Movement encoding by a stretch receptor in the soft-bodied caterpillar,<i>Manduca sexta</i>

Simon, Michael A.; Trimmer, Barry A.

doi:10.1242/jeb.023507

Cited by 28 publications

(27 citation statements)

References 54 publications

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“…Because their muscle anatomy is known so well (Barth, 1937;Eaton, 1988;Kopec, 1919;Libby, 1959;Snodgrass, 1961;Snodgrass, 1993) and each muscle is generally innervated by a single motoneuron (Levine and Truman, 1985;Taylor and Truman, 1974;Weeks and Truman, 1984) these caterpillars show great promise for electromyographic studies of soft-bodied locomotion Dominick and Truman, 1986;Johnston and Levine, 1996a;Johnston and Levine, 1996b;Mezoff et al, 2004;Simon and Trimmer, 2009). Manduca is a relatively large insect (which helps force measurements) using four pairs of abdominal prolegs and a pair of terminal prolegs to generate most of its motion.…”

Section: Manduca Locomotion and Mechanicsmentioning

confidence: 99%

The substrate as a skeleton: ground reaction forces from a soft-bodied legged animal

Lin

Trimmer

2010

Journal of Experimental Biology

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SUMMARY The measurement of forces generated during locomotion is essential for the development of accurate mechanical models of animal movements. However, animals that lack a stiff skeleton tend to dissipate locomotor forces in large tissue deformation and most have complex or poorly defined substrate contacts. Under these conditions, measuring propulsive and supportive forces is very difficult. One group that is an exception to this problem is lepidopteran larvae which, despite lacking a rigid skeleton, have well-developed limbs (the prolegs) that can be used for climbing in complex branched structures and on a variety of surfaces. Caterpillars therefore are excellent for examining the relationship between soft body deformation and substrate reaction forces during locomotion. In this study, we devised a method to measure the ground reaction forces (GRFs) at multiple contact points during crawling by the tobacco hornworm (Manduca sexta). Most abdominal prolegs bear similar body weight during their stance phase. Interestingly, forward reaction forces did not come from pushing off the substrate. Instead, most positive reaction forces came from anterior abdominal prolegs loaded in tension while posterior legs produced drag in most instances. The counteracting GRFs effectively stretch the animal axially during the second stage of a crawl cycle. These findings help in understanding how a terrestrial soft-bodied animal can interact with its substrate to control deformation without hydraulic actuation. The results also provide insights into the behavioral and mechanistic constraints leading to the evolution of diverse proleg arrangements in different species of caterpillar.

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Section: Manduca Locomotion and Mechanicsmentioning

confidence: 99%

The substrate as a skeleton: ground reaction forces from a soft-bodied legged animal

Lin

Trimmer

2010

Journal of Experimental Biology

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“…This is known to generate different forcelength relationships (work loops) in M. sexta muscles and to alter the relative contributions of positive and dissipative work outputs . This could explain why there is a shift in the timing of muscle activation during crawling in the two orientations even when the stepping patterns are the same [Finlayson and Lowenstein, 1958;Grueber et al, 2001;Simon and Trimmer, 2009;van Griethuijsen and Trimmer, 2009] ( fig. 8 ).…”

Section: Multisite Recordings Reveal a Functional Difference In Dim Mmentioning

confidence: 99%

“…For example, during climbing, fluids and tissues will tend to accumulate in posterior segments, increasing the baseline tension on the body wall in those segments. Stretch sensitive mechanosensors such as the stretch receptor organs [Finlayson and Lowenstein, 1958;Simon and Trimmer, 2009] or the multidendritic neuron plexus in the body wall [Grueber et al, 2001] are clearly candidates for relaying this information. M. sexta could use comparisons of the mechanosensory activity in different body segments to identify its orientation.…”

Section: Implications For Sensingmentioning

confidence: 99%

Orientation-Dependent Changes in Single Motor Neuron Activity during Adaptive Soft-Bodied Locomotion

Metallo

Trimmer²

2015

Brain Behav Evol

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Recent major advances in understanding the organizational principles underlying motor control have focused on a small number of animal species with stiff articulated skeletons. These model systems have the advantage of easily quantifiable mechanics, but the neural codes underlying different movements are difficult to characterize because they typically involve a large population of neurons controlling each muscle. As a result, studying how neural codes drive adaptive changes in behavior is extremely challenging. This problem is highly simplified in the tobacco hawkmoth Manduca sexta, which, in its larval stage (caterpillar), is predominantly soft-bodied. Since each M. sexta muscle is innervated by one, occasionally two, excitatory motor neurons, the electrical activity generated by each muscle can be mapped to individual motor neurons. In the present study, muscle activation patterns were converted into motor neuron frequency patterns by identifying single excitatory junction potentials within recorded electromyographic traces. This conversion was carried out with single motor neuron resolution thanks to the high signal selectivity of newly developed flexible microelectrode arrays, which were specifically designed to record from M. sexta muscles. It was discovered that the timing of motor neuron activity and gait kinematics depend on the orientation of the plane of motion during locomotion. We report that, during climbing, the motor neurons monitored in the present study shift their activity to correlate with movements in the animal's more anterior segments. This orientation-dependent shift in motor activity is in agreement with the expected shift in the propulsive forces required for climbing. Our results suggest that, contrary to what has been previously hypothesized, M.sexta uses central command timing for adaptive load compensation.

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“…For example, when filiform tactile sensors on the body surface of Manduca sexta are in contact with the environment they are inevitably activated by movements of the caterpillar itself [23]. Similarly, the response properties of some proprioceptive receptors such as the stretch-receptor organs in Manduca sexta suggest they are not well suited for real-time sensing of segment length [24] but they are activated by external forces [25]. It is therefore possible that by sensing self-deformation an animal such as Manduca sexta is able to collect critical information about its interaction with the environment.…”

Section: Introductionmentioning

confidence: 99%

Gait control in a soft robot by sensing interactions with the environment using self-deformation

et al. 2016

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All animals use mechanosensors to help them move in complex and changing environments. With few exceptions, these sensors are embedded in soft tissues that deform in normal use such that sensory feedback results from the interaction of an animal with its environment. Useful information about the environment is expected to be embedded in the mechanical responses of the tissues during movements. To explore how such sensory information can be used to control movements, we have developed a soft-bodied crawling robot inspired by a highly tractable animal model, the tobacco hornworm Manduca sexta. This robot uses deformations of its body to detect changes in friction force on a substrate. This information is used to provide local sensory feedback for coupled oscillators that control the robot's locomotion. The validity of the control strategy is demonstrated with both simulation and a highly deformable three-dimensionally printed soft robot. The results show that very simple oscillators are able to generate propagating waves and crawling/inching locomotion through the interplay of deformation in different body parts in a fully decentralized manner. Additionally, we confirmed numerically and experimentally that the gait pattern can switch depending on the surface contact points. These results are expected to help in the design of adaptable, robust locomotion control systems for soft robots and also suggest testable hypotheses about how soft animals use sensory feedback.

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Movement encoding by a stretch receptor in the soft-bodied caterpillar,Manduca sexta

Cited by 28 publications

References 54 publications

The substrate as a skeleton: ground reaction forces from a soft-bodied legged animal

The substrate as a skeleton: ground reaction forces from a soft-bodied legged animal

Orientation-Dependent Changes in Single Motor Neuron Activity during Adaptive Soft-Bodied Locomotion

Gait control in a soft robot by sensing interactions with the environment using self-deformation

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