Abstract
The neuronal networks that control the motion of the individual legs in insects, in particular in the stick insect, are located in the pro-, meso- and meta-thoracic ganglia. They ensure high flexibility of movement control. Thus, the legs can move in an apparently independent way, e.g., during search movements, but also in tight coordination during locomotion. The latter is evidently a very important behavioural mode. It has, therefore, inspired a large number of studies, all aiming at uncovering the nature of the inter-leg coordination. One of the basic questions has been as to how the individual control networks in the three thoracic ganglia are connected to each other. One way to study this problem is to use phase response curves. They can reveal properties of the coupling between oscillatory systems, such as the central pattern generators in the control networks in the thoracic ganglia. In this paper, we report results that we have achieved by means of a combined experimental and modelling approach. We have calculated phase response curves from data obtained in as yet unpublished experiments as well as from those in previously published ones. By using models of the connected pro- and meso-thoracic control networks of the protractor and retractor neuromuscular systems, we have also produced simulated phase response curves and compared them with the experimental ones. In this way, we could gain important information of the nature of the connections between the aforementioned control networks. Specifically, we have found that connections from both the protractor and the retractor “sides” of the pro-thoracic network to the meso-thoracic one are necessary for producing phase response curves that show close similarity to the experimental ones. Furthermore, the strength of the excitatory connections has been proven to be crucial, while the inhibitory connections have essentially been irrelevant. We, thus, suggest that this type of connection might also be present in the stick insect, and possibly in other insect species.
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References
Akay T, Ludwar BCh, Göritz ML, Schmitz J, Büschges A (2007) Segment specificity of load signal processing depends on walking direction in the stick insect leg muscle control system. J Neurosci 27:3285–3294
Bässler U (1977) Sensory control of leg movement in the stick insect Carausius morosus. Biol Cybern 25:61–72
Bässler U (1983) Neural basis of elementary behavior in stick insects. Springer, Berlin
Borgmann A, Scharstein H, Büschges A (2007) Intersegmental coordination: influence of a single walking leg on the neighboring segments in the stick insect walking system. J Neurophysiol 98:1685–1696
Borgmann A, Hooper SL, Büschges A (2009) Sensory feedback induced by front-leg stepping entrains the activity of central pattern generators in caudal segments of the stick insect walking system. J Neurosci 29:2972–2983
Borgmann A, Tóth TI, Gruhn M, Daun-Gruhn S, Büschges A (2011) Dominance of local sensory signals over inter-segmental effects in a motor system: experiments. Biol Cybern 105:399–411
Büschges A (1995) Role of local nonspiking interneurons in the generation of rhythmic motor activity in the stick insect. J Neurobiol 27:488–512
Büschges A (1998) Inhibitory synaptic drive patterns motoneuronal activity in rhythmic preparations of isolated thoracic ganglia in the stick insect. Brain Res 783:262–271
Büschges A, Gruhn M (2008) Mechanosensory feedback in walking: from joint control to locomotor patterns. Adv Insect Physiol 34:193–230
Cruse H (1990) What mechanisms coordinate leg movement in walking arthropods? TINS 13:15–21
Cruse H (2009) Principles of insect locomotion. In: Arena P, Patane L (eds) Spatial temporal patterns for action-oriented perception in roving robots. Springer, Berlin, pp 1–57
Daun S, Rybak IA, Rubin J (2009) The response of a half-center oscillator to external drive depends on the intrinsic dynamics of its components: a mechanistic analysis. J Comput Neurosci 27:3–36
Daun-Gruhn S, Tóth TI (2011) An inter-segmental network model and its use in elucidating gait-switches in the stick insect. J Comput Neurosci 31:43–60
Daun-Gruhn S, Tóth TI, Borgmann A (2011) Dominance of local sensory signals over inter-segmental effects in a motor system: modeling studies. Biol Cybern 105:413–426
Delcomyn F (1971) The locomotion of the cockroach Periplaneta americana. J Exp Biol 54:453–496
Delcomyn F (1981) Insect locomotion on land. In: Herreid CF, Fourtner CR (eds) Locomotion and energetics in arthropods. Plenum Press, New York, pp 103–125
Grabowska M, Godlewska E, Schmidt J, Daun-Gruhn S (2012) Quadrupedal gaits in hexapod animals—inter-leg coordination in free-walking adult stick insects. J Exp Biol 215:4255–4266
Graham D (1972) A behavioural analysis of the temporal organisation of walking movements in the 1st instar and adult stick insect (Carausius morosus). J Comp Physiol A 81:23–52
Graham D (1985) Pattern and control of walking in insects. Adv Insect Physiol 18:31–140
Hill AV (1953) The mechanics of active muscle. Proc R Soc Lond (Biol) 141:104–117
Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500–544
Hughes GM (1952) The co-ordination of insect movements. I. The walking movements of insects. J Exp Biol 29:167–285
Knops S, Tóth TI, Guschlbauer C, Gruhn M, Daun-Gruhn S (2013) A neuromechanical model for the neuronal basis of curve walking in the stick insect. J Neurophysiol 109:679–691
Laurent G, Burrows M (1989) Distribution of intersegmental inputs to nonspiking local interneurons and motor neurons in the locust. J Neurosci 9:3019–3029
Laurent G, Burrows M (1989) Intersegmental interneurons can control the gain of reflexes in adjacent segments of the locust by their action on nonspiking local interneurons. J Neurosci 9:3030–3039
Ludwar BC, Westmark S, Büschges A, Schmidt J (2005) Modulation of membrane potential in mesothoracic moto- and interneurons during stick insect front leg walking. J Neurophysiol 93:1255–1265
Pearson KG, Franklin R (1984) Characteristics of leg movements and patterns of coordination in locusts walking on rough terrain. Int J Robot res 3:101–112
Ritzmann RE, Büschges A (2007) Adaptive motor behavior in insects. Curr Opin Neurobiol 17:629–636
Schmitz J (1986) The depressor trochanteris motoneurones and their role in the coxa-trochanteral feedback loop in the stick insect Carausius morosus. Biol Cybern 55:25–34
Schmitz J (1986) Properties of the feedback system controlling the coxa-trochanter joint in the stick insect Carausius morosus. Biol Cybern 55:35–42
Schultheiss NW, Prinz AA, Butera RJ (eds) (2012) Phase response curves in neuroscience. Theory, experiment, and analysis. Springer Series in Computational Neuroscience, vol 6. Springer, New York
Tóth TI, Daun-Gruhn S (2011) A putative neuronal network controlling the activity of the leg motoneurons of the stick insect. Neuroreport 22:943–946
Tóth TI, Knops S, Daun-Gruhn S (2012) A neuromechanical model explaining forward and backward stepping in the stick insect. J Neurophysiol 107:3267–3280
Westmark S, Oliveira EE, Schmidt J (2009) Pharmacological analysis of tonic activity in motoneurons during stick insect walking. J Neurophysiol 102:1049–1061
Wilson DM (1966) Insect walking. Ann Rev Entomol 11:103–122
Winfree AT (2000) The geometry of biological time, 2nd edn. Springer, New York
Acknowledgments
We thank Drs. J. Schmidt and A. Büschges for helpful discussions in the course of this work. This work was funded by the Deutsche Forschungsgemeinschaft Grants DA1182/1-1 and GR3690/4-1.
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Tóth, T.I., Grabowska, M., Rosjat, N. et al. Investigating inter-segmental connections between thoracic ganglia in the stick insect by means of experimental and simulated phase response curves. Biol Cybern 109, 349–362 (2015). https://doi.org/10.1007/s00422-015-0647-5
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DOI: https://doi.org/10.1007/s00422-015-0647-5