A separate local pattern-generating circuit controls the movements of each swimmeret in crayfish

Murchison, David; Chrachri, Abdesslam; Mulloney, Brian

doi:10.1152/jn.1993.70.6.2620

Cited by 74 publications

(70 citation statements)

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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%

“…We then show that the half-center structure of the local-CPG circuits (21)(22)(23) and the topology of the inter-CPG connections in the crayfish swimmeret circuit (19,20) provide a robust neural mechanism for producing the 0.25 phase-locked metachronal wave. This reduces the previously determined constraints on the phase response properties of the CPGs to a single condition.…”

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confidence: 98%

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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%

mentioning

confidence: 98%

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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“…Examples include swimmeret beating in the crayfish (Mulloney and Hall, 2007), insect flight (Robertson and Pearson, 1985) and swimming in the leech (Brodfuehrer et al, 1995a). Aside from swimmeret beating (Murchison et al, 1993), the kernel for rhythmic movements is often distributed across segmental units (e.g., flight circuit) (Robertson and Pearson, 1983) or is difficult to elicit and sustain in a single segmental unit. In the leech CNS, for example, serotonin can promote the semblance of the swim motor pattern in a single isolated ganglion, but it is weak and not sustained over time (Hocker et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

Dopamine Activates the Motor Pattern for Crawling in the Medicinal Leech

Puhl¹,

Mesce²

2008

J. Neurosci.

120

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Locomotion in segmented animals is thought to be based on the coupling of "unit burst generators," but the biological nature of the unit burst generator has been revealed in only a few animal systems. We determined that dopamine (DA), a universal modulator of motor activity, is sufficient to activate fictive crawling in the medicinal leech, and can exert its actions within the smallest division of the animal's CNS, the segmental ganglion. In the entire isolated nerve cord or in the single ganglion, DA induced slow antiphasic bursting (ϳ15 s period) of motoneurons known to participate in the two-step elongation-contraction cycle underlying crawling behavior. During each cycle, the dorsal (DE-3) and ventral (VE-4) longitudinal excitor motoneurons fired ϳ180°out of phase from the ventrolateral circular excitor motoneuron (CV), which marks the elongation phase. In many isolated whole nerve cords, DE-3 bursting progressed in an anterior to posterior direction with intersegmental phase delays appropriate for crawling. In the single ganglion, the dorsal (DI-1) and ventral (VI-2) inhibitory longitudinal motoneurons fired out of phase with each DE-3 burst, further confirming that the crawl unit burst generator exists in the single ganglion. All isolated ganglia of the CNS were competent to produce DA-induced robust fictive crawling, which typically lasted uninterrupted for 5-15 min. A quantitative analysis indicated that DA-induced crawling was not significantly different from electrically evoked or spontaneous crawling. We conclude that DA is sufficient to activate the full crawl motor program and that the kernel for crawling resides within each segmental ganglion.

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“…When they control motor patterns involving segmentally repeated muscles or appendages, e.g., swimming in lamprey (Cohen 1987a,b;Grillner et al 1991Grillner et al , 1995, leech (Friesen and Pearce 1993), and crayfish Murchison et al 1993) and peristaltic heartbeat activity in leeches (Calabrese and Peterson 1983;Peterson 1983a,b), these pattern generators are distributed along several segments of the nerve cord. They have often been characterized as being organized as autonomous segmental oscillators, which are coupled by intersegmental synaptic connections that coordinate the segmental oscillators so that a stable intersegmental pattern is produced.…”

Section: Introductionmentioning

confidence: 99%

Phase Relationships Between Segmentally Organized Oscillators in the Leech Heartbeat Pattern Generating Network

Masino

Calabrese

2002

Journal of Neurophysiology

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Motor pattern generating networks that produce segmentally distributed motor outflow are often portrayed as a series of coupled segmental oscillators that produce a regular progression (constant phase differences) in their rhythmic activity. The leech heartbeat central pattern generator is paced by a core timing network, which consists of two coupled segmental oscillators in segmental ganglia 3 and 4. The segmental oscillators comprise paired mutually inhibitory oscillator interneurons and the processes of intersegmental coordinating interneurons. As a first step in understanding the coordination of segmental motor outflow by this pattern generator, we describe the functional synaptic interactions, and activity and phase relationships of the heart interneurons of the timing network, in isolated nerve cord preparations. In the timing network, most (∼75%) of the coordinating interneuron action potentials were generated at a primary spike initiation site located in ganglion 4 (G4). A secondary spike initiation site in ganglion 3 (G3) became active in the absence of activity at the primary site. Generally, the secondary site was characterized by a reluctance to burst and a lower spike frequency, when compared with the primary site. Oscillator interneurons in G3 inhibited spike activity at both initiation sites, whereas oscillator interneurons in G4 inhibited spike activity only at the primary initiation site. This asymmetry in the control of spike activity in the coordinating interneurons may account for the observation that the phase of the coordinating interneurons is more tightly linked to the G3 than G4 oscillator interneurons. The cycle period of the timing network and the phase difference between the ipsilateral G3 and G4 oscillator interneurons were regular within individual preparations, but varied among preparations. This variation in phase differences observed across preparations implies that modulated intrinsic membrane and synaptic properties, rather than the pattern of synaptic connections, are instrumental in determining phase within the timing network.

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A separate local pattern-generating circuit controls the movements of each swimmeret in crayfish

Cited by 74 publications

References 0 publications

Neural mechanism of optimal limb coordination in crustacean swimming

Neural mechanism of optimal limb coordination in crustacean swimming

Dopamine Activates the Motor Pattern for Crawling in the Medicinal Leech

Phase Relationships Between Segmentally Organized Oscillators in the Leech Heartbeat Pattern Generating Network

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