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A Mechanism for Neuronal Coincidence Revealed in the Crayfish Antennule

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A Mechanism for Neuronal Coincidence Revealed in the Crayfish Antennule A mechanism for neuronal coincidence revealed in the crayfish antennule DeForest Mellon, Jr.* and Kate Christison-Lagay Department of Biology, University of Virginia, Charlottesville, VA 22903 Edited by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved August 6, 2008 (received for review May 7, 2008) Startle reflexes employ specialized neuronal circuits and synaptic duction velocities. Similar conduction-velocity adjustment mech- features for rapid transmission of information from sense organs anisms for achieving interneuronal or effector synchrony are to responding muscles. Successful excitation of these pathways known from a few central and efferent pathways in vertebrates requires the coincidence of sensory input at central synaptic (13, 14) as well as in cephalopod molluscs (15). Our findings contacts with giant fiber targets. Here we describe a pathway could be of critical importance in other systems where synchro- feature in the crayfish tailflip reflex: A position-dependent linear nous arrival of spikes may be required from spatially dispersed gradation in sensory axonal conduction velocities that can ensure primary sensory neurons, such as afferents from cercal filiform the coincident arrival of impulses from near-field hydrodynamic hairs in cockroaches, or lateral line neuromasts or skeletal– sensilla along the crayfish antennules at their synaptic contacts muscle spindles in vertebrates. with central nervous elements that drive startle behavior. This The medial giant-fiber system in crayfish, which mediates provides a previously unexplored mechanism to ensure optimum backward tailflips in response to sudden stimulation of the responses to sudden threatening stimuli. Preliminary findings thorax, legs, or head, is not nearly as well-examined as the lateral indicate that axons supplying distally located sensilla increase their giants, although it is thought that the synaptic organization of diameters at least ten-fold along the antennular flagella and raise afferent inputs to the medial giants is similar to that of the lateral the possibility that more modest, graduated, diameter changes in giants, and suddenness of stimulus onset is also critical for axons originating from progressively more proximal sensilla along evoking medial giant spikes (9, 16, 17). It seems reasonable to the antennule underlie the observed modifications in axonal con- hypothesize, therefore, that coincident arrival of afferent spikes duction velocity. at their synapses with the medial giants is as important as it is for lateral giant activation. In fact, the situation is even more critical crustacean ͉ sensory receptor ͉ startle reflex ͉ giant axons ͉ for the medial giants than for the lateral giants, whose distributed hydrodynamic sensilla afferent inputs to their synaptic targets in the several abdominal segmental ganglia comprise relatively short pathways; the two n prey–predator interactions, speed of responses to threaten- medial giants, by contrast, have only a single input and spike- Iing stimuli can mean the difference between capture and generating region—in the brain—and they receive afferents escape; thus, animals across phyletic boundaries have evolved from widely differing distances along the thoracic and head startle reflexes for rapid responses to approaching threats. The appendages via several different neuronal pathways (16). We neurophysiological substrates of startle behaviors include inter- have identified a small population of highly sensitive, bidirec- neuron axons of very large diameters that conduct impulses tional hydrodynamic receptor sensilla on the antennules (first rapidly to excite relevant efferent pathways (1–5) and electrical antennae) in the crayfish P. clarkii that potentially drives the synapses in the sensory-afferent pathways that trigger the inter- medial giant fibers, and whose dramatically calibrated axonal neurons and, in some systems, the motor neurons involved in the conduction properties must assure simultaneity of arrival in behavior (6). One of the startle behaviors that has been most spikes generated in the sensillar array. This constitutes a neu- intensively studied is a tailflip reflex initiated by one of the two ronal coincidence mechanism that should subserve precisely the sets of these high-speed interneurons—the lateral giant fi- sort of afferent synchrony requirement so critical for both the bers—in the ventral nerve cord of crayfish (7–12). Rectifying lateral giant and the medial giant pathways. electrical synapses between sensory-afferent terminals and the lateral giant fibers and between large tactile interneurons and Results the lateral giants, passes current directly into these paired axons Feathered sensilla are prominent near-field hydrodynamic sen- and, when several afferent terminals fire simultaneously, they sors on the crayfish abdomen (18, 19) and undoubtedly largely sum effectively to produce enhanced excitatory postsynaptic comprise the afferent limb of the lateral giant startle reflex. potentials in their targets (11). Furthermore, nonrectifying Morphologically similar standing feathered sensilla occur electrical interconnections among the afferent terminals exist sparsely distributed along the ventro-lateral aspects of the lateral whereby active terminals can directly recruit inactive terminals antennular flagellum and the ventro-medial aspects of the to provide additional depolarization to the lateral giants (12). medial flagellum (Fig. 1A). Their numbers range from 6–10 Coincidence of arrival of afferent input is crucial to these individual sensilla on each flagellum (mean ϭ 8, Ϯ0.6; n ϭ 11), processes and, thus, to initiate the startle response mediated by and they are most numerous along the basal 50% of the flagellar the lateral giants. What is not understood, however, is the neural axis (Fig. 1C). Like feathered sensilla described on the tailfan mechanism that explains the synchronous arrival at central (18) and earlier on the cephalothorax (20), each antennular synapses of sensory-afferent impulses from varying distances, a sensillum is supplied by two sensory neurons that have opposite problem that is especially critical for the other giant-fiber system in the crayfish, the medial giants, because of the long distances traversed by sensory spikes to their target synapses in the brain. Author contributions: D.M. designed research; D.M. and K.C.-L. performed research; D.M. Here we report that a population of hydrodynamic receptor and K.C.-L. analyzed data; and D.M. wrote the paper. sensilla on the antennules of the crayfish Procambarus clarkii The authors declare no conflict of interest. potentially drives the medial giant system to initiate startle This article is a PNAS Direct Submission. behavior and achieves simultaneity of impulse delivery through *To whom correspondence should be addressed. Email: [email protected]. graded, position-dependent variations in the sensory-axon con- © 2008 by The National Academy of Sciences of the USA 14626–14631 ͉ PNAS ͉ September 23, 2008 ͉ vol. 105 ͉ no. 38 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0804385105 Downloaded by guest on September 24, 2021 Fig. 1. Physical properties and response characteristics of standing feathered sensilla. (A) Head of Procambarus clarkii, indicating (arrows) both flagella of the right-hand antennule (Attribution: see ref. 30). (B) Scanning electron micrograph of a standing feathered sensillum on the lateral flagellum of P. clarkii. Other types of sensilla are in the background and foreground. (Scale bar, 100 ␮m.) (C) Distribution of standing feathered sensilla on 11 different lateral and medial flagella along their normalized lengths. (D) Upper and lower traces are extracellularly recorded electrical responses of neuronal pairs to sinusoidal mechanical stimulation of two feathered sensilla. Probe excursions were 200 ␮m peak-to-peak and generated differential responses to bidirectional movements parallel to the flagellar axis, with occasional electrical summations. (E) Polar plots of responses from a pair of neurons associated with one feathered sensillum to ramp deflections of the sensillum tip of 100 ␮m in extent. Response overlap near the least preferred stimulus direction is partially because of minute, unavoidable, mechanical vibrations of the probe and the high sensitivity of the associated neurons. (F) Relationship between spike frequency and stimulus-probe velocity of NEUROSCIENCE 42 sensory neurons associated with feathered sensilla on the lateral and medial flagella. Data points represent mean spiking frequency Ϯ1 SE. At higher velocities, response magnitude begins to saturate. The curve best fit by the data is a first-order exponential, y ϭ 112–107eϪx/832. directional preferences in their respective sensitivity to displace- latency of the medial giant electrical response was 12.59 msec ments. Typical electrophysiological recordings from two stand- (range: 6.96–17.32 msec, n ϭ 18), well within the range of ing feathered sensilla are shown in Fig. 1B to sinusoidal tip latencies for medial giant activation measured previously (16) displacements of 200 ␮m at a frequency of 1 Hz. The polar plots following sudden taps to the second antennae or the head. To shown in Fig. 1E indicate the mean, normalized spiking response determine whether the difference in response latencies—2.73 of a pair of neurons associated with a feathered sensillum to msec—obtained by the two stimulus methods might be because unidirectional 100-␮m tip excursions applied parallel to the of conduction time of the afferents within
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