Encoding of near-range spatial information by descending interneurons in the stick insect antennal mechanosensory pathway

Ache, Jan Marek; Dürr, Volker

doi:10.1152/jn.00281.2013

Cited by 13 publications

(31 citation statements)

References 58 publications

(58 reference statements)

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“…hindlegs (Ache and Dürr, 2013). Spatial co-ordination has also been described in locusts and horse-head grasshoppers, both of which adjust their front leg positions in 3D space according to visual cues (Niven et al, 2010;Niven et al, 2012).…”

Section: Research Articlementioning

confidence: 95%

“…S1) (Dean and Wendler, 1983), and the hindlegs follow the middle legs in 3D space (Figs 2-4). Indeed, descending interneurons of the head ganglia were shown to encode antennal posture (Ache and Dürr, 2013) and local interneurons of the metathoracic ganglion encode the positions of middle leg tarsus (Brunn and Dean, 1994). This cascade of information transfer between adjacent limbs is likely to improve locomotion efficiency by helping each leg to find appropriate foothold in complex natural environments.…”

Section: Sensory Control Of Foot Placementmentioning

confidence: 99%

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Spatial coordination of foot contacts in unrestrained climbing insects

Theunissen

Vikram

Dürr

2014

Journal of Experimental Biology

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Animals that live in a spatially complex environment such as the canopy of a tree, constantly need to find reliable foothold in threedimensional (3D) space. In multi-legged animals, spatial co-ordination among legs is thought to improve efficiency of finding foothold by avoiding searching-movements in trailing legs. In stick insects, a 'targeting mechanism' has been described that guides foot-placement of hind-and middle legs according to the position of their leading ipsilateral leg. So far, this mechanism has been shown for standing and tethered walking animals on horizontal surfaces. Here, we investigate the efficiency of this mechanism in spatial limb coordination of unrestrained climbing animals. For this, we recorded whole-body kinematics of freely climbing stick insects and analysed foot placement in 3D space. We found that touch-down positions of adjacent legs were highly correlated in all three spatial dimensions, revealing 3D co-ordinate transfer among legs. Furthermore, targeting precision depended on the position of the leading leg. A second objective was to test the importance of sensory information transfer between legs. For this, we ablated a proprioceptive hair field signaling the levation of the leg. After ablation, the operated leg swung higher and performed unexpected searching movements. Furthermore, targeting of the ipsilateral trailing leg was less precise in anteroposterior and dorsoventral directions. Our results reveal that the targeting mechanism is used by unrestrained climbing stick insects in 3D space and that information from the trochanteral hair field is used in ipsilateral spatial co-ordination among legs.

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Section: Research Articlementioning

confidence: 95%

Section: Sensory Control Of Foot Placementmentioning

confidence: 99%

Spatial coordination of foot contacts in unrestrained climbing insects

Theunissen

Vikram

Dürr

2014

Journal of Experimental Biology

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“…The DIN models simulate the multivariate information transfer from an active touch system to a motor control system. For three reasons, we choose the antennal mechanosensitive pathway of the stick insect Carausius morosus as the paragon for our model: i) A behavioural reach-to-grasp paradigm in stick insects [ 5 ] requires fast information transfer of antennal posture and movement; ii) both the antennal tactile system [ 12 , 13 ] and the thoracic leg motor control networks [ 14 , 15 ] are well studied; and iii) a population of spiking DINs has been described that conveys diverse, multivariate information about antennal posture and movement to thoracic neural networks [ 16 ]; [ 17 ]. Our objective was to devise models of several different DIN types, including position- and motion-sensitive DINs, drawing from a small set of computational modules such as linear filters and a noisy spike generator.…”

Section: Introductionmentioning

confidence: 99%

“…Our model explains spike response patterns of four distinct DIN classes as described by [ 16 ], making it an exceptionally complete and versatile model of a descending neural pathway. We show that input from hair fields alone is sufficient to explain a large fraction of the response variants found in a real DIN population, including position-and motion-sensitive, ON-type, and OFF-type interneurons.…”

Section: Introductionmentioning

confidence: 99%

A Computational Model of a Descending Mechanosensory Pathway Involved in Active Tactile Sensing

Ache

Dürr

2015

PLoS Comput Biol

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Many animals, including humans, rely on active tactile sensing to explore the environment and negotiate obstacles, especially in the dark. Here, we model a descending neural pathway that mediates short-latency proprioceptive information from a tactile sensor on the head to thoracic neural networks. We studied the nocturnal stick insect Carausius morosus, a model organism for the study of adaptive locomotion, including tactually mediated reaching movements. Like mammals, insects need to move their tactile sensors for probing the environment. Cues about sensor position and motion are therefore crucial for the spatial localization of tactile contacts and the coordination of fast, adaptive motor responses. Our model explains how proprioceptive information about motion and position of the antennae, the main tactile sensors in insects, can be encoded by a single type of mechanosensory afferents. Moreover, it explains how this information is integrated and mediated to thoracic neural networks by a diverse population of descending interneurons (DINs). First, we quantified responses of a DIN population to changes in antennal position, motion and direction of movement. Using principal component (PC) analysis, we find that only two PCs account for a large fraction of the variance in the DIN response properties. We call the two-dimensional space spanned by these PCs ‘coding-space’ because it captures essential features of the entire DIN population. Second, we model the mechanoreceptive input elements of this descending pathway, a population of proprioceptive mechanosensory hairs monitoring deflection of the antennal joints. Finally, we propose a computational framework that can model the response properties of all important DIN types, using the hair field model as its only input. This DIN model is validated by comparison of tuning characteristics, and by mapping the modelled neurons into the two-dimensional coding-space of the real DIN population. This reveals the versatility of the framework for modelling a complete descending neural pathway.

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“…When these delays are combined with body dynamics, they could make it difficult to maintain stable control (Cowan et al, 2006;Lee et al, 2008;Elzinga et al, 2012). The 23 ms median latency we have measured is longer than the ∼10 ms latency that has been measured by stimulating the antenna near its base and measuring activity in descending interneurons in cockroaches (Burdohan and Comer, 1990), stick insects (Ache and Durr, 2013) and crickets (Gebhardt and Honegger, 2001). We reason that this difference in latency is due to the location of stimulation as these studies deflected the basal segments of the antenna (scape and pedicel) while we displaced the antenna near its tip.…”

Section: Tuning Of Individual Mechanoreceptors By Latency and Temporamentioning

confidence: 75%

Sensory processing within antenna enables rapid implementation of feedback control for high-speed running maneuvers

Mongeau

Sponberg

Miller

2015

Journal of Experimental Biology

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Animals are remarkably stable during high-speed maneuvers. As the speed of locomotion increases, neural bandwidth and processing delays can limit the ability to achieve and maintain stable control. Processing the information of sensory stimuli into a control signal within the sensor itself could enable rapid implementation of whole-body feedback control during high-speed locomotion. Here, we show that processing in antennal afferents is sufficient to act as the control signal for a fast sensorimotor loop. American cockroaches Periplaneta americana use their antennae to mediate escape running by tracking vertical surfaces such as walls. A control theoretic model of wall following predicts that stable control is possible if the animal can compute wall position (P) and velocity, its derivative (D). Previous whole-nerve recordings from the antenna during simulated turning experiments demonstrated a population response consistent with P and D encoding, and suggested that the response was synchronized with the timing of a turn executed while wall following. Here, we record extracellularly from individual mechanoreceptors distributed along the antenna and show that these receptors encode D and have distinct latencies and filtering properties. The summed output of these receptors can be used as a control signal for rapid steering maneuvers. The D encoding within the antenna in addition to the temporal filtering properties and P dependence of the population of afferents support a sensory-encoding notion from control theory. Our findings support the notion that peripheral sensory processing can enable rapid implementation of whole-body feedback control during rapid running maneuvers.

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Encoding of near-range spatial information by descending interneurons in the stick insect antennal mechanosensory pathway

Abstract: Ache JM, Dürr V. Encoding of near-range spatial information by descending interneurons in the stick insect antennal mechanosensory pathway.

Cited by 13 publications

References 58 publications

Spatial coordination of foot contacts in unrestrained climbing insects

Spatial coordination of foot contacts in unrestrained climbing insects

A Computational Model of a Descending Mechanosensory Pathway Involved in Active Tactile Sensing

Sensory processing within antenna enables rapid implementation of feedback control for high-speed running maneuvers

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