Behavioral analysis of internal memory states using cooling-induced retrograde amnesia in Limax flavus

Abstract

Temporal evolution of internal memory states in a terrestrial mollusk, Limax flavus, was studied using cooling-induced retrograde amnesia. The slug was conditioned to avoid carrot odor by temporally correlated presentation of carrot juice and a bitter-taste stimulus of quinidine sulfate. We could induce retrograde amnesia by cooling of the conditioned slug immediately after the training trial. Thus, we studied the memory states in the slug using the retrograde amnesia according to strategies used in the studies of memory states in mammals or insects. In the early process of memory acquisition, at least two distinctive memory states were observed, short-term memory and long-term memory (LTM). For LTM, two states were also observed. One was a reactivated state of LTM, which was sensitive to the cooling used to induce the amnesia. The other was a so-called resting state of LTM, which was insensitive to cooling. A few days after memory acquisition, further evolution was observed in that the amnesia could not be induced even if the memory trace was reactivated. The results obtained in Limax flavus was comparable with those obtained in a variety of animals.

Retrieval and Reconsolidation: Toward a Neurobiology of Remembering

“…www.learnmem.org after acquisition or 1 min after the well-established memory is reactivated by a brief exposure to the carrot conditioned stimulus (Yamada et al 1992;Sekiguchi et al 1997).…”

Spontaneous Recovery from Extinction Depends on the Reconsolidation of the Acquisition Memory in an Appetitive Learning Paradigm in the Honeybee (Apis mellifera)

“…This acquisition memory then undergoes a consolidation process that results in its stabilization and hence the stabilization of the CR, a process that is referred to as reconsolidation (Spear, 1973;Sara, 2000;Nader, 2003;Dudai and Eisenberg, 2004). Either consolidation of extinction memory or reconsolidation of the acquisition memory has been observed in different studies in vertebrates (Nader et al, 2000;Berman and Dudai, 2001;Vianna et al, 2001;Anokhin et al, 2002;Debiec et al, 2002) and in invertebrates (Yamada et al, 1992;Sekiguchi et al, 1997;Pedreira et al, 2002;Child et al, 2003;Sangha et al, 2003a,b), leading to the hypothesis that consolidation of extinction memory learning and reconsolidation of acquisition memory may be two competing processes (Nader, 2003;Dudai, 2004). Recent studies confirm this hypothesis by showing a separation between both processes by varying the strength of the CS (Eisenberg et al, 2003;Pedreira and Maldonado, 2003;Suzuki et al, 2004).…”

Onset of Amnesia Is Delayed with a Decrease in Inhibition of Protein Synthesis during Odor-taste Associative Learning in the Terrestrial Slug Limax valentianus

“…A previous study using Limax has shown that presentation to a conditioned slug of a conditioned stimulus followed immediately by cooling induces amnesia if such an operation is done within about 3 days after conditioning, but is less effective if done later than 3 days (Yamada et al ., 1992). Both results strongly support the notion that the mechanism underlying memory retention differs between up to 3 days and thereafter, and that the memory state becomes stable within 3 days.…”

“…Slugs can learn to avoid the odor of innately preferred food such as carrot juice after it is presented in combination with quinidine, a substance whose taste typically provokes aversive behavior in Limax (Gelperin, 1975;Sahley et al ., 1981). This associative memory can be established by one-trial conditioning, and thus we can ask precise questions about the time-dependent processes of memory consolidation (Yamada et al ., 1992;Sekiguchi et al ., 1997;Matsuo et al ., 2002). Slugs can retain such memories for several weeks and we reported in a previous study (Matsuo et al ., 2002) that protein synthesis is required for long-term memory formation, as has been shown in many other species with various paradigms (Davis and Squire, 1984;Stork and Welzl, 1999).…”