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ARTICLE IN PRESS JID:CRASS3 AID:2439 /FLA [m3+; v 1.59; Prn:29/03/2006; 15:59] P.1 (1-13) 1 53 2 54 3 C. R. Biologies ••• (••••) •••–••• 55 4 http://france.elsevier.com/direct/CRASS3/ 56 5 57 6 Neurosciences 58 7 59 8 The physiological construction of the neurone concept (1891–1952) 60 9 61 10 Jean-Gaël Barbara 62 11 63 12 ‘Recherches épistémologiques et historiques sur les sciences exactes et les institutions scientifiques’ (REHSEIS), CNRS UMR 7596, 64 13 ‘Neurobiologie des processus adaptatifs’, CNRS UMR 7102, université Pierre-et-Marie-Curie, 65 14 7, quai Saint-Bernard, case 14, 75252 Paris cedex 05, France 66 15 Received 15 November 2005; accepted after revision 15 February 2006 67 16 68 17 69 Presented by J.-M. Blengino 18 70 19 71 20 72 21 Abstract 73 22 Steps in the physiological construction of the neurone concept are described. Early ideas on the function of the nerve cell led 74 23 to later polemics on the neurone doctrine and the speculative attitude of histophysiology. Researches of Sherrington and Adrian 75 24 emerged from a specific British context, and confronted American oscillography and Berger rhythm. At the end of various polemics, 76 25 the neurone was constructed by the intracellular technique and the use of concepts borrowed from other sub-disciplines. Analysis 77 26 of these paths demonstrates underlying disciplinary interactions as essential factors. To cite this article: J.-G. Barbara, C. R. 78 27 Biologies ••• (••••). 79 28 2006 Académie des sciences. Published by Elsevier SAS. All rights reserved. 80 29 Résumé 81 30 Construction physiologique du concept de neurone (1891–1952). Les étapes de la construction physiologique du concept de 82 31 neurone sont décrites. Les idées initiales sur la fonction de la cellule nerveuse aboutissent aux polémiques sur la théorie du neurone 83 32 et les prétentions spéculatives de l’histophysiologie. Les programmes de recherche de Sherrington et Adrian émergent d’un contexte 84 33 britannique spécifique et se confrontent à l’oscillographie américaine et au rythme de Berger. Au terme de polémiques multiples, le 85 34 neurone se constitue par la technique intracellulaire et l’incorporation de concepts issus d’autres sous-disciplines. L’analyse de ces 86 35 voies démontre les interactions entre disciplines sous-jacentes comme des facteurs essentiels. Pour citer cet article : J.-G. Barbara, 87 36 C. R. Biologies ••• (••••). 88 37 2006 Académie des sciences. Published by Elsevier SAS. All rights reserved. 89 38 Keywords: Neurone concept; Disciplines; Neurone doctrine; Histophysiology; Electrophysiology 90 39 91 Mots-clés : Concept de neurone ; Disciplines ; Théorie du neurone ; Histophysiologie ; Électrophysiologie 40 92 41 93 42 94 43 1. Introduction tween nerve fibres and the soma of nerve cells. The 95 44 UNCORRECTEDneurone conceptPROOF of Heinrich Waldeyer (1836–1921) [1] 96 45 The classical presentation of the neurone doctrine de- was established upon topography of sub-cellular ele- 97 46 scribes main achievements and controversies over dif- ments such as dendrites, somata, nuclei, fibrils, and ax- 98 47 99 ferent techniques and interpretations of relations be- ons (1891). However, the idea of polarized functional 48 100 interactions between cell parts allowed a new interpre- 49 101 E-mail address: 50 [email protected] (J.-G. Barbara). tation of the neurone, which emphasized the role of the 102 51 1631-0691/$ – see front matter 2006 Académie des sciences. Published by Elsevier SAS. All rights reserved. 103 52 doi:10.1016/j.crvi.2006.03.014 104 ARTICLE IN PRESS JID:CRASS3 AID:2439 /FLA [m3+; v 1.59; Prn:29/03/2006; 15:59] P.2 (1-13) 2 J.-G. Barbara / C. R. Biologies ••• (••••) •••–••• 1 soma in the propagation of nerve impulse. The success parts of nerve cells, although anatomical and functional 53 2 of the neurone doctrine promoted further physiologi- continuity between them was assumed. Rather, cells 54 3 cal speculations with marked differences among Eu- were described as enlarged portions of fibres, unipolar, 55 4 ropean countries. The legitimacy of histology to com- bipolar or multipolar, depending on the number of fibres 56 5 ment on the function of nerve cells seemed to over- in contact [2]. Nerve cells were not considered neces- 57 6 lap that of physiology. Conversely, physiology inter- sary for the transmission of the nervous impulse through 58 7 acted with histology, when this discipline was able to ganglia, since most anatomists considered at least that 59 8 adopt, criticize and even rectify the neurone concept. some fibres were uninterrupted in crossing these struc- 60 9 However, physiologists differed in this attitude, espe- tures. However, multipolar nerve cells in the anterior 61 10 cially between Britain and France. A comparison of horn of spinal cord were seen as necessary connecting 62 11 physiological conceptions on nerve cells within partic- devices between sensory and motor impulses. In 1857, 63 12 ular contexts of reception and rectification of the neu- Claude Bernard (1813–1878) concluded: 64 13 rone doctrine is needed. Our goal is to establish how 65 14 different research programmes devoted to the nervous “D’après ce qui précède, on voit que les cellules 66 15 system emerged at the beginning of the 20th century. seraient tantôt l’origine des fibres nerveuses, tantôt 67 16 An implicit reference to the central role of the nerve des organules placés sur le trajet de ces fibres. On 68 17 cell in some programmes determined original paths in pourrait dans ces cas considérer les tubes comme 69 18 the careers of Charles Sherrington (1857–1952) and les conducteurs du système nerveux, dont les cel- 70 19 Edgar Douglas Adrian (1889–1977). British physiology lules seraient l’agent élaborateur ou collecteur.”[2 71 20 was more inclined than French or American to local- (pp. 127–128)]1 72 21 ize nervous properties in neuronal elements. Numerous 73 22 polemics arose between axonology, electroencephalog- Occasionally, some histologists and physiologists 74 23 raphy, and neurophysiology. Occasionally, they deter- criticized this simplistic view. The discovery by Louis- 75 24 mined heuristic syncretisms between distant research Antoine Ranvier (1835–1922) of the T structure of 76 25 77 programmes. These events finally led to the modern sensory neurones in dorsal root ganglia [3] established 26 78 neurone concept developed with intracellular recordings a new type of contact between fibres and nerve cells, 27 (1952). This paper aims at examining old rooted episte- 79 where the soma could neither be seen necessarily as a 28 mological problems that paralleled the construction of 80 collector, nor receptor. The British physiologist Michael 29 the neurone concept from 1891 to 1952. An emphasis is 81 Foster (1836–1907) also criticised the role assigned to 30 put on the role of pre-established scientific disciplines, 82 the soma. 31 sub-disciplines and their relations as important factors 83 32 contributing to the genesis of epistemological conflicts. 84 “[...] reflex action is carried on undoubtedly through 33 Conversely, resolutions and synthesis of different ap- 85 cells. But it does not follow that a cellular mechanism 34 proaches are seen as major determinants of conceptual 86 is essential in the sense at all events that the nuclei of 35 advances and redefinitions of disciplines. Therefore, the 87 the cells have anything to do with the matter [...]” [4] 36 history of the neurone concept gives us the opportu- 88 37 nity to ask some intermingled problems between social 89 Such criticisms were both ancient and common. 38 factors and epistemological knots in examining the re- 90 They supposed functional continuity between fibres 39 lations at work in the constructions of both disciplines 91 only relied on their anatomical continuity, with cells 40 and concepts. 92 41 considered as trophic centres. This view was already 93 held by the first French professor of histology at the 42 2. Consensus and initial discussions on the nerve 94 43 cell Parisian ‘Faculté de médecine’, Charles Robin (1821– 95 44 1885), a famous opponent of the cell theory [5 (p. 542)]. 96 45 Before the neurone doctrineUNCORRECTED was established, most In his work, PROOF the exclusion of cells as a general con- 97 46 physiologists and anatomists held a common view of stituent of tissues led to this early form of reticularism 98 47 nerve cells, considered as necessary loci of anatomical (1892): 99 48 interactions between fibres. Such conceptions referred 100 49 specifically to the soma of cells, located in the grey mat- 101 1 “From previous facts, [nerve] cells should either be the origin of 50 102 ter of nerve centres, as opposed to fibres and protoplas- fibres or organelles placed on fibre paths. In such cases, tubes would 51 mic processes. The nerve cell was occasionally termed represent conductors of the nervous system, with cells being a making 103 52 ‘nucleus’. In no way were nerve fibres understood as or a collecting agent.” 104 ARTICLE IN PRESS JID:CRASS3 AID:2439 /FLA [m3+; v 1.59; Prn:29/03/2006; 15:59] P.3 (1-13) J.-G. Barbara / C. R. Biologies ••• (••••) •••–••• 3 1 “Au-delà de l’état cellulaire, il y a l’état d’organisa- anatomopathology and physiology. In the 19th century, 53 2 tion ; [...] le mot cellule ne suffit pas, puisqu’il n’im- these disciplines were often associated in teaching, jour- 54 3 plique pas les états de fibre, de tube, états qui sont nals and scientific programmes. However (1), at the turn 55 4 tout aussi réels que l’état dit cellulaire.” [5 (p. 18)]2 of the 20th century, French Bernardian physiology de- 56 5 veloped into an independent discipline, which increas- 57 6 Conversely, the early cellularist anatomist Math- ingly rejected the concepts and methods of anatomy.

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