopic patients. After four years in pri-vate practice as an ophthalmologist (1908–1912), he returned to the University of Zurichas an assistant in the Physiology Institute. In 1917, at the age of 36 years, he became Chairof Physiology, a position he held until 1951. In all, Hess published original work and


thoughts for 70 years (1903–1973), thereby slightly exceeding the 69-year span of Sherring-ton�s publications (1884–1953)!

Even in the early 1920s, Hess recognized that neural circuitry in the brainstem coordi-nates a variety of autonomic functions. To advance this idea, he pioneered the study ofCNS function in intact, freely moving mammalian preparations, in which he chronicallyimplanted tripolar stimulating electrodes to activate brainstem axons and neurons (seeFig. 27.8 in Jung, 1992). The responses he noted included not only vegetative changesin blood pressure, heart rate, and respiratory activity, but also behavioral aspects ofemotion (e.g., increased and deceased alertness, aggressiveness, anger, flight, sleep).

Less widely known is that throughout the above work, Hess became increasingly inter-ested in the principles of motor organization. He observed that electrical stimulation incertain motor structures of the brainstem and basal ganglia could elicit directed move-ments that were accompanied with appropriate postural changes. This prompted him tomodel goal-oriented movements and their accompanying postural adjustments. Contraryto the then prevailing influence of Sherrington (1906) and Magnus (1924), Hess held theview that without anticipation of postural adaptations (a component of his framework‘‘ereismatic’’ system), goal-directed movements (his ‘‘teleokinetic’’ system) were doomedto failure; the effects of reflexes were too slow to compensate for self-induced disturbancesproduced by voluntary movements. In order to transmit this notion to his students, Hessused a very effective human model of volitional goal-oriented movements, which is shownin Fig. 3.

Fig. 3 shows that the goal of voluntary movement (teleokinetic motility) in Hess�smodel was represented by a student who was to jump from the shoulders of anotherstudent to a defined target on the floor. The supporting student represented the frame-work (postural support) of the movement. The demonstration showed that the inten-tional movement was only correctly performed if a third student was behind theback of the postural student providing anticipatory set (bereitschaft). Possibly, bothpostural framework and anticipatory set can be considered to comprise Hess�s ereis-matic motility.

In evaluating the significance of the model in Fig. 3, which is central to modern ideas onthe integration of posture and movement, it is important to emphasize its sharp distinctionfrom the above-described ‘‘inside-out’’ approach of Sherringon and his colleagues. Forexample, the distinguished and imaginative German neurologist, Richard Jung (1911–1986), commented in an inspirational memoir that while he was most impressed withthe scientific rigor of the pre-World War II Oxford and Cambridge neuroscientists, hewas 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) consideredsingle facts (i.e., single-cell and isolated reflex results) only in their context with functionalsystems or in their significance for the organism’’ (i.e., the ‘‘outside-in’’ approach, asdefined above).

In his later years, Hess strongly advocated the need to integrate neurophysiology withpsychology, as had been the practice in the late 19th century (see below). For example, hislast book (Hess, 1962) and article (Hess & Fischer, 1973) are still relevant to psychologicalaspects of movement neuroscience.

Hess�s modern-day relevance for ideas on the integration of posture and movement areemphasized 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):

Fig. 3. Hess�s concept of the need for integration of goal-directed movement (Hess�s ‘‘teleokinetic motility’’) andits framework anticipatory and supportive postural support (‘‘ereismatic motility’’). Three medical studentsrepresent 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 posturalanticipatory set. Both (2) and (3) likely comprise Hess�s ‘‘ereismatic motility’’. The leap (goal) is achievedappropriately (a–c) when (1), (2) and (3) are highly coordinated. The leap is unsuccessful (d–f) when there is a lackof coordination between the three simultaneous needs of the performance. Jung redrew these sketches from anunpublished motion picture made by Hess in 1943 for use in his medical school teaching. Similar sketchesappeared in Hess (1965). Preceding still pictures from the motion picture were provided in Hess (1943). (FromField et al., 1960; Jung and Hassler, 1960, p. 904, Fig. 13. Reprinted with permission from The AmericanPhysiological Society.)


‘‘. . . (1) An intentional action is induced by a conscious drive and set. (2) The perception ofthe object in a goal-oriented movement3 and its memorized content contribute to the driveand motivation for prehension. (3) A manifold of innervation patterns characterizes theprobing 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 overtmovement.


steadily improving the performance by learning. (5) Disturbances of central coordinationare compensated adaptively.’’

Clearly, modern-day movement neuroscientists owe much to Hess!

4. Nikolai Bernstein (1896–1966)

In sharp contrast to Sherringon and Hess, Bernstein�s life and career had some tragicelements, particularly in his later years (Feigenberg & Latash, 1996). Sadly, it was onlyafter his death that he received the well-deserved, international accolades for movementneuroscience contributions that have made him pre-eminent in this field. These accoladesactually began the year of his death (Gelfand, Gurfinkel, Fomin, & Tsetlin, 1966) and havethereafter increased progressively (see, e.g., Bernstein, 2003; Bongaardt, 2001; Feigenberg,2004; Latash, 1998b, 2005; Latash & Turvey, 1996; Whiting, 1984). It is likely that hewould receive even more renown if his 1947 book, which was his most detailed expositionon movement neuroscience, was translated into English. Bernstein received a Stalin PrizeAward for this book in 1948. Wastefully, however, he was dismissed from his Moscowposition at the USSR Academy of Sciences in 1950 for his scientific viewpoints, particu-larly those that argued against some of Pavlov�s views. Bernstein�s reinstatement was ini-tiated after Stalin�s death in 1953. This was a relatively slow process, however, and it wasdue at least in part to his ill health. He was again reasonably active and certainly locallyinfluential throughout the early 1960s until his death in 1966 (for further details, seeFeigenberg, 2004; Feigenberg & Latash, 1996).

Bernstein was born into a stellar academic family, with parents and close relatives par-ticularly strong in the fine arts, humanities, medicine, and mathematics (Feigenberg &Latash, 1996). After completing his MD degree in 1919 at the University of Moscow inthe USSR and a 3-year stint in the Soviet army, he was given the opportunity in 1922to develop a motor control laboratory at the Moscow Central Institute of Labor. In the1920s, he was also affiliated with the Moscow Institute of Psychology. It is well to remem-ber that the Soviet regime was reasonably supportive of, albeit somewhat ambivalent,about the scientific intelligentsia and their research up to 1929 (see pgs. 72–122 in Vuci-nich, 1984). In this usually supportive, but always highly charged, environment Bernsteininitially flourished as an innovative investigator. ‘‘. . . At different times, he created labo-ratories of motor control at the Labor Protection Institute, All-Union Institute of Sports,Institute of Musical Science, All-Union Institute of Experimental Medicine, Institute ofNeurology (Academy of Medical Sciences), and the Moscow Institute of Prosthetic Appli-ances’’ (pg. 2 in Gurfinkel & Cordo, 1998). Bernstein seems unique in the extent of hisself-taught, eclectic approach to movement neuroscience. His remarkable insight intomovement found one of its fullest expressions in his essays on the origins and constructionof movements (Essays 3 and 4, respectively, in Latash & Turvey, 1996), which should beessential initial reading for trainees in movement neuroscience.

Bernstein�s research career spanned four decades (1922–1967), with his 1967 book pub-lished a few months after his death. His contributions to movement neuroscience extendedfor a much longer period, however, given the eventual 1991 (in Russian) and 1996 (in Eng-lish; Latash & Turvey, 1996) publication of a treatise on dexterity. This work was actuallyin galley proof form in 1950 when Bernstein was subject to particularly harsh treatmentfrom the Soviet power structure (Feigenberg & Latash, 1996). Similarly, Bernstein(1992) is a recapitulation of his career-long contributions to prosthetics. Also, a book


he wrote for publication in 1936 has only recently been published (Bernstein, 2003)4 inRussian, and its translation into English is not yet forthcoming.

Today, Bernstein is perhaps most widely known for his work on self-controlling biolog-ical systems. His work in this area, which must surely have been assisted by severalGerman precedents (Wiesendanger, 1997, 1998), paralleled that of Arturo Rosenblueth(1900–1970) and Norbert Wiener (1894–1964; see Wiener, 1948).

Among movement neuroscientists, Bernstein is also given great credit for combiningquantitative cyclographic kinesiology, in which area he made several technical improve-ments, with imaginative ideas on the neural control of movement. The latter were basedon evolutionary, fundamental neuroscience, and applied (clinical) neuroscience conceptsand findings. Indeed, he achieved a synthesis of movement neuroscience and biomechanicsthat has rarely been equaled subsequently. Bernstein employed this synthesis in a remark-able theoretical description of simple to complex movements in a wide variety of animalspecies (his Essay 3 in Latash & Turvey, 1996). Most of his work, however, involved quan-titative experimental and theoretical studies on the intact and brain-damaged human andin the development of prosthetic devices for the latter.

For the present purposes, it is sufficient to focus on three Bernstein concepts: movementas a ‘‘structure’’, his definition of motor coordination, and his hierarchical theory of motorcoordination.

The first of these concepts was developed, in part, in Bernstein (1929) and progressivelyrefined up to Bernstein (1940/1967), in which article it is stated that ‘‘. . . movements are notchains of details but structures which are differentiated into details; they are structurallywhole, simultaneously exhibiting a high degree of differentiation of elements and differingin 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 Bern-stein (1935), is his definition of motor coordination as ‘‘. . . overcoming excessive degrees offreedom of our movement organs, that is, turning the movement organs into controllablesystems . . . the degrees of freedom can be both kinematic and dynamic’’ (Essay 2, pg. 41 inLatash & Turvey, 1996).

The third concept also began to develop in Bernstein (1935/1967): ‘‘. . . there exist in thecentral 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 processof the movement in its entire course of time’’ (pg. 37 in Bernstein, 1967; i.e., the Englishtranslation of Bernstein, 1935). Later, in Bernstein (1947), he provided a far fuller andcomplete (V.S. Gurfinkel, personal communication) account of this concept with the ideathat ‘‘. . . 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 motorproblem 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 IvanPavlov (1849–1936). It was in galley proof form and ready for printing in 1936 by the State Publishing House ofBiological and Medical Literature. Bernstein insisted that it be withdrawn, however, because Pavlov�s death in1936 denied the latter, whom Bernstein respected greatly, the opportunity to counter Bernstein�s points (personalcommunication from Anatol Feldman; also pg. 249 in Feigenberg & Latash, 1996).


Gurfinkel and Cordo (1998) have summarized Bernstein�s ideas on the functional anat-omy of the above concept, which accommodated distributed and parallel processingthroughout the CNS, with all three subject to evolutionary pressures. Today, it is wellknown that the testing of this third concept led to major advances in current understand-ing of the neural control of locomotion. This began with work undertaken in Moscow inthe 1960s,5 which then spread to an international effort (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 Bernstein�s third concept in subse-quent delineation of the tripartite interactions between descending command signals, sen-sory feedback, and spinal pattern generators in an overall control program forlocomotion. Over 30 years ago, a relatively unread albeit important article by Gurfinkeland Shik (1973) proposed that the same Bernstein concept might mean that gravity-con-taining postures are organized and controlled similarly. Surprisingly, this provocative con-cept has commanded little subsequent attention. If Bernstein�s above three concepts areconsidered as one, however, then it is worth testing the possibility that posture (in allits forms) and movement are one and the same type of Bernsteinian structure. This ideahas yet to be tested, however.

It has been said with authority that ‘‘. . . Bernstein was highly familiar with the physi-ological and neurological literature, which is clearly evident in his unpublished (1936)book . . .’’ (pg. 2 in Gurfinkel & Cordo, 1998). In this now published book, Bernstein(2003)4 discussed Western work from Flourens to Lashley (V.S. Gurfinkel, personal com-munication). Nonetheless, a potential blot on Bernstein�s otherwise impeccable scholarlyescutcheon is that he did not always acknowledge the Western precedents to some ofhis ideas. For example, the above-mentioned Bewegungsformeln had precedents in thework of Liepman (1900), Brown (1916), Lashley (1917), Head (1920), and Wachholder(1928), and presumably several others. It seems likely, however, that Bernstein�s wealthof personally generated movement data and analysis provided the primary basis for hisBewegungsformeln proposition (Gurfinkel & Cordo, 1998). It is also surprising that Lash-ley�s work appears not to have influenced Bernstein, even though they came to many sim-ilar conclusions while using different methods. For example, Lashley�s (1929) observationson brain-injured rats and Bernstein�s on the kinemetics of human movements led to thesame conclusion, invariant goal achievement by variable means: i.e., the same motor taskaccomplished using different muscle and joints, an idea that dates back to at least Kohn-stamm (1901) and Foerster (1902). In other words, Lashley�s ‘‘principle of motor equiva-lence’’ (Lashley, 1933) and Bernstein�s ‘‘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 collaboratorsowed much to the ideas of Bernstein, even though they had virtually no direct contact with him (personalcommunication from G.N. Orlovsky). These gifted interdisciplinary movement neuroscientists were alsostimulated by the enlightened leadership and quantitative contributions of two mathematician/physicists, IsraelGelfand (1913–; see Berkinblit, Vasilev, & Shik, 1974) and Mikhail Tsetlin (1924–1966; see Editors� Obituary,1966), Institute of Problems of Information Transmission (formerly called the Institute of Biological Physics),USSR Academy of Sciences, Moscow, USSR.

Fig. 4. An important finding that emerged from testing a key Bernstein concept. This diagram summarizescurrent understanding of the control of vertebrate locomotion, and it owes much to the testing of ideas presentedby 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 cordpattern generators (CPGs), and sensory feedback. (The quoted material that follows is from pg. 5 in Grillner andWallen, 2004.) ‘‘The locomotor CPGs in the spinal cord are turned on from the brainstem via reticulospinalpathways. Disinhibition of the basal ganglia�s output to the mesencephalic (mesopontine, MLR) and diencephalic(DLR) locomotor centers results in increased activity in reticulospinal neurons (RS), which, in turn, cooperatewith 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 acidagonists combined with sensory input’’. (B) Gait transitions during locomotion. With increased activation of thelocomotor centers, the speed of locomotion increases. In quadrupeds, this also leads to shifts in interlimbcoordination, from walk to trot and, finally, to gallop. (C) An asymmetric activation of SR neurons gives rise toan asymmetric output of the left (L) and right (R) sides. This will result in a turning movement from one side tothe other. Note that the thrust of the Grillner and Wallen (2004) article was that it is misleading to draw adistinction between innate and learned movements across vertebrates, a viewpoint that extends on some thoughtspreviously espoused by Bernstein (see his Essay 3 in Latash and Turvey, 1996). (From Mori et al., 2004; Grillnerand Wallen, 2004, p. 5, Fig. 2. Reprinted with permission from Elsevier.)


‘‘principle of flexible coupling’’ of Albrecht Bethe (1872–1954: for review of this point, seeWiesendanger, 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 theneural basis for memory (pgs. 34–35 in Bernstein, 1967) while in the very same articlehe failed to acknowledge the existence of Lashley�s 1933 report!

In defense of Bernstein, he was certainly a victim of his times in the repressive Sovietregime that developed after 1929, when Stalin came into full power. This Soviet era(1921–53) was noted for its widespread (Vucinich, 1984), albeit with isolated exceptions(see pgs. 337–380 in Bailes, 1978), political intrusion into the conduct of science. As aresult, by the 1930s and subsequently, Bernstein presumably had few, if any, contacts withWestern scientists. Also, his work was mostly published in Russian journals and by Rus-sian publishing houses (Gurfinkel & Cordo, 1998), information that was rarely read in theWest. This is presumably one of the reasons that his Western peers ignored his work until


the mid 1960s. It remains puzzling, however, that the same fate did not befall the Russianwritings of Pavlov, which certainly created much interest in the West well before theawarding of his 1904 Nobel Prize. Another reason is that at least in English-speakingcountries up to the late 1960s, the ‘‘inside-out’’ approach to CNS control mechanismsfor posture and movement was far more favored than the ‘‘outside-in’’ strategy ofBernstein and Hess.

5. Summary thoughts

It should not be construed from the above that Sherrington�s ‘‘inside-out’’ approach tohis own experimental work was any less valuable than the ‘‘outside-in’’ approach of Hessand Bernstein. To the contrary, both are absolutely essential to advance movement neu-roscience, as is the case in all the biological sciences. By the early 20th century, however,it would have been extremely difficult for any single investigator or any single laboratoryto give equal emphasis to the two approaches. This problem grew progressively afterWWII, particularly with the advent of the techniques of molecular biology in the mid-to-late 1970s. To offset this problem, much emphasis has been placed in recent years onthe need for movement neuroscientists to (1) display an appreciation of and contributeto interdisciplinary research (interdisciplinarity), (2) have knowledge of comparativeadvances (interphyletic awareness), and (3) adopt transnational approaches to advancemovement neuroscience. The current state-of-the-play in these three areas is commentedupon below with due consideration to their historical precedents.

5.1. Interdisciplinarity

In the field 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 thefirst half of the 20th century, and then progressively increased up to the present day. IfBernstein�s interdisciplinary prowess had been understood in the West in the 1920–1950s, this process may well have been further accelerated. For example, the interdisciplin-ary composition of his own and his immediate successors� laboratories in the Academy ofScience of the USSR became much more visible to Western workers with the 1955 publi-cation of the Russian journal, Biofizika, and its English translation, Biophysics. In theWest, theoretical and applied advances in electrical and mechanical engineering and the1950s� step jump in computer science possibilities matched these developments afterWWII. These developments, together with a wide variety of international symposia onmovement neuroscience, had much to do with the post 1980s emergence in the West ofinterdisciplinary pre- and postdoctoral training programs that provide substantial interac-tions between the life and physical sciences. The power of this approach is exemplified inFig. 5, which shows how modern engineering control theory now contributes to a partic-ularly difficult problem in movement neuroscience: making sense of the wealth of intricatespinal circuitry involved in the elaboration of movement. Prochazka (1993) used this figureas an example of both ‘‘interphyletic awareness’’ (defined below) and how finite state (con-ditional), adaptive (self organizing) predictive control, neural networks, and fuzzy logicare now being used to understand spinal circuitry and advance prosthetics research (seealso Prochazka, 1996).

Fig. 5. An example of both the interface between neuroscience and engineering, and interphyletic awareness.The figure demonstrates the proposed use of finite state control in the elaboration of a stepping move-ment. Shown are schematics of a stick insect, locust, lobster, cat, active leg prosthesis, and a human witha functional electrical stimulation device. In each case, pairs of sensory variables are indicated when usedin a conditional way to initiate the swing phase of the step. That is, if displacement exceeds threshold andforce has declined below threshold, flexion is then initiated. Approximate positions of identified sensors(natural and artificial) are shown. (From Prochazka, 1993, p. 8, Fig. 1. Reprinted with permission fromIEEE).

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The above developments have precedents in the efforts of many scientists born in the19th century (including Hess and Bernstein to much greater extent than Sherrington).Also, the interface between movement neuroscience and psychology had a promising


start in the 19th century due to the efforts of the two founders of modern-day psychol-ogy: Wilhelm Wundt (1832–1920) and William James (1842–1910). They both were orig-inally trained as clinicians and then became active in physiology and its interface withpsychology. For movement neuroscience, the contributions of subsequent psychologistsborn in the 19th century were also profound: e.g., the work of Narziss Ach (1871–1946),Wilhelm Wirth (1872–1952), Robert Woodworth (1869–1962), 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 psychologyand movement neuroscience (for examples, see: Paillard, 1960, 1986; Whiting, 1984;Worringham, 1992). Sherrington�s role was somewhat different. He certainly championedthe study of both, but as relatively separate entities (see, e.g., Sherrington, 1940).

Despite the extent and quality of the effort of those who initially advanced the interfacebetween psychology and movement neuroscience, the current interaction between thesetwo areas is weaker than that between biological and physical science approaches, at leastin 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 significance formovement neuroscience of considering selected neural control mechanisms and strategiesthat are applicable to invertebrates, non-mammalian vertebrates, and mammalian verte-brates, including humans (for review: Pearson, 1993). Furthermore, a synthesis of‘‘inside-out’’ and ‘‘outside-in’’ approaches is more readily achievable in invertebrate andnon-mammalian vertebrate species than in mammalian vertebrates. Such a comparativeemphasis 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 (1830–1904), August Forel(1848–1931), Jacob von Uexkull (1864–1944), Albrecht Bethe (1872–1954), James Gray(1891–1975), Paul Weiss (1898–1989), and Erich von Holst (1908–1962).

Among the three subjects of this article, Bernstein seems to have been the most stronglyinfluenced by comparative findings. Sherrington and Hess may well have kept up with rel-evant comparative literature but they, themselves, wrote no articles with the interphyleticinterest and insight displayed in Essay 3 of Bernstein�s 1991/1996 book on dexterity (seepgs. 45–96 in Latash & Turvey, 1996). In retrospect, this is somewhat surprising consid-ering the respect Sherrington held for his comparative mentor, Walter Gaskell (see pgs.11–13 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, ionchannels, myosin isoforms, Ca2+ binding proteins) and cellular (e.g., mitosis, metabolicpathways, synaptic transmission) mechanisms than for the systems and organismic levelsof enquiry. Nonetheless, the case for the latter two is no less compelling. For example, ithas been particularly prominent in studies on the neural control of locomotion since atleast the early 1970s (for various aspects of this point, see Clarac, 1991; Delcomyn,1980; Grillner, Stein, Stuart, Forrsberg, & Herman, 1986; Herman, Grillner, Stein, & Stu-art, 1976; Stein, 1999; Stein, Grillner, Selverston, & Stuart, 1997; Stuart & McDonagh,


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 (1879–1916), had survived a 1916 planecrash and gone on with his stellar career (Fletcher, 1934), the British, and indeed WesternEuropean and North American, pre-WWII research on posture and movement may haveemphasized far more work on non-mammalian vertebrates and invertebrates (Stuart et al.,2001). Lucas sought to change ‘‘. . . the lack of interaction between evolutionary conceptsand physiological research . . . Lucas emphasized that �. . . the primary problem of compar-ative physiology. . .[is] the question to what extent and along what lines the functionalcapabilities 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 fieldbecoming progressively more transnational, with scientists often working for several yearsin foreign countries, attending international symposia in a wide variety of countries, andcontributing to the activities of organizations that promulgate international training andcollaboration. Such activities were also evident in the 19th century, but slowed in the firstpart of the 20th century by events leading to WWs I and II, and a post-WWII (if not post-WWI) seeming aversion in English-speaking countries to the rich tradition of Germanmovement neuroscience (Wiesendanger, 1997, 1998).

Sherrington profited greatly from the steady influx of Rhodes Scholars and other like-motivated 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 bio-medical area to which they were subsequently attracted (e.g., pgs. 92–94 in Eccles &Gibson, 1979). He had great empathy for Canada and the USA, which countries he visi-ted several times, and even came close to accepting a position at the University of Tor-onto in the early 1900s (pgs. 21–22 in Eccles & Gibson, 1979). Sherrington�s laboratoryat 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 ortwo of discussion. In most cases, it appears that both they and Sherrington enjoyed andprofited from their exchanges (e.g., pg. 88 in Granit, 1966), an exception being a visit byHess in �1917–1918 (pg. 413 in Hess, 1963). In return, Sherrington traveled widelythroughout Europe, including a 1914 trip to St. Petersburg to see Pavlov (pg. 56 inBrazier, 1959).

In view of the above, it is bothersome that Sherrington gave no credit to, nor evencited, the seminal findings on human spinal reflexes of the German physiologist, PaulHoffmann (1884–1962). These findings included the ‘‘Eigenreflex’’, which Hoffmannproposed was a monosynaptic pathway (Hoffmann, 1910, 1922, 1934). This was laterproven, and it became known as the ‘‘H-reflex’’ in Hoffman�s honor (for further details,see Jung, 1992; Wiesendanger, 1997). This blind spot of Sherrington is even moretroubling because Hoffmann worked with him at the University of Liverpoolin �1912, at least two years after Hoffman�s first major article on spinal reflexes(Hoffmann, 1910).

It is also puzzling why Sherrington paid virtually no attention to the ‘‘outside-in’’ fin-dings and viewpoints of outstanding German movement neuroscientists like Liepman


(1900), Kohnstamm (1901), Foerster (1902), and later, von Holst (1932).6 In my opinion,Sherrington�s 1885-onwards, outspoken opposition to Prussian militarism (Granit, 1966;Eccles & Gibson, 1979) was not a factor. Note, for example, Granit (1966; pg. 60) com-ment that ‘‘. . . Important studies on the spinal animal were performed in Goltz�s labora-tory in the nineties [i.e., 1890s] and Sherrington visited it several times’’. Rather, it wouldappear that Sherrington�s adherence to ‘‘inside-out’’ findings in movement neuroscienceoutweighed his intrinsic transnationalism!

In sharp contrast to Sherrington, Hess had limited international opportunities despitehis 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 trainforeign workers. This was also to the detriment of international movementneuroscience.

It remains unknown to Western workers if Bernstein would have liked to interact withhis international peers. Certainly, both he and they would have profited from the one-on-one exchange of ideas. The power structure of his country throughout his adult life, how-ever, did not favor internationalism in science, thereby diminishing the influence of USSRscience at the international level, and reducing the visibility of innumerable outstandingscientists, including Bernstein.

In final summary, modern movement neuroscience stands on the shoulders of manygiants, who were trained in several countries and in several different fields. 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 willconvince the next generation of movement neuroscientists that interdisciplinarity, inter-phyletic awareness, and transnationalism can continue to open new doors in this ever-intriguing field.

Acknowledgements

Presented, in part, as oral presentations at (1) the international symposium HigherNervous Control of Posture and Locomotion: Parallel and Centralized Control Systems

(organizer/director, Shigemi Mori), National Institute for Physiological Sciences, Oka-zaki, Japan, March 18–20, 2001 and (2) the 7th Motor Control and Human Skill Confer-

ence (convener, Jan Piek), Freemantle, Western Australia, February 3–7, 2005. Note thatthe former symposium was followed by a research volume: Mori, S., Stuart, D.G., andWiesendanger, M. (2003). Brain mechanisms for the integration of posture and movement,Volume 143, Progress in Brain Research. Amsterdam: Elsevier. I would like to thankRoger Enoka, Sten Grillner, Shigemi Mori, Mark Latash, and Mario Wiesendangerfor reviewing a draft of this article. Understandably, their viewpoints do not necessarilycoincide with those expressed in this report. Also thanked are Patricia Pierce for her edi-torial assistance, Nga Nguyen for her library research, and Mario Wiesendanger andWulfila Gronenberg for their help with the translated titles of several German articlesand books.

6 The published contributions of Erich von Holst (1908–1962) span 1932 to his untimely death in 1962. Muchof his work is summarized in a two-volume collection (von Holst, 1969).


References

Adrian, E. T. (1966). Thomas Graham Brown. Biographical Memoirs of Fellows of the Royal Society, 12, 23–33.Akert, K. (Ed.). (1981). Biological order and brain organization. Selected works of W.R. Hess. Berlin: Springer.Akert, K. (1999). Walter Rudolf Hess (1881–1973) and his contribution to neuroscience. Journal of the History of

the Neurosciences, 8, 248–263.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, 45–53.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. 249–270). 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 biodynamicsof walking, running and jumping]. Moscow: Physical Culture and Sport (For English translation, see chap. IIIin Bernstein, 1947).

Bernstein, N. A. (1935/1967). Problema vzaimootnosheniya koordinazii i lokalizazii [The problem of theinterrelation of coordination and localization]. Arkhiv Biologicheskikh Nauk, 38, 1–38 (For Englishtranslation, 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 fiziologii 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. 59–84). 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. 1–58). Washington, DC: AmericanPhysiological Society.

Bretag, A. (1983). Who did invent the intracellular microelectrode? Trends in Neuroscience, 6, 365.Brown, T. G. (1916). Die Reflex Funktionen des Zentralnervensystems mit besonderer Berucksichtigung der

rhythmischen Tatigkeiten bei Saugetieren [Reflex functions of the central nervous system with particularconsideration of rhythmic activities in mammals]. Ergebnisse der Physiologie, 15, 480–490.

Clarac, F., Humphrey, D. R., & Freund, H. J. (1991). How do sensory and motor signals interact duringlocomotion? A comparative point of view. In Dahlem workshop on motor control: Concepts and issues

(pp. 199–201). Chichester, UK: John Wiley and Sons.Creed, R. S., Denny-Brown, D., Eccles, J. C., Liddell, E. G. T., & Sherrington, C. S. (1932). Reflex activity of the

spinal cord. Oxford, UK: Clarendon Press (Note: This book�s chap. 7 [p. 55] was written solely by Sherringtonand it may be considered ‘‘. . . his last purely scientific writing and . . . the crowning achievement of the OxfordSchool . . .’’ [pages 65–66 in Eccles and Gibson, 1979]).

Delcomyn, F. (1980). Neural basis of rhythmic behavior in animals. Science, 210, 492–498.Eccles, J. C., & Gibson, W. C. (1979). Sherrington: His life and thought. Berlin: Springer-Verlag.Editors� Obituary (1966). Mikhail, L�Vovich Tsetlin. Biophysics, 11, 1080–1082 (Translation from the Russian

journal Biophysika).Feigenberg, I. M. (2004). Nikolai Bernstein. Ot refleksa k modeli buduschego [Nikolai Bernstein. From the reflex

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. 247–275). Mahwah, NJ: Lawrence Erlbaum.Fletcher, W. M. (Ed.). (1934). Keith Lucas. Cambridge, UK: Heffer (Note: Originally written in 1916; published

after Fletcher�s 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 ofcoordination – an analysis of movement disorders occurring with diseases of the central nervous system andtheir rational therapy]. Jena, Germany: Fischer.

Fulton, J. F. (1955). A textbook of physiology. Philadelphia: W.B. Saunders.


Gelfand, I. M., Gurfinkel, V. S., Fomin, S. V., & Tsetlin, M. L. (1966). Models of the structural-functionalorganization of certain biological systems. Moscow: Academy of Science of the USSR [in Russian] (Englishtranslation by C. R. Beard and edited by J. S. Barlow, Boston: MIT Press).

Gillespie, C. C. (Ed.). (1973). Lucas, Keith. Dictionary of Scientific Biography (Vol. VIII, pp. 532–535). New York:Charles Scribner�s 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, 773–790.

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, 3–12.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, 206–209 (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, 152–155.Gurfinkel, V. S., & Cordo, P. J. (1998). The scientific legacy of Nikolai Bernstein. In M. L. Latash (Ed.), Progress

in motor control - Bernstein’s traditions in movement studies (pp. 1–19). Champaign, IL: Human Kinetics.Gurfinkel, 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. 217–234). 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, 199–223.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, 441–448, 537–541. (For English translation, see chap. 15 in Akert,1981).

Hess, W. R. (1943). Teleokinetische und ereismatische Kraftesysteme in der Biomotorik [Teleokinetic andereismatic mechanisms and biomotor functions]. Helvetica Physiologica Acta, 1, C62–C63 (For Englishtranslation see chap. 16 in Akert, 1981).

Hess, W. R. (1949). Das Zwischenhirn. Syndrome, Localisationen, Funktionen [Autonomic and extrapyramidalfunctions]. 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, 400–423.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 ananalysis of concrete examples]. Archiv far Psychiatrie und Nervenkrankheiten, 207, 33–44.

Hess, W. R., Burgi, S., & Bucher, V. (1946). Motorische Funktionen des Tektal- und Tegment-algebeites [Motorfunctions of tectal and tegmental areas]. Monatsschrift fur Psychiatrie und Neurologie, 112, 1–52 (For Englishtranslation, 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, 109–118.

Hildebrand, J. G., & Shepherd, G. M. (1997). Mechanisms of olfactory discrimination: Common principlesacross phyla. Annual Review of Neuroscience, 20, 595–631.

Hoffmann, P. (1910). Beitrage zur Kenntnis der menschlichen Reflexe mit besonder Berucksichtigung derelektrischen Erscheinungen [Contributions to the knowledge of human reflexes with particular reference toelectrical phenomena]. Archiv fur Anatomie, Physiologie und wissenschaftliche Medicin, 1910, 223–246.

Hoffmann, P. (1922). Die Eigenreflexe (Sehnenreflexe) menschlicher Muskeln [The monosynaptic reflexes (tendonreflexes) of human muscles]. Berlin: Springer-Verlag.

Hoffmann, P. (1934). Die physiologischen Eigenschaften der Eigenreflexe [The physiological properties ofmonosynaptic reflexes]. Ergebnisse der Physiologie, 34, 15–108.

Hommel, B. (2003). Planning and representing intentional action. The Scientific World Journal, 3, 593–608.


Hommel, B., Ridderinkof, K. R., & Theewes, J. (2002). Cognitive control f attention and action: Issues andtrends. Psychological Research, 66, 215–219.

Hoyle, G. (1983). Origins of intracellular microelectrodes. Trends in Neuroscience, 6, 163.Jung, R. (1981). Walter R. Hess (1881–1973) [Ditto; an obituary]. Reviews of Physiology, Biochemistry and

Pharmacology, 88, 1–22.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. 477–511). Boston: Birkhauser (First published byMIT 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. 863–927). Washington, DC: AmericanPhysiological Society.

Kohnstamm, O. (1901). Uber Koordination, Tonus und Hemmung [On coordination, muscle tone andinhibition]. Zeitschrift fur Diat und Physikalische Therapie, 4, 112–122 [in German].

Lashley, K. S. (1917). The accuracy of movement in the absence of excitation from a moving organ. American

Journal of Physiology, 43, 169–194.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, 1–42.Latash, M. (1998a). Neurophysiological basis of movement. Champaign, IL: Human Kinetics.Latash, M. L. (Ed.). (1998b). Progress in motor control – Bernstein’s traditions in movement studies. Champaign,

IL: Human Kinetics.Latash, M. L. (2005). A new biography of Nikolai Bernstein. Motor Control, 9, 1–2.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, 135–222.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, 15–44, 102–132, 188–197.Liddell, E. G. T. (1952). Charles Scott Sherrington: 1857–1952. Obituary Notices of Fellows of the Royal Society,

8, 241–270.Loeb, G. E. (1987). Hard lessons in motor control from the mammalian spinal cord. Trends in Neuroscience, 10,

108–113.Lucas, K. (1909). The evolution of animal function. Science Progress, 20 cent., London, 3, 472–483.Lundberg, A. (1969). Reflex control of stepping Nansen memorial lecture to Norwegian Academy of Sciences.

Oslo: Universitetsforlarget.Lundberg, A., & Phillips, C. G. (1973). T Graham Brown�s film on locomotion in the decerebrate cat. Journal of

Physiology (London), 231, 90–91.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, 13–27.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. 167–1708). Washington, DC: AmericanPhysiological 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. 415–441). Ordrecht: Martinus Nijhoff Publishers.Pearson, K. G. (1993). Common principles of motor control in vertebrates and invertebrates. Annual Review of

Neuroscience, 16, 265–297.Philippson, M. (1905). L�autonomie et la centralisation dans le systeme nerveux des animaux: etude de

physiologie experimentale et compare [Autonomy and centralization in the nervous system of animals: Studiesin experimental and comparative physiology]. Brussels: Falk.


Porter, R., & Lemon, R. (1993). Corticospinal function and voluntary movement. New York: Oxford UniversityPress.

Prochazka, A. (1993). Comparison of natural and artificial movement control of movement. IEEE Transactions

on Rehabilitation Engineering, 1, 7–17.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. 89–127).New York: Oxford University Press.

Prus, J. (1898). Ueber die Leitungsbahnen und Pathogenese der Rindenepilepsie [Pathways and pathogenesis ofcortical epilepsy]. Wiener klinische Wochenschrift, 11, 857–863.

Rushworth, M. F., Walton, M. E., Kennerley, S. W., & Bannerman, D. M. (2004). Action sets and decisions inthe medial frontal cortex. Trends in Cognitive Science, 8(9), 410–417.

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. HughlingsJackson Lecture. Brain, 54, 1–48.

Sherrington, C. S. (1932). Inhibition as a coordinative factor. Nobel Lecture, December 12, 1932. In Les Prix

Nobel (pp. 278–289). Stockholm: Nobel Foundation.Sherrington, C. S. (1940). Man on his nature. The Gifford lectures, Edinburgh, 1937–38. Cambridge, UK:

Cambridge University Press.Shik, M. L., Severin, F. V., & Orlovsky, G. N. (1966). Organization of locomotor synergism. Biophysics, 11,

1011–1019.Stein, P. S. G. (1999). Central pattern generators and interphyletic awareness. Progress in Brain Research, 123,

259–271.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. 277–284). 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. 95–105). Bethesda, MD: Society forNeuroscience.

Stuart, D. G., & McDonagh, J. C. (1998). Reflections on a Bernsteinian approach to systems neuroscience: Thecontrolled locomotion of high-decerebrate cats. In M. L. Latash (Ed.), Progress in motor control – Bernstein’s

traditions in movement studies (pp. 21–49). 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 inmovement science (pp. 317–374). Champaign, IL: Human Kinetics.

Swazey, J. P. (1969). Reflexes and motor integration: Sherrington’s concept of integrative action. Cambridge, MA:Harvard University Press.

Vogt, C., & Vogt, J. (1906–1907). Zur Kenntnis der elektrisch erregbaren Hirnindengebiete bei den Saugetieren[About the actual knowledge of the electrically excitable cortical areas in mammals]. Journal fur Psychologieund Neurologie, 8, 277–456.

Vogt, C., & Vogt, J. (1919–1920). Allegemeinere Ergebnisse unserer Hirnforschung [General results from ourbrain research]. Journal fur Psychologie und Neurologie, 25, 279–461.

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, 547–588.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 intoEnglish: (1973). Coral Gables, FL, USA: Hillsdale).

Vucinich, A. (1984). Empire of knowledge: The Academy of Sciences of the USSR (1917–1970). Berkeley, CA:University of California Press.

Wachholder, K. (1928). Willkurliche Haltung und Bewegung [Volitional standing and moving]. Ergebnisse der

Physiologie, 26, 568–775.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.


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. 103–124). Basel: S.Karger AG.

Wiesendanger, M. (1998). Bernstein�s principle of equal simplicity and related concepts. In M. L. Latash (Ed.),Progress in motor control – Bernstein’s traditions in movement studies (pp. 105–125). Champaign, IL: HumanKinetics.

Wilson, S. A. K. (1924). The old motor system and the new. Archives of Neurology and Psychiatry, 11, 385–404.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. 807–825). Amsterdam: Elsevier B.V.

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