JEB Classics 4411 THE CENTRAL NERVOUS peripheral sense organs in the musculature JEB Classics is an occasional CONTROL OF INSECT or the integument. Charles Sherrington’s column, featuring historic work on vertebrate proprioceptors publications from The Journal of FLIGHT (Sherrington, 1906) gave the model a Experimental . These plausible mechanism. It was accepted that articles, written by modern experts some degree of intrinsic central patterning in the field, discuss each classic must be present in fish and amphibian paper’s impact on the field of locomotion (e.g. Lissman, 1946a,b) but biology and their own work. A proprioceptive feedback was thought to be PDF of the original paper is essential for the generation of motor output available from the JEB Archive in rhythmic locomotion. Erich von Holst (http://jeb.biologists.org/). saw an interplay between peripheral and central control (von Holst, 1935) and later, with newly in vogue, this was named the Reafference Principle by Mittelstaedt and von Holst, in which they addressed what happens in the central nervous system where sensory feedback from muscles impacts motor output (Mittelstaedt and von Holst, 1950). By introducing cybernetic to concepts of central nervous function they went beyond prevalent simplistic reflex concepts.

There was good neurophysiological evidence for central pattern generation A copy of Wilson’s 1961 classic paper ‘The dating back to the classic work of E. central nervous control of flight in a locust’ s Adrian who showed that isolated ventral can be accessed from nerve cords of a water beetle Dytiscus http://jeb.biologists.org/cgi/content/abstract marginalis produced rhythmic output /38/2/471 (Adrian, 1931). Similarly Peter Miller c showed that respiratory rhythms in the It seems that the workings of the human migratory locust do not depend on phasic mind thrive on polarities; us vs them for i input (Miller, 1960). example, or good vs evil, preformation vs epigenesis, nature vs nurture. But reality Technical advances in electrophysiology generally lies between the poles. So it is during post-World War II decades, s with the history of ideas about the control especially the refinement of the cathode ray of rhythmic locomotion, a function that is oscilloscope, made extracellular recording the very essence of animaldom. The a powerful tool for the neural basis of polarity in the present case is the issue of behaviour, and Wilson was poised to make s peripheral vs central control of rhythmic the most of these new and powerful locomotion. techniques. Some 20 years after Gray’s Croonian Lecture, Wilson’s paper provided Why is Don Wilson’s classic 1961 paper a evidence to reject the proprioceptive chain a pivot point in the history of this question? reflex model by rigorously demonstrating Before 1961 the predominant concept was that the full motor pattern of locust flight l that rhythmic locomotor behaviour, such as could be generated by fully deafferented swimming, flying or breathing, is thoracic ganglia, which could not receive maintained and regulated by a chain of the inputs required by the proprioceptive reflexes, that proprioceptive feedback at chain model.

C one instant shapes motor output at the next. The evidence came primarily from direct Don Wilson, a student of one of the observation of normal and modified motion greatest comparative neurobiologists, the in numerous metamerically segmented late Ted Bullock, had already established a animals, especially annelids, arthropods reputation for comparative neurobiology and fish. The concept of peripheral control with studies on sea anemonies, annelids

B of rhythmic locomotion was epitomized by and octopus before he joined Torkel Weis Sir James Gray – a founder of The Journal Fogh’s lab in the Zoophysiological Institute of Experimental Biology – in his Croonian at the University of Copenhagen. Weis

E Lecture to the Royal Society (Gray, 1939). Fogh had been pursuing a meticulous His model proposed that the muscular analysis of flight mechanics in the desert rhythms of locomotion that issue from the locust Schistocerca gregaria and had

J central nervous system are controlled and developed an experimental system in which maintained by rhythmical input from a tethered locust could be induced to fly

THE JOURNAL OF EXPERIMENTAL BIOLOGY JEB Classics 4412 persistently in the controllable output of a could be taken to imply a purely reflex but also gave direct experimental support to wind tunnel and to maintain strictly integration of the flight motor. the ethological concept of the genetically coordinated movements of the two pairs of determined fixed action pattern that is wings over long time periods (Weis Fogh, The next series of operations were crucial. released by appropriate input (Hoyle, 1956a). Having developed the flight They opened the way to a new paradigm 1980). Thus it can be argued that Wilson’s system, Weis Fogh explored aspects of for they showed that total removal of the search for the neurophysiological basis of sensory input relevant to flight and, sources of periodic input did not abolish rhythmic locomotor behaviour led directly reflecting the general paradigm of the time, patterned motor output. Deafferentation to the of as a developed a model consistent with the idea slowed the flight sequence but the cycle discrete, if eclectic, discipline. that proprioceptive feedback generated the otherwise resembled the normal intact cycle of motor commands, but the search pattern closely. If flight was not maintained A note on Don Wilson himself: His writing for the critical phasic input was unavailing by reflex feedback then the motor pattern was of a piece with the man; he was spare, (Weis Fogh, 1956b). Wilson and Weis must have originated within the ganglia. muscular, and entirely without pretence. Besides his intensive research activity he Fogh then began a fruitful The requisite mechanism was certainly there, for Wilson showed the presence of ‘a was actively engaged in the social neurophysiological collaboration (Wilson multiplicity of oscillators’ in the flight movements of the sixties; his equipment at and Weis Fogh, 1962) that led to the control system. Thus he proposed that ‘the Berkeley included a bullhorn with which to publication of Wilson’s classic paper. First basic co-ordination of flight is an inherent address student rallies. He was a skilled they built a detailed picture of neural function of the central nervous system but and graceful rock climber. I had the output to the flight muscles, and then that peripheral feedback loops influence pleasure of making an easy climb with him compiled a catalog of phasic and tonic the frequency of operation and details of in Yosemite not long before his untimely sensory inputs to the thoracic ganglia. They pattern.’ death in 1970 at 36 years of age by concluded that the input could potentially drowning in a rafting accident on the ‘allow of a purely reflex integration of the A host of subsequent studies on annulates notorious Middle Fork of the Salmon River flight pattern’. So far the model was and vertebrates, too many to mention in Idaho. As with Mozart, one can only orthodox feedback-based. here, have confirmed Wilson’s conclusion; wonder what he might have achieved given the control of numerous rhythmic a longer life. Then came a series of skilful experiments behaviours, not only locomotion, proved in which Wilson successively eliminated to be at neither pole, neither peripheral 10.1242/jeb.02592 sensory input to the thoracic ganglia while input nor central programs alone. Instead, John S. Edwards recording motor output in increasingly cut- central pattern generators are modulated University of Washington away preparations in order to evaluate the by tonic and phasic sensory feedback, [email protected] influence of sensory feedback (Fig. 1). which serves to adapt motions to the real First the head and suboesophageal ganglion heterogeneous world of errors in References were removed and, despite the absence of genetically determined motor programs, of Adrian, E. D. (1931). Potential changes in the the wind-sensitive head sensory hairs that bumps, turbulence, injury and aging. isolated nervous system of Dytiscus marginalis. normally activate flight after the locust Wilson’s breakthrough paper was followed J. Physiol. 72, 132-151. jumps, normal though slowed flight could by another important contribution with a Ewer, D. W. (1953). The anatomy of the be initiated by means of the tarsal reflex clear demonstration that the bifunctional nervous system of the tree locust, Acanthaeris and maintained in an airstream. Following muscles that effect two distinct patterns, ruficornis. I. The adult metathorax. Arm. Natal on with a series of further operations in walking and flying, in the locust were Mus. 13, 467-481. under independent control and thus not Ewer, D. W. (1954). The anatomy of the which thoracic connectives in the ventral nervous system of the tree locust, Acanthaeris nerve cord, and sensory nerves were subject to a fixed set of connexions (Wilson, 1962). His view of the role of ruficorms. II. The adult mesothorax. J. Ent. Soc. selectively severed built a catalogue of the S. Afr. 17, 27-37. numerous sources of sensory input that sensory feedback in diverse behaviour Gray, J. (1939). Croonian Lecture. Aspects of patterns is summed up in a paper animal locomotion. Proc. Roy. Soc. B 128, 28- completed shortly before his death 62. (Wilson, 1972), in which he emphasizes Hoyle, G. (1980). Neural mechanisms. In Insect the corrective role of sensory feedback: Biology in the Future (ed. M. Locke and D. S. ‘the importance of sensory feedback in Smith), pp. 635-665. Academic Press. behavior patterns appears not to lie in the Lissman, H. W. (1946a). The neurological basis cueing of sequences but rather in the of the locomotory rhythm in the spinal dogfish correction of errors inherent in genetically (Scyllium canicula, Acanthius vulgaris). I. Reflex behaviour. J. Exp. Biol. 23, 143-161. determined motor programs’. Recognition Lissman, H. W. (1946b). The neurological basis that neurohormonal modulation of central of the locomotory rhythm in the spinal dogfish circuits added a further complex layer to (Scyllium canicula, Acanthius vulgaris). II. The the control of rhythmic behaviour effect of deafferentation. J. Exp. Biol. 23, 162- Fig. 1. Diagram of a dissection of Schistocerca. emerged later but was built on the 176. The dorsal tegmentary nerve supplying the head foundation concept of the central pattern Marder, E. and Calabrese, R. L. (1996). hairs is indicated as a solid line. The nerves and generator (Marder and Calabrese, 1996). Principles of rhythmic motor pattern generation. Physiol. Rev. 76, 687-717. ganglia are numbered as in Ewer (Ewer, 1953; It may be simplistic to cite one paper as Miller, P. L. (1960). Respiration in the desert Ewer, 1954). rn indicates recurrent nerve. The locust. I. The control of ventilation. J. Exp. Biol. positions of the dorsal longitudinal muscles and the fons et origo of an entire field but, as 37, 224-236. elevator muscles are indicated. The controller Graham Hoyle has pointed out, Wilson’s Mittelstaedt, H. and von Holst, E. (1954). depressors lie behind the elevators rn this view. paper not only established the role of Reafferenzprincip und Optomotorik. Zool. Anz. Many non-flight structures are omitted. central patterning in rhythmic behaviour 151, 253-259.

THE JOURNAL OF EXPERIMENTAL BIOLOGY JEB Classics 4413 Sherrington, C. S. (1906). On the locust (Schistocerca gregaria ). Phil. Trans. B the thorax of grasshoppers. J. Exp. Biol. 39, 669- proprioceptive system, especially in its reflex 239, 459-510. 677. aspect. Brain 29, 467-482. Weis Fogh, T. (1956b). Biology and physics of Wilson, D. M. (1972). Genetic and sensory von Holst, E. (1935). Die Koordination der locust flight. IV. Notes on sensory mechanisms mechanisms for locomotion and orientation in Bewegung bei den Arthropoden in Abhangigkeit in locust flight. Phil. Trans. B 239, 553-584. animals. Am. Sci. 60, 358-365. von zentralen und peripheren Bedingungen. Biol. Wilson, D. M. (1961). The central nervous Wilson, D. M. and Weis Fogh, T. (1962). Rev. 10, 2234-2261. control of locust flight. J. Exp. Biol. 38, 471- Patterned activity of co-ordinated motor units, Weis Fogh, T. (1956a). Biology and physics of 490. studied in flying locusts. J. Exp. Biol. 39, 643- locust flight. II. Flight performance of the desert Wilson, D. M. (1962). Bifunctional muscles in 667.

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