How the bending kinematics of swimming lampreys build negative pressure fields for suction thrust

Gemmell, Brad J.; Fogerson, Stephanie M.; Costello, John H.; Morgan, James L.; Dabiri, John O.; Colin, Sean P.

doi:10.1242/jeb.144642

Cited by 48 publications

(68 citation statements)

References 52 publications

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“…To increase the sensitivity of our swimming assay, we used ANY-maze software (Stoelting) to quantify kinematic parameters including maximum speed, total distance traveled, and latency to immobility. Notably, our observation of the maximum swimming speed of approximately three body lengths seconds −1 in uninjured lampreys was consistent with previous reports (Gemmell et al, 2016). As with the semiquantitative assessment, deficits were clearly observed immediately following TX but improved over the following weeks.…”

Section: Ptpσ Knockdown Modestly Impaired Behavioral Recovery From Txsupporting

confidence: 92%

PTPσ Knockdown in Lampreys Impairs Reticulospinal Axon Regeneration and Neuronal Survival After Spinal Cord Injury

Rodemer

Zhang

Sinitsa

et al. 2020

Front. Cell. Neurosci.

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Traumatic spinal cord injury (SCI) results in persistent functional deficits due to the lack of axon regeneration within the mammalian CNS. After SCI, chondroitin sulfate proteoglycans (CSPGs) inhibit axon regrowth via putative interactions with the LAR-family protein tyrosine phosphatases, PTPσ and LAR, localized on the injured axon tips. Unlike mammals, the sea lamprey, Petromyzon marinus, robustly recovers locomotion after complete spinal cord transection (TX). Behavioral recovery is accompanied by heterogeneous yet predictable anatomical regeneration of the lamprey's reticulospinal (RS) system. The identified RS neurons can be categorized as "good" or "bad" regenerators based on the likelihood that their axons will regenerate. Those neurons that fail to regenerate their axons undergo a delayed form of caspase-mediated cell death. Previously, this lab reported that lamprey PTPσ mRNA is selectively expressed in "bad regenerator" RS neurons, preceding SCI-induced caspase activation. Consequently, we hypothesized that PTPσ deletion would reduce retrograde cell death and promote axon regeneration. Using antisense morpholino oligomers (MOs), we knocked down PTPσ expression after TX and assessed the effects on axon regeneration, caspase activation, intracellular signaling, and behavioral recovery. Unexpectedly, PTPσ knockdown significantly impaired RS axon regeneration at 10 weeks post-TX, primarily due to reduced long-term neuron survival. Interestingly, cell loss was not preceded by an increase in caspase or p53 activation. Behavioral recovery was largely unaffected, although PTPσ knockdowns showed mild deficits in the recovery of swimming distance and latency to immobility during open field swim assays. Although the mechanism underlying the cell death following TX and PTPσ knockdown remains unknown, this study suggests that PTPσ is not a net negative regulator of long tract axon regeneration in lampreys.

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Section: Ptpσ Knockdown Modestly Impaired Behavioral Recovery From Txsupporting

confidence: 92%

PTPσ Knockdown in Lampreys Impairs Reticulospinal Axon Regeneration and Neuronal Survival After Spinal Cord Injury

Rodemer

Zhang

Sinitsa

et al. 2020

Front. Cell. Neurosci.

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“…Excluding the cells within an interrogation window that contain a body may be accomplished by dynamic masking. Dynamic masks may be isolated with image processing from a single-channel recording when the body is uniformly illuminated (Gemmell et al, 2016), but the lighting conditions that are amenable to recording particles are generally unfavorable for visualizing the body. As a consequence, the body is often manually drawn for each frame of the video (Gemmell et al, 2016;Tytell and Lauder, 2004), which is labor-intensive.…”

Section: Resultsmentioning

confidence: 99%

“…Dynamic masks may be isolated with image processing from a single-channel recording when the body is uniformly illuminated (Gemmell et al, 2016), but the lighting conditions that are amenable to recording particles are generally unfavorable for visualizing the body. As a consequence, the body is often manually drawn for each frame of the video (Gemmell et al, 2016;Tytell and Lauder, 2004), which is labor-intensive. As demonstrated presently, MSV provides the opportunity to resolve this challenge by producing images of the moving body under transmitted illumination that may be easily converted into a dynamic binary mask.…”

Section: Resultsmentioning

confidence: 99%

Multichannel Stroboscopic Videography (MSV): A technique for visualizing multiple channels for behavioral measurements

Soto

McHenry

2019

Journal of Experimental Biology

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Biologists commonly visualize different features of an organism using distinct sources of illumination. Such multichannel imaging has largely not been applied to behavioral studies because of the challenges posed by a moving subject. We address this challenge with the technique of multichannel stroboscopic videography (MSV), which synchronizes multiple strobe lights with video exposures of a single camera. We illustrate the utility of this approach with kinematic measurements of a walking cockroach (Gromphadorhina portentosa) and calculations of the pressure field around a swimming fish (Danio rerio). In both, transmitted illumination generated high-contrast images of the animal's body in one channel. Other sources of illumination were used to visualize the points of contact for the feet of the cockroach and the water flow around the fish in separate channels. MSV provides an enhanced potential for high-throughput experimentation and the capacity to integrate changes in physiological or environmental conditions in freely-behaving animals.

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“…7) (17,25,27). Even among anguilliform swimmers, the larval lampreys studied by Gemmell et al (25,26) have particularly large anterior body movements (28). These undulations rotate the body surface, which accelerate the adjacent fluid, strengthen the fluid's vorticity, and generate large regions of negative pressure (Fig.…”

Section: The Anterior Body Produces Thrust Due To Airfoil-like Mechanicsmentioning

confidence: 99%

“…Specifically, Gemmell et al (25,26) quantified the pressure distribution around larval lampreys and found that they produce negative pressures along the anterior parts of their bodies, resulting in thrust forces. In essence, larval lampreys suck themselves forward.…”

Section: Introductionmentioning

confidence: 99%

The fish body functions as an airfoil: surface pressures generate thrust during carangiform locomotion

Lucas

Lauder

Tytell

2020

Preprint

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The anterior body of many fishes is shaped like an airfoil turned on its side. With an oscillating angle to the swimming direction, such an airfoil experiences negative pressure due to both its shape and pitching movements. This negative pressure acts as thrust forces on the anterior body. Here, we apply a high-resolution, pressure-based approach to describe how two fishes, bluegill sunfish (Lepomis macrochirus Rafinesque) and brook trout (Salvelinus fontinalis Mitchill), swimming in the carangiform mode, the most common fish swimming mode, generate thrust on their anterior bodies using leading-edge suction mechanics, much like an airfoil. These mechanics contrast with those previously reported in lampreys -anguilliform swimmers -which produce thrust with negative pressure but do so through undulatory mechanics. The thrust produced on the anterior body of these carangiform swimmers through negative pressure comprises 28% of the total thrust produced over the body and caudal fin, substantially decreasing the net drag on the anterior body. On the posterior region, subtle differences in body shape and kinematics allow trout to produce more thrust than bluegill, suggesting that they may swim more effectively. Despite the large phylogenetic distance between these species, and differences near the tail, the pressure profiles around the anterior body are similar. We suggest that such airfoillike mechanics are highly efficient, because they require very little movement and therefore relatively little active muscular energy, and may be used by a wide range of fishes since many species have appropriately-shaped bodies. Significance StatementMany fishes have bodies shaped like a low-drag airfoil, with a rounded leading edge and a smoothly tapered trailing region, and move like an airfoil pitching at a small angle. This shape reduces drag but its significance for thrust production by fishes has not been investigated experimentally. By quantifying body surface pressures and forces during swimming, we find that the anterior body shape and movement allows fishes to produce thrust in the same way as an oscillating airfoil. This work helps us to understand how the streamlined body shape of fishes contributes, not only to reducing drag, but also directly to propulsion, and, by quantitatively linking form and function, leads to a more complete understanding fish evolution and ecology.

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How the bending kinematics of swimming lampreys build negative pressure fields for suction thrust

Cited by 48 publications

References 52 publications

PTPσ Knockdown in Lampreys Impairs Reticulospinal Axon Regeneration and Neuronal Survival After Spinal Cord Injury

PTPσ Knockdown in Lampreys Impairs Reticulospinal Axon Regeneration and Neuronal Survival After Spinal Cord Injury

Multichannel Stroboscopic Videography (MSV): A technique for visualizing multiple channels for behavioral measurements

The fish body functions as an airfoil: surface pressures generate thrust during carangiform locomotion

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