Local-Distributed Integration by a Novel Neuron Ensures Rapid Initiation of Animal Locomotion

Department of Biology, University of Virginia, P.O. Box 400328, Charlottesville, VA 22904-4328, USA.
Journal of Neurophysiology (Impact Factor: 2.89). 10/2010; 105(1):130-44. DOI: 10.1152/jn.00507.2010
Source: PubMed


Animals are adapted to respond quickly to threats in their environment. In many invertebrate and some vertebrate species, the evolutionary pressures have resulted in rapidly conducting giant axons, which allow short response times. Although neural circuits mediating escape behavior are identified in several species, little attention has been paid to this behavior in the medicinal leech, a model organism whose neuronal circuits are well known. We present data that suggest an alternative to giant axons for the rapid initiation of locomotion. A novel individual neuron, cell E21, appears to be one mediator of this short-latency action in the leech. In isolated nerve cord and semi-intact preparations, cell E21 excitation initiates and extends swimming and reduces the cycle period. The soma of this cell is located caudally, but its axon extends nearly the entire length of the nerve cord. We found that cell E21 fires impulses following local sensory inputs anywhere along the body and makes excitatory synapses onto the gating cells that drive swimming behavior. These distributed input-output sites minimize the distance information travels to initiate swimming behavior, thus minimizing the latency between sensory input and motor output. We propose that this single cell E21 functions to rapidly initiate or modulate locomotion through its distributed synaptic connections.

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    • "In some systems, individual cells within a given group may contribute differentially to specific outputs or modulations of behavior (Heinrich, 2002; Kristan et al., 2005; Dubuc et al., 2008; Jordan et al., 2008; Buchanan, 2011). In the medicinal leech, specific swim command-like neurons appear more dedicated or multifunctional (Brodfuehrer and Burns, 1995; Brodfuehrer et al., 1995; Brodfuehrer et al., 2008; Mullins et al., 2011). The swim trigger neuron Tr-2, for example, can initiate or at other times terminate swimming (Brodfuehrer and Friesen, 1986; O'Gara and Friesen, 1995). "
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    ABSTRACT: In this report we posed the overarching question: What multiple contributions can a single neuron have on controlling the behavior of an animal, especially within a given context? To address this timely question, we studied the neuron R3b-1 in the medicinal leech. This bilaterally paired neuron descends from the cephalic ganglion and projects uninterrupted through the segmental ganglia comprising the nerve cord; its terminal arbors invade each hemi-ganglion. We discovered that a single R3b-1 neuron functions as a command neuron in the strictest sense, as it was both necessary and sufficient for fictive crawling behavior. Aside from these command-related properties, we determined that R3b-1 modulates the cycle period of crawl motor activity. R3b-1 has previously been shown to activate swimming behavior, but when the CNS was exposed to dopamine (DA), crawling became the exclusive locomotor pattern produced by R3b-1. DA exposure also led to bursting in R3b-1 that matched periods observed during fictive crawling, even when potential ascending inputs from crawl oscillators were removed. Although the above attributes render R3b-1 an intriguing cell, it is its ability to permit the coordination of the segmentally distributed crawl oscillators that makes this multifunctional neuron so notable. To our knowledge, this cell provides the first biological example of a single command neuron that is also vital for the intersegmental coordination of a locomotor behavior. Furthermore, our study highlights the importance of DA as an internal contextual cue that can integrate functional layers of the nervous system for adaptive behavior.
    Full-text · Article · Dec 2012 · The Journal of Neuroscience : The Official Journal of the Society for Neuroscience
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    • "were unexpected but are compatible with cell E21 properties in the broader context of leech behavior. The soma of cell E21 is posteriorly located, but its axon extends throughout the nerve cord; moreover, its spikes can be initiated in most or all ganglia (Mullins et al. 2011b). Therefore, cell E21 integrates sensory information from the entire body. "
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    ABSTRACT: The ability of nerve cords and spinal cords to exhibit fictive rhythmic locomotion in the absence of the brain is well-documented in numerous species. Although the brain is important for modulating the fictive motor output, it is broadly assumed that the functional properties of neuronal circuits identified in simplified preparations are conserved with the brain attached. We tested this assumption by examining the properties of a novel interneuron recently identified in the leech (Hirudo verbana) nerve cord. This neuron, cell E21, initiates and drives stereotyped fictive swimming activity in preparations of the isolated leech nerve cord deprived of the head brain. We report that, contrary to expectation, the motor output generated when cell E21 is stimulated in preparations with the brain attached is highly variable. Swim frequency and episode duration are increased in some of these preparations and decreased in others. Cell E21 controls swimming, in part, via excitatory synaptic interactions with cells 204, previously identified gating neurons that reliably initiate and strongly enhance leech swimming activity when the brain is absent. We found that in preparations with the brain present, the magnitude of the synaptic interaction from cell E21 to cell 204 is reduced by 50% and that cell 204-evoked responses also were highly variable. Intriguingly, most of this variability disappeared in semi-intact preparations. We conclude that neuronal circuit properties identified in reduced preparations might be fundamentally altered from those that occur in more physiological conditions.
    Full-text · Article · Feb 2012 · Journal of Neurophysiology
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    • "Swim-maintenance—In multiple species, the neurons or neuronal populations responsible for maintaining behavior over a period of time also control the cycle period of the behavior. (Kudo and Yamada 1987; Brodin et al. 1988; Böhm and Schilderger 1992; Cazalets et al. 1992; Di Prisco et al. 1997; Deliagina et al. 2000; Hedwig, 2000; Whelan et al. 2000; Dembrow et al. 2003; Paggett et al. 2004; Arshavsky et al. 2010; Mullins et al. 2011ab). In this study, although we saw a consistent reduction in cycle period in isolated SubEG-T preparations compared to the other nerve-cord classes (within the parameters of our analysis, early in the swim), swim duration was quite variable both within and between SubEG-T preparations, indicating that unknown factors contribute to the duration of individual swims. "
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    ABSTRACT: Locomotor systems are often controlled by specialized cephalic neurons and undergo modulation by sensory inputs. In many species, dedicated brain regions initiate and maintain behavior and set the duration and frequency of the locomotor episode. In the leech, removing the entire head brain enhances swimming, but the individual roles of its components, the supra- and subesophageal ganglia, in the control of locomotion are unknown. Here we describe the influence of these two structures and that of the tail brain on rhythmic swimming in isolated nerve cord preparations and in nearly intact leeches suspended in an aqueous, "swim-enhancing" environment. We found that, in isolated preparations, swim episode duration and swim burst frequency are greatly increased when the supraesophageal ganglion is removed, but the subesophageal ganglion is intact. The prolonged swim durations observed with the anterior-most ganglion removed were abolished by removal of the tail ganglion. Experiments on the nearly intact leeches show that, in these preparations, the subesophageal ganglion acts to decrease cycle period but, unexpectedly, also decreases swim duration. These results suggest that the supraesophageal ganglion is the primary structure that constrains leech swimming; however, the control of swim duration in the leech is complex, especially in the intact animal.
    Full-text · Article · Feb 2012 · Journal of Comparative Physiology
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