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Archived Comments for: Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary

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  1. Attempt at a neuroanatomical glossary failed?

    Bernhard Ruthensteiner, Bavarian State Collection of Zoology

    22 March 2011

    Richter et al. claim to provide a precise and consistent terminology for invertebrate nervous system components as a basis for morphological descriptions. However, such an attempt faces a specific problem in the first place: identical denomination of structures does not generally imply homology. There are numerous cases in which structures with similar function in taxa without close relationships are identically termed but are not (clearly) homologous. The authors are aware of this problem and try to bypass it - explicitly in their abstract and introduction - by declaring that any term ('entry') they treat should be regarded as 'free of homology assumptions'. In practice, however, this does not seem to be followed consequently; some 'entries' are treated fairly differently in this regard, as exemplified by the following two terms.
    (1) In the case of the 'brain' ('entry' 3) the non-homology concept is clearly followed. 'Brains' are regarded as 'the most prominent anterior condensation of neurons' of nervous systems. From the illustration (Figure 3) it follows that homology is not even implied within phyla (e.g. molluscs: more ganglionic components included in cephalopods than in other taxa). Accordingly, the conceptual meaning of 'brain' does not differ from what it always has been - mostly as a common name but also in science (e.g. Nielsen, 2005). This leaves unclear why the authors found it worth spending that much space (several pages) on this 'entry', especially since the term has hardly any relevance for phylogenetic considerations, which are precisely ('neurophylogeny'!) what all this should be about. Moreover, the authors' suggestions in the context of the 'brain' become seriously problematic when other important terms are 'discouraged' with the intention of eliminating them from morphological descriptions. To provide one example: In certain molluscan taxa, such as gastropods, there are clearly recognizable separate cerebral ganglia that can be homologized among taxa and, thus, carry potential information for phylogeny. I maintain that elimination of the 'cerebral ganglion' term (or similar ones) - as suggested in the paper - would be a step backwards instead of an improvement.
    (2) Things are very different in the case of the 'tetraneuron' ('entry' 43). Here one gets the strong impression that the term is largely based on a homology assumption, which would very much contradict the conception provided in the authors' introduction. This concerns a hypothesis (not supported in recent molecular analyses, e.g. Hausdorf et al., 2010) of a clade combining Mollusca and Kamptozoa (the 'Tetraneuralia', e.g. Wanninger, 2009). According to this hypothesis, the 'tetraneuron' forms the main synapomorphy uniting these two phyla. When treating the term, it remains ignored that there are other cases of tatraneurous nervous systems (e.g. in the annelid Tetraneura sensu Reisinger, 1972), which might additionally indicate that the 'tetraneuron' term is not at all free of homology assumptions.
    Another weakness of the paper is inconsistency of terms. There are many cases in which definitions and explanations of one term are in conflict with those of others, as in the following examples. It appears as a discrepancy when a 'commissure' ('entry' 6) is characterized as 'connecting longitudinal neurite bundles' while 'ganglia' ('entry' 10) are defined (among other characteristics) as being 'transversally connected by commissures'. The difference between 'nerve cord' ('entry' 20) and 'neurite bundle' ('entry' 24) remains diffuse. These terms appear to have been confused repeatedly, because in several places, for cords containing somata, the term 'neurite bundle' is found instead of 'nerve cord' (e.g. p. 29, Figure 30 for the longitudinal cords of Bothrioplana semperi). Problems like these are not necessarily conceptual ones but likely rather reflect difficulties with fusing the input from such a large number of coauthors. Nevertheless they constitute a major failure, when the declared purpose of the paper was to provide 'a precise and consistent terminology' (abstract, introduction).
    The paper has additional, comparatively minor flaws, such as missing or erroneous figure captions (e.g. many unexplained symbols in Figure 3; missing dorso-ventral orientation for Figure 30B). However, the inadequately mastered homology assumption problem and the inconsistent terminology impair the value of the work so decisively that it does not seem suitable as a basis for terminology in further neuro-morphological studies. It even may be asked whether the paper, instead of clarifying things, contributes to further terminological confusion.

    References
    Hausdorf B, Helmkampf M, Nesnidal MP, Bruchhaus I. Phylogenetic relationships within the lophophorate lineages (Ectoprocta, Brachiopoda and Phoronida). Mol Phylogenet Evol 2010, 55:1121-1127.
    Nielsen C. Larval and adult brains. Evol Dev 2005, 7:483-489.
    Reisinger E: Die Evolution des Orthogons der Spiralier und das Archicoelomatenproblem. Z Zool Syst Evolut-forsch 1972, 10:1-43.
    Wanninger A. Shaping the Things to Come: Ontogeny of Lophotrochozoan Neuromuscular Systems and the Tetraneuralia Concept. Biol Bull 2009, 216:293-306.

    Competing interests

    None declared

  2. Reply

    Thomas Stach, Freie Universitaet Belrin

    28 December 2011

    The comment `Attempt at a neuroanatomical glossary failed¿ by Ruthensteiner (Ruthensteiner 2011; shortly called `commentary¿ hereafter) criticizes the publication `Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary¿ by Richter and co-authors (Richter et al. 2011, shortly called `neuro-glossary¿ hereafter). In the following reply, I will address and hopefully clarify the issues raised by Ruthensteiner (2011) point by point.

    A central and recurrent criticism of the commentary maintains that definitions in the neuro-glossary are not homology-free and thus do not accord to the standards outlined in the neuro-glossary itself. This issue is exemplified by the definition of the term `tetraneurion¿ in the commentary. The definition of `tetraneurion¿ in the neuro-glossary itself reads:

    {43} Tetraneurion
    A tetraneurion is a cluster of neurons. It is part of a ->nervous system and consists of two prominent pairs of longitudinal ->neurite bundles: one inner, ventral pair and one more dorsally situated lateral pair.

    The definition is purely structural. The fact that this structural arrangement of neurite bundles is found in Kamptozoa and Mollusca - and that some authors (Bartolomaeus 1993, 1997, Salvini-Plawen and Bartolomaeus 1995, Haszprunar 1996, Ax 1999, Wanninger 2009) have suggested a sister-group relationship of these taxa - does not affect the definition. If one would discover a hitherto unknown tunicate for example, one could decide based on this definition whether one could apply the term tetraneurion to describe its nervous system or not. Or to phrase it differently, structures that can be labeled with a specific term defined in the neuro-glossary can be hypothesized to be homologous. In fact it is desirable but not logically obligatory that potentially homologous structures are named identically. Cases were structures are named differently, yet homology can be suggested based on similarities and after phylogenetic analysis, also exist; an example would be the swim bladder in teleosts and lungs in tetrapods. The reason to separate the suggestion of a hypothesis of primary homology from the definition of a term is ultimately to avoid a vicious circle: homology (or apomorphy, see de Pinna 1991) is used to support monophyly, therefore monophyly should not be used to define terminology that potentially is used to suggest primary homology. The example of four longitudinal neurite bundles in polychaetes mentioned in the commentary (see also Storch 1913, Reisinger 1972) has been thoroughly reviewed by Orrhage and Mueller (2005). The arrangements described in this more recent review do not accord to the structural definition of tetraneurion sensu Richter et al. (2010). However, it could still be suggested that a pair of lateral nerves found in many polychaetes is homologous to the pleurovisceral connectives in mollusks.

    Whereas the commentary suggested that the definition of `tetraneurion¿ was biased by homology assumptions, it criticized the definition of `brain¿ as being free of homology assumptions but superfluous. The commentary uses the comparison of the gastropod brain to the cephalopod brain as an example of brains that are not homologous. However, the separation of naming a structure from the suggestion of homology of similar structures, allows for a more precise comparison. An analogous example to the molluscan brains can be seen in the brains of different craniates. The brain in mammals is usually considered homologous to the brain of sharks. However, in the former the occipital nerve XII is a true cranial nerve traversing the neurocranium but the homologous nerve is a spinal nerve outside the brain case in the latter (e.g. Mickoleit 2004). One possible conceptualization (= suggestion of primary homology, de Pinna 1991, Richter 2005) of this factual situation is that the brains of these vertebrates are homologous and that the addition of nerve XII and parts of the spinal cord to the brain is a separate homologous feature found in amniotes. Similarly it could be suggested that the brain of Lymnaea stagnalis is homologous to the brain of Sepia officinalis, yet in the latter ganglia were added and changed in position. These changes could then also be considered as separate characters in phylogenetic considerations (numerous other similar examples come to mind: tagmata and appendages of arthropods, parapodia in polychaetes, vertebrae in craniates, etc.). Of course, there could be alternative ways of character coding. In any case as shown using the term `brain¿ can in specific contexts and in explicit and transparent character coding have decisive phylogenetic relevance.

    The commentary conflates the issue discussed in the preceding paragraph with the suggestion in the neuro-glossary to use brain, whenever the definition given under `{3} brain¿ applies and discourages the use of `cephalic ganglion,¿ if this is the case. The commentary describes this as an attempt to eliminate the term `cephalic ganglion¿ from morphological descriptions altogether. This is a misunderstanding. The neuro-glossary suggests that the term ganglion should be restricted to structures that accord to the respective definition. In the case of cerebral ganglia of gastropods mentioned in the commentary, a cerebral ganglion would be part of the brain but ` in accordance with the definition and suggestion of the neuro-glossary ` it would not constitute the gastropod brain.

    In the criticism of entry (6) `commissure¿ the commentary confuses definition and background comments in the neuro-glossary, when constructing a contradiction in claiming that `a 'commissure' ('entry' 6) is characterized as 'connecting longitudinal neurite bundles' while 'ganglia' ('entry' 10) are defined (among other characteristics) as being 'transversally connected by commissures.' The definition in the neuro-glossary reads:

    {6} Commissure
    A commissure is a `neurite bundle. It is part of a `nervous system. It is transversely oriented and the majority of its `neurites are axons of interneurons.

    This definition does invoke neither longitudinal neurite bundles nor ganglia to define the term commissure. The central part of the definition is the transverse orientation of the neurite bundles. The term `commissure¿ (sensu Richter et al. 2010) can therefore be used without contradiction in cases where the neurite bundles in question connect both longitudinal neurite bundles and ganglia.

    Another specific criticism raised in the commentary concerns the distinction between the terms `nerve cord¿ and `neurite bundle,¿ which according to the commentary remains obscure. The definitions of these terms in the neuro-glossary read:

    {20} Nerve cord
    A nerve cord is a cluster of `neurons. It is the most prominent longitudinally extending condensed part of a `nervous system.

    {24} Neurite bundle
    A neurite bundle is a cluster of ->neurites. It is part of the ->nervous system. The neurites are arranged in parallel to form a bundle.

    Thus, we have to take recourse to entries 23 and 28:

    {23} Neurite
    A neurite is a cell process. It is part of a ->neuron. Neurites are divided into primary neurites, axons, and dendrites.

    {28} Neuron
    A neuron is a cell. It is part of the ->nervous system and consists of a soma that gives rise to ->neurites, which conduct electric excitation in a directed way. A neuron communicates with other cells via `synapses. Most neurons synthesize and secrete ->neuroactive substances.

    In combination, these definitions result in the distinction that a `neurite bundle¿ refers to cell processes of neurons whereas `nerve cord¿ refers to clusters of neurons. Therefore, neurite bundles can be part of nerve cords but not vice versa.

    Specifically referring to these definitions, the commentary of Ruthensteiner (2011) names labeling in Figure 30:
    `... because in several places, for cords containing somata, the term 'neurite bundle' is found instead of 'nerve cord' (e.g. p. 29, Figure 30 for the longitudinal cords of Bothrioplana semperi). Problems like these are not necessarily conceptual ones but likely rather reflect difficulties with fusing the input from such a large number of coauthors. Nevertheless they constitute a major failure, when the declared purpose of the paper was to provide 'a precise and consistent terminology'.¿
    However, the schematic textbook presentation of the nervous system of B. semperi is not precise enough to allow deciding whether the line labeled with `neurite bundle¿ points indeed to a neurite bundle within the ventral cord or should be labeled `ventral cord¿ instead. The neuro-glossary is most probably not free from oversights or errors and in case of a second expanded edition of the neuro-glossary constructive and specific criticism would be highly welcome.

    The commentary conclusively repeats the critique of an `inadequately mastered homology assumption problem and (`) inconsistent terminology¿ that would `impair the value of the work (i.e. the neuro-glossary; TS) so decisively that it does not seem suitable as a basis for terminology in further neuro-morphological studies.¿ This critique has been addressed in the preceding paragraphs and it is up to the reader to weigh the arguments offered. In my opinion outlined above the two bases of this summary assessment of the neuro-glossary by Ruthensteiner (2011) are not valid. At least the examples criticized in the commentary do not conflict with the goal of homology-free structural definitions and do not demonstrate an inconsistent use of terminology in the neuro-glossary.
    Given the structural complexity and diversity of nervous systems combined with the individuality of zoologists, there will most probably be cases where terminological problems and reasons for dispute arise. I hope that transparent and constructive discussions could then result in an improved and expanded version of the neuro-glossary.


    Literature cited:

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    de Pinna, MGG: Concepts and tests of homology in the cladistic paradigm, Cladistics 1991, 7:367-394.
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    Ruthensteiner B: Attempt at a neuroanatomical glossary failed? Frontiers in Zoology 2010, 7:29 doi:10.1186/1742-9994-7-29
    Storch O: Vergleichend-anatomische Polychaetenstudien, Sitz.-Ber. Akad. Wiss. Wien. (Math.-nat. Kl.) 1913, 122: 877-988.
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    Wanninger A: Shaping the things to come: ontogeny of lophotrochozoan neuromuscular systems and the Tetraneuralia concept, Biol Bull 2009, 216:293-306.

    Competing interests

    None declared.

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