Functional organization of crayfish abdominal ganglia. III. Swimmeret motor neurons

Mulloney, Brian; Hall, Wendy M.

doi:10.1002/(sici)1096-9861(20000403)419:2<233::aid-cne7>3.0.co;2-y

Cited by 30 publications

(49 citation statements)

References 40 publications

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“…This centrally generated rhythm is the primary determinant of the swimmeret coordination (SI Text, sections 1.2, 2.1, and 3). Experiments on the crayfish neural ventral cord indicate that (i) each swimmeret is innervated by an anatomically separate and functionally independent CPG (22,33), and (ii) these CPGs are connected through ascending and descending coordinating neurons (19). Thus, the neural circuit driving metachronal swimmeret movements can be considered as a chain of four pairs of neuronal oscillators.…”

Section: A Robust Neural Mechanism Producing Phase Constancymentioning

confidence: 99%

Neural mechanism of optimal limb coordination in crustacean swimming

Zhang¹,

Guy²,

Mulloney

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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A fundamental challenge in neuroscience is to understand how biologically salient motor behaviors emerge from properties of the underlying neural circuits. Crayfish, krill, prawns, lobsters, and other long-tailed crustaceans swim by rhythmically moving limbs called swimmerets. Over the entire biological range of animal size and paddling frequency, movements of adjacent swimmerets maintain an approximate quarter-period phase difference with the more posterior limbs leading the cycle. We use a computational fluid dynamics model to show that this frequency-invariant stroke pattern is the most effective and mechanically efficient paddling rhythm across the full range of biologically relevant Reynolds numbers in crustacean swimming. We then show that the organization of the neural circuit underlying swimmeret coordination provides a robust mechanism for generating this stroke pattern. Specifically, the wave-like limb coordination emerges robustly from a combination of the half-center structure of the local central pattern generating circuits (CPGs) that drive the movements of each limb, the asymmetric network topology of the connections between local CPGs, and the phase response properties of the local CPGs, which we measure experimentally. Thus, the crustacean swimmeret system serves as a concrete example in which the architecture of a neural circuit leads to optimal behavior in a robust manner. Furthermore, we consider all possible connection topologies between local CPGs and show that the natural connectivity pattern generates the biomechanically optimal stroke pattern most robustly. Given the high metabolic cost of crustacean swimming, our results suggest that natural selection has pushed the swimmeret neural circuit toward a connection topology that produces optimal behavior. locomotion | coupled oscillators | phase locking | metachronal waves I t is widely believed that neural circuits have evolved to optimize behavior that increases reproductive fitness. Despite this belief, few studies have clearly identified the neural mechanisms producing optimal behaviors. The complexity of behaviors generally makes it difficult to assess their optimality, and neural circuits are often too complicated to concretely link neural mechanisms to the overt behavior. Energy-intensive locomotion such as steady swimming, walking, and flying provides important model systems for studying optimality because the goal of the behavior is clear and it is likely to have been optimized for efficiency (1). For example, the kinematics of locomotion has been shown to be optimal in the cases of the undulatory motion of the sandfish lizard and the lamprey (2, 3). On the other hand, the neural circuits underlying locomotion in most organisms are not sufficiently characterized to understand how they give rise to the optimal motor behavior. Because of the distinct frequency-invariant stroke pattern and the relative simplicity of the neuronal circuit, limb coordination of long-tailed crustaceans during steady swimming provides an ideal model system ...

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Section: A Robust Neural Mechanism Producing Phase Constancymentioning

confidence: 99%

Neural mechanism of optimal limb coordination in crustacean swimming

Zhang¹,

Guy²,

Mulloney

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…These findings suggest that NO is released from certain neurones that contribute to the swimmeret CPG network and modulates rhythmic beating activity of swimmeret motor neurones. NADPH-d-positive branches are extended within the lateral neuropils from the 2nd to 5th abdominal ganglion where dendrites of swimmeret motor neurones and relevant interneurones also projected (Mulloney and Hall, 2000) (H. Aonuma, personal communication). Further histochemical and immunocytochemical studies are needed to identify NOS-containing neurones within swimmeret CPGs.…”

Section: Discussion Endogenous No Levels Contribute To Swimmeret Beatmentioning

confidence: 99%

“…Rhythmic bursts of motor neurone spikes are generated by chains of serially repeated pairs of CPGs, one in each hemiganglion, that are interconnected both bilaterally across the midline and across abdominal segments Wiersma and Ikeda, 1964). The local pattern-generating circuits, including nonspiking local interneurones, and the pathways for intersegmental coordination have been well characterized by the detailed studies of Mulloney and colleagues (Mulloney and Hall, 2000;Mulloney and Hall, 2003;Mulloney and Hall, 2007;Mulloney et al, 2006;Paul and Mulloney, 1985;Smarandache et al, 2009;SmarandacheWellmann et al, 2013;Smarandache-Wellmann et al, 2014; for a review, see Mulloney and Smarandache, 2010;Mulloney and Smarandache-Wellmann, 2012). There is, however, almost no evidence that the rhythmic beating activity of the swimmeret motor neurones is affected by NO.…”

Section: Introductionmentioning

confidence: 99%

Nitric oxide modulates a swimmeret beating rhythm in the crayfish

Mita

Yoshida

Nagayama

2014

Journal of Experimental Biology

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The modulatory effects of nitric oxide (NO) and cAMP on the rhythmic beating activity of the swimmeret motor neurones in the crayfish were examined. Swimmerets are paired appendages located on the ventral side of each abdominal segment that show rhythmic beating activity during forward swimming, postural righting behaviour and egg ventilation in gravid females. In isolated abdominal nerve cord preparations, swimmeret motor neurones are usually silent or show a continuous low-frequency spiking activity. Application of carbachol, a cholinergic agonist, elicited rhythmic bursts of motor neurone spikes. The co-application of L-arginine, the substrate for NO synthesis with carbachol increased the burst frequency of the motor neurones. The co-application of the NO donor SNAP with carbachol also increased the burst frequency of the motor neurones. By contrast, co-application of a NOS inhibitor, L-NAME, with carbachol decreased beating frequency of the motor neurones. These results indicate that NO may act as a neuromodulator to facilitate swimmeret beating activity. The facilitatory effect of L-arginine was cancelled by co-application of the soluble guanylate cyclase (sGC) inhibitor ODQ suggesting that NO acts by activating sGC to promote the production of cGMP. Application of L-arginine alone or membrane-permeable cGMP analogue 8-Br-cGMP alone did not elicit rhythmic activity of motor neurones, but co-application of 8-Br-cGMP with carbachol increased bursting frequency of the motor neurones. Furthermore, application of the membrane-permeable cAMP analogue CPT-cAMP alone produced rhythmic bursting of swimmeret motor neurones, and the bursting frequency elicited by CPT-cAMP was increased by coapplication with L-arginine. Co-application of the adenylate cyclase inhibitor SQ22536 ceased rhythmic bursts of motor neurone spikes elicited by carbachol. These results suggest that a cAMP system enables the rhythmic bursts of motor neurone spikes and that a NO-cGMP signaling pathway increases cAMP activity to facilitate swimmeret beating.

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“…One method to stain a pool of motor neurons is to use backfills from the nerve N1 (Figure 22) 4,23 . Place a well of petroleum jelly around the posterior branch of the nerve N1 to backfill the pool of PS motor neurons.…”

Section: Discussionmentioning

confidence: 99%