Scaling of sensorimotor control in terrestrial mammals

More, Heather L.; Weber, Douglas J.; Hutchinson, John R.; Aung, Steven K.H.; Collins, David F.; Donelan, Max

doi:10.1016/j.cbpa.2009.04.510

Cited by 4 publications

(13 citation statements)

References 55 publications

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“…When animals are involved in extremely rapid control tasks such as predatory escape, where the neuromechanical system is pushed near its operating limit due to neural conduction delays (More et al, 2010), sensorimotor control bandwidth constraints impose fundamental limits on the gains that can be achieved for stable closed-loop control (Cowan et al, 2006;Elzinga et al, 2012). In such cases, animals require a well-tuned control system to compensate for the delays and locomotor dynamics, thus relying on shared processing between the neural and mechanical system (Cowan et al, 2006;Holmes et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Locomotion- and mechanics-mediated tactile sensing: antenna reconfiguration simplifies control during high-speed navigation in cockroaches

Mongeau

Demir

Lee

et al. 2013

Journal of Experimental Biology

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SUMMARYAnimals can expend energy to acquire sensory information by emitting signals and/or moving sensory structures. We propose that the energy from locomotion itself could permit control of a sensor, whereby animals use the energy from movement to reconfigure a passive sensor. We investigated high-speed, antenna-mediated tactile navigation in the cockroach Periplaneta americana. We discovered that the passive antennal flagellum can assume two principal mechanical states, such that the tip is either projecting backward or forward. Using a combination of behavioral and robotic experiments, we demonstrate that a switch in the antenna's state is mediated via the passive interactions between the sensor and its environment, and this switch strongly influences wall-tracking control. When the tip of the antenna is projected backward, the animals maintain greater body-to-wall distance with fewer body collisions and less leg-wall contact than when the tip is projecting forward. We hypothesized that distally pointing mechanosensory hairs at the tip of the antenna mediate the switch in state by interlocking with asperities in the wall surface. To test this hypothesis, we performed laser ablation of chemo-mechanosensory hairs and added artificial hairs to a robotic antenna. In both the natural and artificial systems, the presence of hairs categorically increased an antenna's probability of switching state. Antennal hairs, once thought to only play a role in sensing, are sufficient for mechanically reconfiguring the state of the entire antenna when coupled with forward motion. We show that the synergy between antennal mechanics, locomotion and the environment simplifies tactile sensing.

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Section: Introductionmentioning

confidence: 99%

Locomotion- and mechanics-mediated tactile sensing: antenna reconfiguration simplifies control during high-speed navigation in cockroaches

Mongeau

Demir

Lee

et al. 2013

Journal of Experimental Biology

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“…A giraffe's extreme height, although helpful for feeding, may present challenges for the nervous system to control movement -for example, delays associated with conducting neural impulses down longer body segments. Here we study the neurophysiology of the giraffe hindlimb in terms of two characteristics of sensorimotor performance that we have previously termed 'responsiveness' and 'resolution' (More et al, 2010). These refer to how quickly and precisely, respectively, an animal can sense and respond to a stimulus.…”

Section: Introductionmentioning

confidence: 99%

“…This study is the first to examine the histology of giraffe hindlimb peripheral nerves and their functional characteristics. It adds to our earlier work on the scaling of nerve conduction delay (More et al, 2010) and investigates two additional delays, as well as resolution.…”

Section: Introductionmentioning

confidence: 99%

“…For example, sensing delay, synaptic delay and neuromuscular junction delay are fairly short, on the order of milliseconds (Renshaw, 1940;Katz and Miledi, 1965;Prochazka et al, 1976;Datyner and Gage, 1980;Burke et al, 1983), whereas nerve conduction delay, electromechanical delay and force generation delay can be relatively long, on the order of tens of milliseconds (Burke et al, 1973;Raikova et al, 2007;More et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

“…For a given body size, if an animal has more sensory nerve fibers it can more precisely sense the location of a stimulus; similarly, if an animal has more motor units it can generate finer gradations of muscle force within the same force range (Enoka, 1995;More et al, 2010). Therefore, like responsiveness, resolution is partially dependent on body dimensions.…”

Section: Introductionmentioning

confidence: 99%

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Sensorimotor responsiveness and resolution in the giraffe

O’Connor

Brøndum

et al. 2013

Journal of Experimental Biology

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SUMMARYThe ability of an animal to detect and respond to changes in the environment is crucial to its survival. However, two elements of sensorimotor control -the time required to respond to a stimulus (responsiveness) and the precision of stimulus detection and response production (resolution) -are inherently limited by a competition for space in peripheral nerves and muscles. These limitations only become more acute as animal size increases. In this paper, we investigated whether the physiology of giraffes has found unique solutions for maintaining sensorimotor performance in order to compensate for their extreme size. To examine responsiveness, we quantified three major sources of delay: nerve conduction delay, muscle electromechanical delay and force generation delay. To examine resolution, we quantified the number and size distribution of nerve fibers in the sciatic nerve. Rather than possessing a particularly unique sensorimotor system, we found that our measurements in giraffes were broadly comparable to size-dependent trends seen across other terrestrial mammals. Consequently, both giraffes and other large animals must contend with greater sensorimotor delays and lower innervation density in comparison to smaller animals. Because of their unconventional leg length, giraffes may experience even longer delays compared with other animals of the same mass when sensing distal stimuli. While there are certainly advantages to being tall, there appear to be challenges as well -our results suggest that giraffes are less able to precisely and accurately sense and respond to stimuli using feedback alone, particularly when moving quickly.

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Electro-Mechanical Delay in Hill-Type Muscle Models

Mörl¹,

Siebert

Schmitt

et al. 2012

J. Mech. Med. Biol.

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In this study, we investigated to which extent Hill-type muscle models can explain the electromechanical delay (EMD). The EMD is a phenomenon that has been well examined in muscle experiments. The EMD is the time lag between a change in muscle stimulation and the subsequent measurable change in muscle force. A variety of processes as, e.g., signal conduction and interaction of contractile and elastic muscle structures contribute to the EMD. The relative contributions of the particular processes have not been fully unveiled so far. Thereto, we simulated isometric muscle contractions using two Hill-type muscle models. Their parameters were extracted from experiments on the cat soleus muscle. In agreement with literature data, predicted EMD values depend on muscle-tendon complex (MTC) length and increase when reducing MTC lengths. The highest EMD values (28 and 27 ms) occur at the lowest MTC length examined (78% of optimal length). Above optimal MTC length, we¯nd EMD saturation (2 ms) in one model. In the other model, the EMD slightly re-increases up to 9 ms at the highest length examined (113% of optimal length). The EMD values predicted by the two models were then compared to EMD values found in the same experiments from which the muscle parameters were extracted. At optimal MTC length, the EMD values, mapping ion release and visco-elastic interactions, predicted by both models (3.5 and 5.5 ms) just partly account for the measured § Corresponding author. value (15.8 ms). The biggest share (about 9 ms) of the remaining 11 ms can be attributed to signal conduction along the nerve and on the muscle surface. Further potential sources of delayed force generation are discussed.

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Scaling of sensorimotor control in terrestrial mammals

Cited by 4 publications

References 55 publications

Locomotion- and mechanics-mediated tactile sensing: antenna reconfiguration simplifies control during high-speed navigation in cockroaches

Locomotion- and mechanics-mediated tactile sensing: antenna reconfiguration simplifies control during high-speed navigation in cockroaches

Sensorimotor responsiveness and resolution in the giraffe

Electro-Mechanical Delay in Hill-Type Muscle Models

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