Correlates of Habituation of a Polysynaptic Reflex in Crayfish In Vivo and In Vitro

Abstract

Reflex leg levation habituates during repeated electrical stimulation of mechanosensory afferents in the dactyl of the fifth walking leg of the crayfish, Procambarus clarkii. This was investigated in decerebrate crayfish, and reproduced in an isolated thoracic ganglion preparation. In vivo, trains of stimuli delivered every 2.5 s produced a gradual decrease in the amplitude of the mechanical response, and a concomitant decrease in the number of impulses per burst in the levator muscle myogram. Near complete recovery occurred after 10 min rest, and transient dishabituation was observed after electrical stimulation of the telson. Less frequent or stronger stimuli led to less rapid habituation. In vitro, the same parametric characteristics of habituation were observed in the levator nerve responses, while the intrinsic variability of the reflex was reduced. The response decrement was shown to be unrelated to changes in the afferent excitation. Evoked polysynaptic excitatory postsynaptic potentials (EPSPs) in levator motorneurons decreased in parallel with the levator neurogram. This decrease was unrelated to any change in the resting membrane potential of the levator motorneurons. Interneurons with habituating EPSPs, antagonistic depressor motorneurons with habituating inhibitory postsynaptic potentials and non-habituating responses in other motorneuronal groups were also found. These findings point to a central locus of habituation upstream from the motorneurons, and offer prospects for a detailed investigation of the mechanisms of habituation in a polysynaptic system.

Adaptive motor control in crayfish

“…Similar results were obtained in an in vitro preparation of the ventral nerve cord with the considered leg attached. In this case, the compound EPSPs recorded from levator motoneurons and the compound inhibitory postsynaptic potentials recorded from depressor motoneurons progressively decreased (Marchand and Barnes, 1992).…”

“…In crayfish, a similar mechanism was demonstrated in the polysynaptic pathways supporting the escape response (Zucker, 1972b). Such mechanisms, however, were not demonstrated for habituation in other polysynaptic pathways such as defense response (Hawkins and Bruner, 1981) and leg levation reflex (Marchand and Barnes, 1992).…”

“…In intact crayfish, gentle pinching of the dactyl can elicit a brief levation of the leg. Such responses involve force-sensitive mechanoreceptors since, in vivo, the electrical stimulation (125-ms train at 100 Hz) of dactyl sensory afferents reproduce the levation response (Marchand and Barnes, 1992). However, if this electrical stimulation is repeated at 2.5-s intervals, the response (movement amplitude and number of muscle potentials in levator EMG) progressively decreases.…”

“…Unlike the escape response habituation, when habituation is established in the levation reflex arc, a train of shocks to the telson can achieve a dishabituation (Marchand and Barnes, 1992).…”

Habituation of LG-mediated tailflip in the crayfish

“…Habituation is subject to plasticity in invertebrates, as has been shown in the siphon withdrawal reflex in Aplysia (Kandel 2001(Kandel , 2009, the proboscis extension response of honeybees (Braun and Bicker 1992;Hammer and Menzel 1998) and the lateral giant (LG)-mediated tailflip of crayfish (Krasne 1969;Krasne and Woodsmall 1969;Zucker 1972b;Wine et al 1975;Bryan and Krasne 1977;Fricke 1984;Marchand and Barnes 1992;Edwards et al 1994;Krasne and Teshiba 1995;Edwards et al 1999;Araki and Nagayama 2003;Edwards 2009;Nagayama and Newland 2011). Since the LG-mediated tailflip is a stereotyped behavior (Wiersma 1947) and crayfish have a relatively simple central nervous system with relatively few and often identifiable neurons (Wine 1984;Nagayama et al 1993aNagayama et al , b, 1994, crayfish represent a good animal to analyze the cellular basis of habituation.…”