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Stable phase-shift despite quasi-rhythmic movements: a CPG-driven dynamic model of active tactile exploration in an insect.

Harischandra N, Krause AF, Dürr V - Front Comput Neurosci (2015)

Bottom Line: The effect of proprioceptor ablations could be simulated by changing the amplitude and offset parameters of the joint oscillators, only.We found that the phase-lead of the distal scape-pedicel (SP) joint relative to the proximal head-scape (HS) joint was essential for producing the natural tactile exploration behavior and, thus, for tactile efficiency.Based on our modeling results, we propose that a constant phase difference is coded into the CPG of the antennal motor system and that proprioceptors are acting locally to regulate the joint movement amplitude.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Cybernetics, Faculty of Biology, Bielefeld University Bielefeld, Germany ; Cognitive Interaction Technology Center of Excellence (CITEC), Bielefeld University Bielefeld, Germany.

ABSTRACT
An essential component of autonomous and flexible behavior in animals is active exploration of the environment, allowing for perception-guided planning and control of actions. An important sensory system involved is active touch. Here, we introduce a general modeling framework of Central Pattern Generators (CPGs) for movement generation in active tactile exploration behavior. The CPG consists of two network levels: (i) phase-coupled Hopf oscillators for rhythm generation, and (ii) pattern formation networks for capturing the frequency and phase characteristics of individual joint oscillations. The model captured the natural, quasi-rhythmic joint kinematics as observed in coordinated antennal movements of walking stick insects. Moreover, it successfully produced tactile exploration behavior on a three-dimensional skeletal model of the insect antennal system with physically realistic parameters. The effect of proprioceptor ablations could be simulated by changing the amplitude and offset parameters of the joint oscillators, only. As in the animal, the movement of both antennal joints was coupled with a stable phase difference, despite the quasi-rhythmicity of the joint angle time courses. We found that the phase-lead of the distal scape-pedicel (SP) joint relative to the proximal head-scape (HS) joint was essential for producing the natural tactile exploration behavior and, thus, for tactile efficiency. For realistic movement patterns, the phase-lead could vary within a limited range of 10-30° only. Tests with artificial movement patterns strongly suggest that this phase sensitivity is not a matter of the frequency composition of the natural movement pattern. Based on our modeling results, we propose that a constant phase difference is coded into the CPG of the antennal motor system and that proprioceptors are acting locally to regulate the joint movement amplitude.

No MeSH data available.


Simulation of hair field ablation experiments. (A) Representative trials of the original data from Krause et al. (2013). (B,C,D) follow the same arrangement and graphics details as described for Figure 4. In comparison with the simulation of intact antennae (Figure 4) only the amplitude μi and offset Ci (mean angle of oscillation) of the oscillators were changed according to the average values obtained from experimental data. The parameter values are tabulated in Table 3. The dotted red curves in the inserts show the average cross-correlogram for the data from ablation experiments (n = 5).
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Figure 5: Simulation of hair field ablation experiments. (A) Representative trials of the original data from Krause et al. (2013). (B,C,D) follow the same arrangement and graphics details as described for Figure 4. In comparison with the simulation of intact antennae (Figure 4) only the amplitude μi and offset Ci (mean angle of oscillation) of the oscillators were changed according to the average values obtained from experimental data. The parameter values are tabulated in Table 3. The dotted red curves in the inserts show the average cross-correlogram for the data from ablation experiments (n = 5).

Mentions: Next, we tested to what extent our model was able to simulate experimental data on animals with sensory ablations. For this, we used data on antennal movement after sequential ablation of all dorsal antennal hair fields, as reported by Krause et al. (2013). Figure 5 shows the simulated antennal tip trajectories and the joint angle time courses for each model, along with the same correlation analysis as used in Figure 4. The main effect of the ablation of these antennal proprioceptors was a strong increase in the working ranges of both antennal joints of the animals, as illustrated by the much wider ellipses of the antennal tip trajectories in Figure 5 (top). Hair field ablation experiments were simulated using the same three model variants as for intact animals, i.e., the pattern formation networks were exactly the same as before. The only difference was that the simulation of the ablation experiments required a change of the amplitude and offset settings of the oscillators controlling each joint (see Table 3). In all three models, the increase in amplitude of both joint oscillators resulted in the broadening of the antennal searching space. Despite the similarity in working ranges, the trajectory of the variable frequency model Mmsd again differed from that of the other two models; Mc and Mm models showed relatively persistent patterns in the tip trajectories, whereas Mmsd did not. Similar to the simulation of intact antennae, the cross-correlograms revealed a persistent phase coupling between SP and HS joints in Mc and Mm models. With regard to the mean cross-correlograms, the difference between the model and the experimental data was slightly larger for ablation experiments than in the intact situation (Figure 4). There were two reasons for this: first, the frequency spectrum used for the model was set according to data on intact animals; second, the phase difference varied slightly more in animals with hair field ablations compared to intact animals. A relatively low and broader central peak of the mean cross-correlogram (red dotted curve in Figure 5) of the ablation experiments stems from an overall shift of the frequency spectrum to lower frequencies, together with additional variability. Note that up- or down-scaling the frequency spectra of the Mc model by 50% did not change the characteristic shape of the antennal tip trajectory (see Supplementary Figure 1). Therefore, we used the frequency spectrum of intact animals for simulating the ablation experiments as well.


Stable phase-shift despite quasi-rhythmic movements: a CPG-driven dynamic model of active tactile exploration in an insect.

Harischandra N, Krause AF, Dürr V - Front Comput Neurosci (2015)

Simulation of hair field ablation experiments. (A) Representative trials of the original data from Krause et al. (2013). (B,C,D) follow the same arrangement and graphics details as described for Figure 4. In comparison with the simulation of intact antennae (Figure 4) only the amplitude μi and offset Ci (mean angle of oscillation) of the oscillators were changed according to the average values obtained from experimental data. The parameter values are tabulated in Table 3. The dotted red curves in the inserts show the average cross-correlogram for the data from ablation experiments (n = 5).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4543877&req=5

Figure 5: Simulation of hair field ablation experiments. (A) Representative trials of the original data from Krause et al. (2013). (B,C,D) follow the same arrangement and graphics details as described for Figure 4. In comparison with the simulation of intact antennae (Figure 4) only the amplitude μi and offset Ci (mean angle of oscillation) of the oscillators were changed according to the average values obtained from experimental data. The parameter values are tabulated in Table 3. The dotted red curves in the inserts show the average cross-correlogram for the data from ablation experiments (n = 5).
Mentions: Next, we tested to what extent our model was able to simulate experimental data on animals with sensory ablations. For this, we used data on antennal movement after sequential ablation of all dorsal antennal hair fields, as reported by Krause et al. (2013). Figure 5 shows the simulated antennal tip trajectories and the joint angle time courses for each model, along with the same correlation analysis as used in Figure 4. The main effect of the ablation of these antennal proprioceptors was a strong increase in the working ranges of both antennal joints of the animals, as illustrated by the much wider ellipses of the antennal tip trajectories in Figure 5 (top). Hair field ablation experiments were simulated using the same three model variants as for intact animals, i.e., the pattern formation networks were exactly the same as before. The only difference was that the simulation of the ablation experiments required a change of the amplitude and offset settings of the oscillators controlling each joint (see Table 3). In all three models, the increase in amplitude of both joint oscillators resulted in the broadening of the antennal searching space. Despite the similarity in working ranges, the trajectory of the variable frequency model Mmsd again differed from that of the other two models; Mc and Mm models showed relatively persistent patterns in the tip trajectories, whereas Mmsd did not. Similar to the simulation of intact antennae, the cross-correlograms revealed a persistent phase coupling between SP and HS joints in Mc and Mm models. With regard to the mean cross-correlograms, the difference between the model and the experimental data was slightly larger for ablation experiments than in the intact situation (Figure 4). There were two reasons for this: first, the frequency spectrum used for the model was set according to data on intact animals; second, the phase difference varied slightly more in animals with hair field ablations compared to intact animals. A relatively low and broader central peak of the mean cross-correlogram (red dotted curve in Figure 5) of the ablation experiments stems from an overall shift of the frequency spectrum to lower frequencies, together with additional variability. Note that up- or down-scaling the frequency spectra of the Mc model by 50% did not change the characteristic shape of the antennal tip trajectory (see Supplementary Figure 1). Therefore, we used the frequency spectrum of intact animals for simulating the ablation experiments as well.

Bottom Line: The effect of proprioceptor ablations could be simulated by changing the amplitude and offset parameters of the joint oscillators, only.We found that the phase-lead of the distal scape-pedicel (SP) joint relative to the proximal head-scape (HS) joint was essential for producing the natural tactile exploration behavior and, thus, for tactile efficiency.Based on our modeling results, we propose that a constant phase difference is coded into the CPG of the antennal motor system and that proprioceptors are acting locally to regulate the joint movement amplitude.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Cybernetics, Faculty of Biology, Bielefeld University Bielefeld, Germany ; Cognitive Interaction Technology Center of Excellence (CITEC), Bielefeld University Bielefeld, Germany.

ABSTRACT
An essential component of autonomous and flexible behavior in animals is active exploration of the environment, allowing for perception-guided planning and control of actions. An important sensory system involved is active touch. Here, we introduce a general modeling framework of Central Pattern Generators (CPGs) for movement generation in active tactile exploration behavior. The CPG consists of two network levels: (i) phase-coupled Hopf oscillators for rhythm generation, and (ii) pattern formation networks for capturing the frequency and phase characteristics of individual joint oscillations. The model captured the natural, quasi-rhythmic joint kinematics as observed in coordinated antennal movements of walking stick insects. Moreover, it successfully produced tactile exploration behavior on a three-dimensional skeletal model of the insect antennal system with physically realistic parameters. The effect of proprioceptor ablations could be simulated by changing the amplitude and offset parameters of the joint oscillators, only. As in the animal, the movement of both antennal joints was coupled with a stable phase difference, despite the quasi-rhythmicity of the joint angle time courses. We found that the phase-lead of the distal scape-pedicel (SP) joint relative to the proximal head-scape (HS) joint was essential for producing the natural tactile exploration behavior and, thus, for tactile efficiency. For realistic movement patterns, the phase-lead could vary within a limited range of 10-30° only. Tests with artificial movement patterns strongly suggest that this phase sensitivity is not a matter of the frequency composition of the natural movement pattern. Based on our modeling results, we propose that a constant phase difference is coded into the CPG of the antennal motor system and that proprioceptors are acting locally to regulate the joint movement amplitude.

No MeSH data available.