Talk:Neuroethology of Insect Walking
Contents |
Review by Paul Katz
This article is extremely well written and thorough. I have just one point that I would like to raise: The title of the article is Neurobiology of Insect Walking, yet none of the illustrations show a neuron, a nervous system, or an electrophysiological recording. These aspects are discussed in the text and could be illustrated. In the absence of such illustration and given the strong emphasis on other features, you might consider changing the title to "Biomechanics of Insect Walking". I am in favor of calling it "Neuroethology of Insect Walking" because that incorporates the behavior and the neurobiology. --Paul S. Katz 17:59, 23 January 2013 (UTC)
Change title word Neurobiology
I think that calling the article Biomechanics of Insect walking would be misleading. We really do not talk about biomechanics much at all and I suspect other authors would be better for such an article. I am OK with "Neuroethology" and in fact like that a lot. I am a bit concerned that fewer people know what Neuroethology is. But that may be OK. You are right that there are no neurobiology figures, but the text is heavily devoted to neurobiology.
I will await what others think about this matter.
Redirect
I made a new article entitled "Neuroethology of Insect Walking" and redirected the "Neurobiology..." article here. So, now people can find both. --Paul S. Katz 23:02, 23 January 2013 (UTC)
Review by Ansgar Bueschges
This article is basically well structured and well written. It introduces the reader into basic aspects of the neurobiology of insect locomotion mostly from the viewpoint of one of the most thoroughly studied insects, the cockroach. It can be a very valuable contribution to Scholarpedia.
I have some suggestions that shall help to improve clarity of presentation:
1. I think in order to approve the title "neuroethology" the review may give more room to introducing the task that the nervous system is resolving, when generating walking. I suggest a figure with some physiological data showing the activity of motoneurons and muscles during stepping.
2. The authors may consider to modify the title by saying "Neuroethology of insect walking - insights from studying cockroach and stick insect". I suggest this because even though the auhtors try to keep the text general at introductory sections, still as a biologist one may argue that much of the text is based the morphology and evolutionary specialization of these two animals.
3. When introducing the section "Basic Leg Movements Associated with Walking" the authors introduce coordination patterns known from insects. They explain metachtronal wave and tripod coordination. Why is tetrapod coordination not mentioned? The authors may decide to give reference to the discussion that one may see the three coordination patterns (metachronal pattern, tetrapod and tripod coordination) as some kind of a continuum, which spans across the speed range of walking (e.g. Wosnitza et al. 2013). A slight extension of this section may be justified due to the fact that the auhtors amis for an introduction to insect walking in general.
4. At the end of the section "Basic Leg Movements Associated with Walking" the authors introduce aspects of biomechanics, but they do not introduce the reader to the important role muscles play in transforming neural signals into forces. I think this would be important, because neurobiologists for long simply overlooked the importance of the neuromuscular transformation. Current results from the cockroach (as well as from the stick insect) could be mentioned here.
5. The authors differentiate between "Reflexes" and "CPGs". At places it is difficult for the reader to discriminate between the following influences:(i) sensory signals modify motor activity by reflex action (based on direct or polysynaptic pathways); (ii) sensory signals affect CPG activity, e.g. switch phase of CPG-activity, and thereby in turn affect motor activity. For better clarity the authors may as well consider to depict the principle sensory and CPG influences in a scheme, e.g. like the one in Büschges & ElManira, 1988, COIN.
6. In the last section the authors report on the exciting new insights into the role distinct brain circuits play in the control of goal directed locomotor behavior. It would be very useful for the reader to have a figure depicting the anatomical setup of the insect nervous system and showing the location and structure of the central body complex. This figure may potentially include reference to the location of the other neural networks described in the previous sections.
I hope the auhtors find these remarks helpful.
Answers to Reviewer's comments
Reviewers' comments: This article is basically well structured and well written. It introduces the reader into basic aspects of the neurobiology of insect locomotion mostly from the viewpoint of one of the most thoroughly studied insects, the cockroach. It can be a very valuable contribution to Scholarpedia. I have some suggestions that shall help to improve clarity of presentation:
Reviewer comment 1. I think in order to approve the title "neuroethology" the review may give more room to introducing the task that the nervous system is resolving, when generating walking. I suggest a figure with some physiological data showing the activity of motoneurons and muscles during stepping.
Author reply: We have added Figure 3 a recording of motoneuron activities during walking.
Reviewer comment 2. The authors may consider to modify the title by saying "Neuroethology of insect walking - insights from studying cockroach and stick insect". I suggest this because even though the authors try to keep the text general at introductory sections, still as a biologist one may argue that much of the text is based the morphology and evolutionary specialization of these two animals.
Author reply: We have added a statement on p. 5 noting that these animals have been the best studied.
Reviewer comment 3. When introducing the section "Basic Leg Movements Associated with Walking" the authors introduce coordination patterns known from insects. They explain metachronal wave and tripod coordination. Why is tetrapod coordination not mentioned? The authors may decide to give reference to the discussion that one may see the three coordination patterns (metachronal pattern, tetrapod and tripod coordination) as some kind of a continuum, which spans across the speed range of walking (e.g. Wosnitza et al. 2013). A slight extension of this section may be justified due to the fact that the authors aim for an introduction to insect walking in general.
Author reply: We have added the following statement on p. 2: At intermediate speeds, the phases of leg movements shift (this is termed gliding coordination) and more than one leg may be lifted at the same time (ex. tetrapod gait, Wosnitza et al. 2013).
Reviewer comment 4. At the end of the section "Basic Leg Movements Associated with Walking" the authors introduce aspects of biomechanics, but they do not introduce the reader to the important role muscles play in transforming neural signals into forces. I think this would be important, because neurobiologists for long simply overlooked the importance of the neuromuscular transformation. Current results from the cockroach (as well as from the stick insect) could be mentioned here.
Author reply: We have added the following text to page 5: It should be noted that in addtion to neural components, muscle properties also play an essential role in how motor neurons generate movements. A thorough review of muscle properties is beyond the scope of this review. The reader is directed to the following reviews for this important aspect of insect locomotionhttp://www.scholarpedia.org/article/Muscle_Physiology_and_Modeling; see also recent investigations in insect muscle properties in (Blümel et al. 2012).
Reviewer comment 5. The authors differentiate between "Reflexes" and "CPGs". At places it is difficult for the reader to discriminate between the following influences:(i) sensory signals modify motor activity by reflex action (based on direct or polysynaptic pathways); (ii) sensory signals affect CPG activity, e.g. switch phase of CPG-activity, and thereby in turn affect motor activity. For better clarity the authors may as well consider to depict the principle sensory and CPG influences in a scheme, e.g. like the one in Büschges & ElManira, 1988, COIN.
Author reply: We now refer the reader to the reference Büschges & ElManira, 1988, COIN on page 6. We have also added text to p. 7 describing the pathways by which sense organs can influence the magnitude and timing of motor outputs and shown these pathways as new Figure 5.
Reviewer comment 6. In the last section the authors report on the exciting new insights into the role distinct brain circuits play in the control of goal directed locomotor behavior. It would be very useful for the reader to have a figure depicting the anatomical setup of the insect nervous system and showing the location and structure of the central body complex. This figure may potentially include reference to the location of the other neural networks described in the previous sections.
Author reply: We have added a diagram of the central complex and circuits in the thoracic ganglion as Figure 7.
Review by Volker Dürr
General comments
With their Scholarpedia Review on "Neuroethology of Insect Walking", Roy Ritzmann and Sasha Zill provide a very informative and readable overview of the neurobiology of cockroach locomotion. Overall, I think that both the text and the figures are very useful and comprehensive. My major criticism is that the article is very much dominated by the authors own research, with addition of hand-selected, very closely related work by a collaborating lab in Cologne. In principle, this doesn't have to be a disadvantage, particularly as both authors are authorities in this research field and have dominated the literature on the neurobiology of cockroach locomotion for decades. Still, I’d find it more correct if the title was "neurobiology of cockroach walking". I realise that the title has been changed in the meantime to "neuroethology". That was somewhat surprising to me, because it mainly deals with reflex loops and a large portion of behavioural work on insect walking is not covered.
If the idea was to have a more general overview on insect walking, I’d suggest three things:
(1) First, additional timely work on sensory-motor loops could be cited, particularly on other insect model systems, e.g. on convergence and modulation among sensory inputs (e.g., Schmitz and Stein (2000); Stein and Schmitz (1999). In many cases this could be done without much changes to the text.
(2) Second, the relevance of slightly differing approaches, most notably those of biomechanics, behavioural physiology and modelling could be discussed briefly. I realise that this is not the focus of this article, and I know that both authors can be very critical about the limitations of other approaches to the study of insect walking, but why not add a brief discussion on this at this place. For example, why not discuss the problem of making inferences about neuronal mechanisms from kinematic investigations (with a reference to complex biomechanics) but also of making inferences about behavioural relevance from electrophysiological measurements (e.g., owing to passive biomechanics of the motor system). Similarly, the benefits/limitations of ground reaction force measurements, pharmacological investigations of central patterning activity, modelling approaches could be dealt with in a section called ”pros and cons of complementary approaches to the study of insect walking”.
(3) Finally, this could be a great place to give a brief account on the development of views about insect walking through the extensive research on neurobiology of cockroaches (e.g., Keir Pearson, Jeff Camhi, etc.), locusts (e.g., Malcolm Burrows) and stick insects (e.g., W. von Buddenbrock, Erich von Holst, Gernot Wendler, Ulrich Bässler). Also, the authors would be the right people to do so (they know most of these people in person, and certainly are well informed about their work). Again, I don’t have a whole A4 page of text in mind, but a brief summary of early approaches, views, conceptions – maybe half a page with citation of important reviews and books.
Specific comments
Preface, L. 3: "most typically move by walking". That's cerainly true for many insect orders like cockroaches, but not for all. I suggest writing something like "all insects are capable of terrestrial locomotion and all of them spend a great deal of their life doing so".
Preface, paragr. 2: Here the authors explain why they want to stay with local circuits in the thorax. Of course the review will be helpful if the authors keep that view, particularly if points 1 and 3 from above were considered. Still I’d like to encourage the authors to be a bit more explicit about the complementary approaches and their relevance. As it is, the review claims implicitly that the understanding of local circuits in the thorax is sufficient (or at least most relevant) to understanding walking behaviour. Instead, the authors are so deeply familiar with the ongoing debates about complementary approaches that they could easily sketch the main arguments about how the sole coverage of thoracic reflex circuits limits our understanding of natural walking behaviour, and which other approaches are currently available to complement this restricted coverage.
Part I, first sentence: "formal reports on leg movement ... start with..." is incorrect. At least the works by Buddenbrock (1920); Holst (1935); Holst (1943) predate the cited work by decades! Also Wendler (1964) would have to be fit in here as well. I realise that these works are written in German, but there are Scholarpedia readers that know some German and my find these references insightful.
Part I, text referring to Fig. 1: The strict distinction between tripod and tetrapod walking is somewhat historical and should be contrasted by recent discussion on the usefulness and appropriateness of gait classification. For example Grabowska et al. (2012) report a large percentage of episodes that cannot be classified unambiguously, Dürr (2005) provides evidence that variable coupling between legs may be better treated as various forms of a free gait. In any case, modelling studies such as the important works by Cruse and co-workers (e.g., Cruse et al. (1995); Kindermann (2002); Dürr et al. (2004) show that state-dependent and/or sensory coupling between single-leg controllers may generate a continuum of gaits from wave gait, to tetrapod gait and tripod gait simply by “stretching” or “compressing” the stance period of the step cycle without altering the swing duration. That way, all gaits are caused by the same kind of metachronal wave progressing along the body, with a simple speed-dependent variable determining the steady state gait pattern. A different arrangement of the legs in Fig 1B would illustrate that better (sorting the six rows for side rather than tripod).
Part I, text referring to Fig. 2: I suggest to include the comparative study by Frantsevich and Wang (2009) and the classic study by Cruse (1976).
Part II, first sentence. "common neural control systems..." seems to contradict the second-to-last sentence of the previous part, where the authors state "clearly, the neural control of thisleg is much different from the other two". This needs to be made clearer. Maybe it would help to state that even in an animal with morphologically similar legs, such as a stick insect, the gains and signs of control variables need to be adapted to the kinematics (e.g., hind legs may need to flex during protraction, whereas front legs may need to extend). Still, the underlying neural network may be very similar. That would differentiate between the circuitry and its control function.
Part II, third paragr.: It may be useful to mention at the end that there are insect preparations in which the coordination appears to be maintained after de-afferentation (locusts) and the cited paper by Büschges et al. also discusses the presence of so-called „spontaneous, recurrent patterns“ which are transient episodes of coordinated activity.
Part II, paragr. 5: I suggest to replace the term reflex reversal by refe modulation and then introduce the term reflex reversal once as a very extreme form of reflex modulation. Also, the sentence on "selective reflex reversals in appropriate legs" is incomprehensible to me, eveb though I know the paper well.
Part II, paragr. 6: "These signals insure that the leg is not lifted". Here, I’suggest to include references about the behavioural relevance. In fact this idea was first supported by behavioural studies on leg coordination in stick insects Cruse and Epstein (1982), scorpions Bowerman (1975) and crustaceans Cruse and Müller (1986); Cruse (1990) and corresponding modelling work of Cruse (see citations above). Of course, only the elegant recent studies by Sasha Zill and collaborators then showed that the campaniform sensillae are involved in such "coordinating influences". Still, the behavioural work emphasises its relvance!
Part II, second-to-last paragr.: "effects have been reproduced in dynamic simulations". This is not correct as it stands. The references refer to two kinds of "dynamic simulations", one to dynamic systems modelling in mathematical terms (sets of differential equations), the other to the modelling of dynamics, i.e., forces. Of course both are connected, but the main points of the cited references are very different. To be fair, the authors ma want to include the recent review by Cruse and co-workers Schilling et al. (2013), which is basically a reply to the review by Silvia Daun-Gruhn.
Part III, first paragr.: This reads as though visual and tactual near-range orientation has only ever been studied by the Ritzmann lab. I suggest to cite the review by Staudacher et al. (2005), some work of immediate relevance to cockroach tactile orientation (e.g., by Okada and Toh (2000; 2006) and maybe one or two works by Roland Strauss on visual orientation in climbing (e.g., Pick and Strauss (2005).
Part IV, last paragraph. I think there's a reference missing for the statements in the first 5 sentences.
References: The citation of Guo and Ritzmann should be printed in a new line.
Reference List
1. Bowerman, R. F. (1975). The control of walking in the scorpion. I. Leg movements during normal walking. J.Comp.Physiol. 100, 183-196.
2. Buddenbrock, W. v. (1920). Der Rhythmus der Schreitbewegungen der Stabheuschrecke Dyxippus. Biol.Zentralbl. 41, 41-48.
3. Cruse, H. (1976). The function of the legs in the free walking stick insect Carausius morosus. J.Comp.Physiol. 112, 235-262.
4. Cruse, H. (1990). What mechanisms coordinate leg movement in walking arthropods? TINS 13, 15-21.
5. Cruse, H. et al. (1995). Walking: a complex behaviour controlled by simple networks. Adaptive Behavior 3, 385-418.
6. Cruse, H. and Epstein, S. (1982). Peripheral influences on the movement of the legs in a walking insect Carausius morosus. J.Exp.Biol. 101, 161-170.
7. Cruse, H. and Müller, U. (1986). Two coupling mechanisms which determine the coordination of ipsilateral legs in the walking crayfish. J.Exp.Biol. 121, 349-369.
8. Dürr, V. (2005). Context-dependent changes in strength and efficacy of leg coordination mechanisms. J.Exp.Biol. 208, 2253-2267.
9. Dürr, V., Schmitz, J., and Cruse, H. (2004). Behaviour-based modelling of hexapod locomotion: linking biology and technical application. Arthropod.Struct.Dev. 33, 237-250.
10. Frantsevich, L. and Wang, W. (2009). Gimbals in the insect leg. Arthropod Structure & Development 38, 16-30.
11. Grabowska, M. et al. (2012). Quadrupedal gaits in hexapod animals - inter-leg coordination in free-walking adult stick insects. The Journal of Experimental Biology 215, 4255-4266.
12. Holst, E. v. (1935). Die Koordination der Bewegung bei den Arthropoden in Abhängigkeit von zentralen und peripheren Bedingungen. Biol.Rev. 10, 234-261.
13. Holst, E. v. (1943). Über relative Koordination bei Arthropoden. Pflügers Arch. 246, 847-865.
14. Kindermann, T. (2002). Behavior and adaptability of a six-legged walking system with highly distributed control. Adaptive Behavior 9, 16-41.
15. Okada, J. and Toh, Y. (2000). The role of antennal hair plates in object-guided tactile orientation of the cockroach (Periplaneta americana). J.Comp.Physiol.A 186, 849-857.
16. Okada, J. and Toh, Y. (2006). Active tactile sensing for localization of objects by the cockroach antenna. J.Comp.Physiol.A 192, 715-726.
17. Pick, S. and Strauss, R. (2005). Goal-driven behavioral adaptations in gap-climbing Drosophila. Current Biology 15, 1473-1478.
18. Schilling, M. et al. (2013). Walknet, a bio-inspired controller for hexapod walking. Biol Cybern 1-23.
19. Schmitz, J. and Stein, W. (2000). Convergence of load and movement information onto leg motoneurons in insects. J.Neurobiol. 42, 424-436.
20. Staudacher, E., Gebhardt, M. J., and Dürr, V. (2005). Antennal movements and mechanoreception: neurobiology of active tactile sensors. Adv.Insect Physiol. 32, 49-205.
21. Stein, W. and Schmitz, J. (1999). Multimodal convergence of presynaptic afferent inhibition in insect proprioceptors. J.Neurophysiol. 82, 512-514.
22. Wendler, G. (1964). Laufen und Stehen der Stabheuschrecke: Sinnesborsten in den Beingelenken als Glieder von Regelkreisen. Z.vergl.Physiol. 48, 198-250.
Answers to Reviewer's comments
General comments
(1) First, additional timely work on sensory-motor loops could be cited, particularly on other insect model systems, e.g. on convergence and modulation among sensory inputs (e.g., Schmitz and Stein (2000); Stein and Schmitz (1999). In many cases this could be done without much changes to the text.
Author Reply: We thank the reviewer for the additional references and have included a number of citations, including the papers by Josef Schmitz and Wolfgang Stein (Local Control, paragraph 6).
(2) Second, the relevance of slightly differing approaches, most notably those of biomechanics, behavioural physiology and modelling could be discussed briefly. I realise that this is not the focus of this article, and I know that both authors can be very critical about the limitations of other approaches to the study of insect walking, but why not add a brief discussion on this at this place. For example, why not discuss the problem of making inferences about neuronal mechanisms from kinematic investigations (with a reference to complex biomechanics) but also of making inferences about behavioural relevance from electrophysiological measurements (e.g., owing to passive biomechanics of the motor system). Similarly, the benefits/limitations of ground reaction force measurements, pharmacological investigations of central patterning activity, modelling approaches could be dealt with in a section called ”pros and cons of complementary approaches to the study of insect walking”.
Author Reply: We have now noted (Introduction, paragraph 4) that a variety of approaches have been used to study insect walking. However, we believe that a section discussing 'pros and cons' of approaches is beyond the scope of this introductory article.
(3) Finally, this could be a great place to give a brief account on the development of views about insect walking through the extensive research on neurobiology of cockroaches (e.g., Keir Pearson, Jeff Camhi, etc.), locusts (e.g., Malcolm Burrows) and stick insects (e.g., W. von Buddenbrock, Erich von Holst, Gernot Wendler, Ulrich Bässler). Also, the authors would be the right people to do so (they know most of these people in person, and certainly are well informed about their work). Again, I don’t have a whole A4 page of text in mind, but a brief summary of early approaches, views, conceptions – maybe half a page with citation of important reviews and books.
Author Reply: We now include a brief, historical overview of studies of insect walking, with citations to earlier work (Introduction, paragraphs 3,4). We also note (Introduction, paragraph 5) that our article is intended as an introduction rather than a complete review of all aspects of research on this subject but include references to other reviews.
Specific comments
Preface, L. 3: "most typically move by walking". That's cerainly true for many insect orders like cockroaches, but not for all. I suggest writing something like "all insects are capable of terrestrial locomotion and all of them spend a great deal of their life doing so".
Author reply: We have modified the statement (Introduction, paragraph 1) to note that all insects are capable of terrestrial locomotion.
Preface, paragr. 2: Here the authors explain why they want to stay with local circuits in the thorax. Of course the review will be helpful if the authors keep that view, particularly if points 1 and 3 from above were considered. Still I’d like to encourage the authors to be a bit more explicit about the complementary approaches and their relevance. As it is, the review claims implicitly that the understanding of local circuits in the thorax is sufficient (or at least most relevant) to understanding walking behaviour. Instead, the authors are so deeply familiar with the ongoing debates about complementary approaches that they could easily sketch the main arguments about how the sole coverage of thoracic reflex circuits limits our understanding of natural walking behaviour, and which other approaches are currently available to complement this restricted coverage.
Author reply: We now include references to introduce the reader to the elegant studies and behavior based-modeling done by Cruse, Dűrr and colleagues (Introduction paragraph 4, Local Control paragraphs 7,8 ). We have also emphasized that study of insect walking (and Neuroethology as a whole) has benefited from diverse approaches but believe that a discussion of the relative merits of different approaches is beyond the scope of this introductory article.
Part I, first sentence: "formal reports on leg movement ... start with..." is incorrect. At least the works by Buddenbrock (1920); Holst (1935); Holst (1943) predate the cited work by decades! Also Wendler (1964) would have to be fit in here as well. I realise that these works are written in German, but there are Scholarpedia readers that know some German and my find these references insightful.
Author reply: We thank the reviewer and have included many of the earlier references, including the report of Morgan, 1887.
Part I, text referring to Fig. 1: The strict distinction between tripod and tetrapod walking is somewhat historical and should be contrasted by recent discussion on the usefulness and appropriateness of gait classification. For example Grabowska et al. (2012) report a large percentage of episodes that cannot be classified unambiguously; Dürr (2005) provides evidence that variable coupling between legs may be better treated as various forms of a free gait. In any case, modelling studies such as the important works by Cruse and co-workers (e.g., Cruse et al. (1995); Kindermann (2002); Dürr et al. (2004) show that state-dependent and/or sensory coupling between single-leg controllers may generate a continuum of gaits from wave gait, to tetrapod gait and tripod gait simply by “stretching” or “compressing” the stance period of the step cycle without altering the swing duration. That way, all gaits are caused by the same kind of metachronal wave progressing along the body, with a simple speed-dependent variable determining the steady state gait pattern. A different arrangement of the legs in Fig 1B would illustrate that better (sorting the six rows for side rather than tripod).
Author reply: We have now clarified these points in the discussion of gaits at different walking speeds (Basic Leg Movements, paragraph 1). We have, however, retained the diagram in Fig. 1B to clearly define the tripod gait as an introduction to the reader.
Part I, text referring to Fig. 2: I suggest to include the comparative study by Frantsevich and Wang (2009) and the classic study by Cruse (1976).
Author reply: These important references are now included.
Part II, first sentence. "common neural control systems..." seems to contradict the second-to-last sentence of the previous part, where the authors state "clearly, the neural control of this leg is much different from the other two". This needs to be made clearer. Maybe it would help to state that even in an animal with morphologically similar legs, such as a stick insect, the gains and signs of control variables need to be adapted to the kinematics (e.g., hind legs may need to flex during protraction, whereas front legs may need to extend). Still, the underlying neural network may be very similar. That would differentiate between the circuitry and its control function.
Author reply: We have now clarified this discrepancy by noting that the phases of movements may differ for front, middle and hindlegs (Local Control, paragraph 2).
Part II, third paragr.: It may be useful to mention at the end that there are insect preparations in which the coordination appears to be maintained after de-afferentation (locusts) and the cited paper by Büschges et al. also discusses the presence of so-called „spontaneous, recurrent patterns“ which are transient episodes of coordinated activity.
Author reply: We have changed the description (Local Control, paragraph 6) and included references to note that the mechanisms of coordination include both central connections and sensory feedback. We believe that a more detailed discussion of the circuitry, while of considerable interest, is more appropriate for a full, rather than introductory, review.
Part II, paragr. 5: I suggest to replace the term reflex reversal by reflex modulation and then introduce the term reflex reversal once as a very extreme form of reflex modulation. Also, the sentence on "selective reflex reversals in appropriate legs" is incomprehensible to me, even though I know the paper well.
Author reply: We are in complete agreement with the reviewer and have changed the description to reflex modulation (Local Control, paragraph 6). However, we also define the term 'reflex reversal' for clarity, as it is extensively used in the literature on walking in both invertebrates (ex. Hellekes et al. 2012) and vertebrates.
Part II, paragr. 6: "These signals insure that the leg is not lifted". Here, I’suggest to include references about the behavioural relevance. In fact this idea was first supported by behavioural studies on leg coordination in stick insects Cruse and Epstein (1982), scorpions Bowerman (1975) and crustaceans Cruse and Müller (1986); Cruse (1990) and corresponding modelling work of Cruse (see citations above). Of course, only the elegant recent studies by Sasha Zill and collaborators then showed that the campaniform sensillae are involved in such "coordinating influences". Still, the behavioural work emphasises its relevance!
Author reply: The suggested references on insects and behavioral work are now included.
Part II, second-to-last paragr.: "effects have been reproduced in dynamic simulations". This is not correct as it stands. The references refer to two kinds of "dynamic simulations", one to dynamic systems modelling in mathematical terms (sets of differential equations), the other to the modelling of dynamics, i.e., forces. Of course both are connected, but the main points of the cited references are very different. To be fair, the authors ma want to include the recent review by Cruse and co-workers Schilling et al. (2013), which is basically a reply to the review by Silvia Daun-Gruhn.
Author reply: We believe we have corrected the statement by deleting the term dynamic. We also now cite the excellent paper by Schilling et al. We believe that differences in the methods used in simulation, while important, are more appropriately discussed in a full review chapter (or book).
Part III, first paragr.: This reads as though visual and tactual near-range orientation has only ever been studied by the Ritzmann lab. I suggest to cite the review by Staudacher et al. (2005), some work of immediate relevance to cockroach tactile orientation (e.g., by Okada and Toh (2000; 2006) and maybe one or two works by Roland Strauss on visual orientation in climbing (e.g., Pick and Strauss (2005).
Author reply: We have now revised the text of that paragraph and included the references and thank the reviewer for noting this omission.
Part IV, last paragraph. I think there's a reference missing for the statements in the first 5 sentences.
Author reply: The reference is now included.
References: The citation of Guo and Ritzmann should be printed in a new line.
Author reply: The reference has now been fixed and has also been updated.
Note
As an interested bystander, I've organized the material on this page in the standard way, with the newest material at the bottom. Let me mention that it is possible to add a signature and date to anything written here by typing ~~~~ at the end. William E. Skaggs 16:29, 21 August 2013 (UTC)
