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Sensitization of the Crayfish Lateral Giant Escape Reaction The Journal of Neuroscience April 1966, 6(4): 1013-1020 Sensitization of the Crayfish Lateral Giant Escape Reaction Franklin B. Krasne and David L. Glanzmanl Department of Psychology and Brain Research Institute, University of California, Los Angeles, California !30024 Most behavioral reactions that habituate can also be dishabit- leased by sensory neuron spikes by virtue of producing a per- uated by strong stimuli. In the best studied cases, dishabituation sistent decrease in the K+ currents that repolarize the terminal seems to be the result of an independent “sensitization” of the after a spike (Kandel and Schwartz, 1982; Klein et al., 1980). behavioral reaction that compensates for habituation without Recently, evidence has been obtained suggesting that identical necessarily abolishing it. Crayfish lateral giant (LG) neuron- effects, in exaggerated form, mediate classical conditioning of mediated escape reactions are one of the most fully analyzed the reflex (Carew et al., 198 1, 1983; Hawkins et al., 1983; Wal- behavioral reactions that are prone to habituation; however, sen- ters and Byrne, 1983). This possibility gives new importance to sitization/dishabituation of LG escape has not previously been the phenomenon of sensitization and generates a need to de- reported. termine the extent to which the findings regarding locus and Here, the effect of strong AC shocks to head or abdomen on mechanism of sensitization as well as those connecting sensi- the ability of 0.1 msec “test” shocks to sensory roots inner- tization to classical conditioning have generality. vating the tailfan to elicit an LG escape response was examined. A system that holds particular promise for probing the gen- Following single AC shocks, test shock threshold for eliciting erality of the findings from Aplysia is the lateral giant fiber (LG) LG escape reliably fell 5-80% and recovered over 15 min to 1 mediated escapereaction of the crayfish. The reaction habituates hr. When AC shocks and test shocks alternated at 90 set inter- (Wine et al., 1975), the circuitry mediating the reaction is well vals, test shock threshold rapidly dropped to an asymptote that analyzed (Krasne, 1969; Zucker, 1972a, b), and, though the was maintained as long as AC shocks were given (up to 2 hr); circuit mediating the reaction is more complex than that found following such repeated AC shocks, recovery often required a to mediate defensive withdrawal in Aplysia, the change respon- number of hours but was complete within 24. Comparable sen- sible for habituation is, as in Aplysia, a use-produced reduction sitization is seen in the response of interneuron A, the largest of transmitter release from sensory neuron terminals (Krasne, of a set of sensory interneurons that links afferents to LGs. AC 1976; Zucker, 1972b). However, neither sensitization nor any shocks (to either head or tail) no longer sensitize abdominal LG form of dishabituation has been reported in this system, and reflex circuitry if the nerve cord is severed between thorax and few signs of its existence have been seen during extensive be- abdomen. Thus, sensitization appears to depend on a neurally havioral and physiological investigations of the reflex (Krasne, conducted influence that arises in the rostra1 half of the animal. unpublished observations; R. S. Zucker, personal communi- Pharmacological evidence suggests that octopamine may me- cation). diate the sensitization. An attempt to obtain sensitization of the LG escape reaction at this time was prompted by the above considerations and was Most behavioral reactions that habituate can also be enhanced encouraged by the recent discovery that exogenous application in excitability, or sensitized, by presenting strong or novel stim- of octopamine, a naturally occurring monoamine of the crayfish uli (Groves and Thompson, 1970; Thompson and Spencer, 1966). nervous system, increases excitability of LG reactions (Glanz- From an adaptive point of view this sensitization can serve to man and Krasne, 1983). It was also hoped that these experi- heighten reactiveness to potential threats in novel or hostile ments would lead to the discovery of circumstances under which environments and restore responsiveness to stimuli previously an endogenous octopaminergic facilitatory system might oper- rendered ineffective by habituation (dishabituation). ate. To maximize the chances of finding the phenomenon, the Such sensitization has been particularly well analyzed in the experiments were done on free, intact animals with chronically Aplysia gill and siphon withdrawal reflex. There, the location implanted stimulating and recording electrodes. of the neural change responsible seems to be largely or entirely at the presynaptic side of synapses between relevant sensory Materials and Methods neurons and their followers, which is also the location of change Animals responsible for habituation of the reflex (seeKandel and Schwartz, Procumbarus clurkii about 2.5 cm rostrum-telson were used in all ex- 1982). The change responsible for sensitization is believed to periments. be induced by input to the terminal from a presynaptic “facil- itator” neuron that releases either a serotonin-like molecule or Preparation of animals a peptide when sensitizing stimuli are presented. This presyn- Recording and stimulating electrodeswere “skewers” made from 00 aptic facilitatory input increases the amount of transmitter re- stainlesssteel insect pins (Wards) insulated by Epoxylite except for a 0.5 mm segmentin the middle of the pin. To implant theseelectrodes Received Mar. 7, 1985; revised July 24, 1985; accepted Oct. 3, 1985. the thorax wasswaddled with wet cloth and the animal tied down ventral side up. Electrodesfor recordingventral cord activity wereinserted into This research was supported by United States Public Health Service Grant NS 08 108. We thank Tina Brown, Gretchen Garrett, Terri Teshiba, Tania Bentler, a small hole in one pleural plate, thrust through the soft belly skin near David Cho, and David Anisman for help in running experiments, and Carl Higgins the lateral margin of the abdomen,passed under or over the nerve cord, for typing the manuscript. which could be seenthrough the soft belly skin, thrust out through the Correspondence should be addressed to Franklin Krasne. contralateral skin and passedthrough a small hole in the contralateral ‘Present address: Center for Neurobiology, Howard Hughes Medical Institute, pleural plate. The skewerswere then adjusted so that the uninsulated 722 W. 168th Street, New York, NY 10032. region was in contact with the nerve cord (Fig. 1, A, and A,). In exper- Copyright 0 1986 Society for Neuroscience 0270-6474/86/041013-08$02.00/O iments where we were primarily interestedin firing of LGs, the skewer 1014 Krasne and Glanzman Vol. 6, No. 4, Apr. 1986 Figure 1. Preparation and sample traces. A, The preparation (A,) showing location of recording and test stimuli electrodes (detailed in A, and A,, re- spectively). A,, The position of skewer electrodes used for optimal recording of giant axons (left) and interneuron A (right). Inset in A,, The relative sizes and locations in the nerve cord of the LG (the giant dorsolateral axons) and intemeuron As (the large, ventrally lo- cated axons); the ventral artery is shown to scale underneath. B, Typical re- sponsesrecorded to test stimuli. In each trace, the first deflection is stimulus ar- tifact. B, and B,, Dots mark interneuron A spikes, the triangle the LG spikes, as seen by a dorsally placed skewer. Marked unit in B,, An interneuron A spike as seen by a ventrally placed skewer. Time calibration, 5 msec. was passed dorsal to the cord. When we were more interested in mon- itoring intemeuron A, the largest of the first-order sensory intemeurons Stimulation and recording in the LG escape reaction circuit, we passed the skewer ventrally between Test stimuli were 0.1 msec negative pulses isolated from ground by a cord and ventral artery. However, either type of placement usually transformer. Stimulus levels are reported here in arbitrary units, but a allowed firing of both LGs and intemeuron A to be recognized. Skewer level of 1.O is approximately 4.5 V at the stimulating electrodes. electrodes were placed in adjacent segments (usually lying between gan- LG reactions were unambiguously recognized by large LG spikes at glia 4 and 5 and ganglia 3 and 4) for recording large connective units recording electrodes followed by large muscle potentials (Fig. 1B). The differentially against an aquarium ground electrode. latency of LG firing was usually within about 4 msec, but occasionally Stimulating electrodes were skewers (Fig. 1, A!, and A,) placed so as longer. We used a 20 msec oscilloscope sweep; any LG firings occurring to lie against roots 2, 3, and 4 of the last abdominal ganglion. Prior to at greater than 20 msec were scored as nonresponses even though be- electrode implantation, the ipsilateral tailfan and more caudal interseg- havioral responses (some of which were long-latency LG reactions and mental joints were immobilized with a cyanoacrylate glue (Histoacryl some of which were non-giant-mediated tail flips) occurred. blue) to prevent flexion of the caudal part of the body or uropod move- Intemeuron A (see Kennedy, 197 1; Sigvardt et al., 1982) was defined ments that would alter the position of nerves being stimulated. The as the first unit with a spike easily discriminable from noise to fire more rostra1 electrode was then inserted into a hole in the fifth pleural reliably at less than 6 msec latency in an ascending stimulus series. Its plate on the side to be stimulated, slid rostromedially into the body latency, except with just-suprathreshold stimuli, was ordinarily about cavity and under the last sternal rib so as to lie over or under roots 2, 2-3 msec (Fig. 1, B, and B,). These characteristics were shown in in- 3, and 4, where they intersected the caudal edge of the rib in their dependent experiments to positively identify a unit whose conduction posterolateral course to the periphery, and thrust out through the soft velocity and receptive field were unique to interneuron A.
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