Behavioral Neuroscience 1996, Vol. 110, No. 4, 840-844 Copyright 19% by ihe American Psychological Association, Inc. 0735-7044/96/$3.00 Recovery From Habituation in Caenorhabditis elegans Is Dependent on Interstimulus Interval and Not Habituation Kinetics Stephen R. Wicks and Catharine H. Rankin University of British Columbia The habituation of the tap withdrawal reflex of Caenorhabditis elegans was assessed to determine whether the kinetics of recovery from habituation were dependent on the interstimulus interval (ISI) used during habituation training, or alternately, on the rate and asymptotic level of habituation produced at a given ISI. Two groups of intact animals were trained at either a I0-s (CON10) or a 60-s (CON60) ISI. Laser ablation was used In alter the habituation kinetics in one further group of animals (PLM10), independent of ISI. Although the PLM10 animals trained at a 10-s ISI habituated like CON60 worms, the recovery from habituation of the PLM10 animals very closely resembled the recovery of the CON10 worms. Thus recovery kinetics are dictated by consequences of a given ISI, which do not impact upon habituation rate and asymptote. This suggests the recruitment of multiple ISI-dependent processes during habituation in C. elegans. Habituation, defined as a decrement in responding as a consequence of repeated stimulation, is observed widely across phylogeny (Groves & Thompson, 1970). Thompson and Spen- cer (1966) have described a number of parametric criteria by which habituation can be distinguished from other forms of response decrement. These criteria include two major effects of the interstimulus interval (ISI) used during training. First, the kinetics of the habituation curve (i.e., initial rate and asymptotic level of habituation) are sensitive to ISI; animals trained at a shorter ISI will habituate faster and deeper than animals trained at a longer ISI. Second, the kinetics of recovery from habituation are sensitive to the ISI used during training; animals trained at a shorter ISI will recover from habituation faster than animals trained at a longer ISI. This second effect is somewhat paradoxical in that the animals that recover fastest are generally the same as those that appeared to be most habituated by the criteria of habituation rate or asymptote. This interpretation—that the kinetics of recovery are deter- mined by the ISI used during training—has remained unchal- lenged since it was introduced almost three decades ago, despite the existence of an obvious alternative hypothesis. It is also possible that the kinetics of recovery from habituation are Stephen R. Wicks, Program in Neuroscience, and Catharine H. Rankin, Department of Psychology', University of British Columbia, Vancouver, British Columbia, Canada. This work was supported by a National Sciences and Engineering Research Council of Canada (NSERC) scholarship and NSERC and Human Frontiers of Science operating grants. We wish to thank J. Byrne for asking the question that inspired this work and Jennifer Galloway for the collection of some of the data in this report. The nematode strain used in this work was provided by the Caenorhabditis Genetics Center, which is funded by the National Institutes of Health National Center for Research Resources. Correspondence concerning this article should be addressed to Catharine H. Rankin, Department of Psychology, University of British Columbia, 2136 West Mall, Vancouver, British Columbia, Canada V6T 1Z4. Electronic mail may be sent via Internet to crankin@cortex. psych.ubc.ca. determined by intrinsic properties of the habituation curve itself rather than the ISI per se. That is, the behavioral conse- quences of habituation at a given ISI (i.e., rate and asymptotic level of habituation) might determine the kinetics of recovery from habituation. However, since ISI also determines the kinetics of habituation, it has not been possible to address this question adequately. The nematode C. elegans has been developed as a model system within which this question may be addressed (Brenner, 1974; Wood, 1988). It demonstrates several forms of behav- ioral plasticity including habituation (Rankin, Beck, & Chiba, 1990). In response to a brief vibration of the substrate on which an animal moves (i.e., a tap), an intact wild-type worm will exhibit a withdrawal reflex which generally involves a reversal through some distance and a resumption of forward locomo- tion in a new direction (Rankin et al., 1990). The circuitry that mediates this reflex has been identified (Wicks & Rankin, 1995a). The tap withdrawal circuit receives input from five sensory neurons that partition the animal into two distinct mechanosensory fields (Charlie & Sulston, 1981): Anterior mechanosensory input leading to reversal responses is medi- ated by the anterior lateral microtubule (ALM) and anterior ventral microtubule (AVM) sensory neuron classes whereas posterior input leading to acceleration responses is mediated by the posterior lateral microtubule (PLM) sensory neuron class. Using laser ablation it is possible to modulate the sensory input to the tap withdrawal circuit and hence modulate the animal's response to a tap stimulus. Previously, it has been shown that this manipulation also affects both the rate and asymptotic level of habituation (Wicks & Rankin, in press). In this study, we utilize single-cell microsurgical ablations of the PLM tail-touch receptors to manipulate the rate and degree of habituation of the tap withdrawal reflex in C. elegans. In intact animals, the kinetics of habituation are determined by the relative strengths of two antagonistic reflexes—a reversal reflex and an acceleration reflex. The ablation of PLM alters habituation kinetics by eliminating the acceleration reflex, which is normally elicited by a tap stimulus. The kinetics of habituation in PLM-ablated animals are determined solely by 840 This document is copyrighted by the American Psychological Association or one of its allied publishers. 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