A mechanism for neuronal coincidence revealed in the crayfish antennule

Abstract

Startle reflexes employ specialized neuronal circuits and synaptic features for rapid transmission of information from sense organs to responding muscles. Successful excitation of these pathways requires the coincidence of sensory input at central synaptic contacts with giant fiber targets. Here we describe a pathway feature in the crayfish tailflip reflex: A position-dependent linear gradation in sensory axonal conduction velocities that can ensure the coincident arrival of impulses from near-field hydrodynamic sensilla along the crayfish antennules at their synaptic contacts with central nervous elements that drive startle behavior. This provides a previously unexplored mechanism to ensure optimum responses to sudden threatening stimuli. Preliminary findings indicate that axons supplying distally located sensilla increase their diameters at least ten-fold along the antennular flagella and raise the possibility that more modest, graduated, diameter changes in axons originating from progressively more proximal sensilla along the antennule underlie the observed modifications in axonal conduction velocity.crustacean ͉ sensory receptor ͉ startle reflex ͉ giant axons ͉ hydrodynamic sensilla

Identified antennular near-field receptors trigger reflex flicking in the crayfish

“…The data indicate that the sensilla are maximally sensitive, i.e. have the lowest thresholds, to impulsive stimuli originating close to the axial plane of the flagellum, as suggested by previous observations of spiking responsiveness using direct sinusoidal mechanical stimulation of the sensillar shaft (Mellon and Christison-Lagay, 2008). As we previously observed, however, the differences in directional sensitivities were not especially acute, except for a definite drop close to 180deg opposite the preferred direction, and they were even less so using near-field stimulation techniques, in which hydrodynamic disturbances close to the antennules originating from any direction are easily sensed.…”

“…The capillary tubing was coupled to the base of an excised crayfish lateral antennular flagellum by means of a short length of appropriately sized latex tubing, and the electrode holder was then connected to a low-level AC amplifier (Grass model P511, AstroMed Inc., West Warwick, RI, USA), an oscilloscope, a digitizer and audio equipment. Spiking activity from neurons associated with standing feathered sensilla, based on amplitude and waveform following stimulation with a small probe (Mellon and Christison-Lagay, 2008;Mellon, 2010), was used to identify a specific sensillum under ϫ100 magnification. The flagellum was then truncated one annulus distal to the sensillum, and saline was gently drawn through the flagellar blood sinus to flush it.…”

“…Previous work indicated that hydrodynamic stimulation of the lateral antennular flagellum evoked a flicking reflex in the crayfish Procambarus clarkii (Mellon, 1997). A subsequent study (Mellon and Christison-Lagay, 2008) then identified a specific population of near-field receptors, the standing feathered sensilla, linearly arrayed along the antennular flagella. We wished to confirm that weak hydrodynamic stimuli are able to excite the feathered sensilla, and to determine whether this specific population of sensors might trigger the flicking reflex previously found to be evoked by hydrodynamic stimuli.…”

“…The sensors comprising the afferent limb of the crayfish flagellar flick reflex in response to antennular stimulation have not been previously identified behaviorally or through examination of their central synaptic connections with EDM motor neurons. In this paper we present electrophysiological and behavioral evidence that standing feathered sensilla on the lateral antennular flagella, sensors that are very sensitive to directly imposed mechanical disturbances (Mellon and Christison-Lagay, 2008), respond readily to water particle motions, and constitute a specific afferent pathway that triggers antennular flicking. In addition, we present circumstantial evidence that spatial summation of inputs from the array of feathered sensilla decreases the latency of the flick response.…”

Neuronal Birth Order Identifies a Dimorphic Sensorineural Map

“…If these observations are extrapolated and combined with our findings, one emergent possibility is that the C-start will only be triggered by the coincident input on the Mauthner cell from "high sensitivity/low conduction velocity" and "lower sensitivity/high conduction velocity" neuronal classes. This model will safeguard the animal from startling upon stimuli that would depolarize one neuronal subclass but not the other, and is reminiscent of the escape strategy of crayfish, in which a mechanosensory stimulus activates parallel neuronal pathways with different reaction times that trigger the startle when arriving coincidently to an output command neuron (Reichert and Wine, 1982;Mellon and Christison-Lagay, 2008). However, more complex processing of hydrodynamic stimuli is possible, with multiple neuromasts contributing to the probability of depolarizing excitatory signals from the lateral line to the Mauthner cell (Korn et al, 1974).…”