Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Formation of Long-term Olfactory Memory in the Cricket Gryllus bimaculatus
Graduate School of Life Sciences, Tohoku University, Katahira 2-1-1, Aoba-ku, Sendai 980-8577, Japan
Correspondence to be sent to: Makoto Mizunami, e-mail: makoto{at}biology.tohoku.ac.jp
Key words: context, cricket, insect, learning, long-term memory, olfaction
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Introduction |
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 Top Introduction Long-term retention of olfactory...Temporal determinants of...Context-dependent olfactory...Conclusion and future...AcknowledgementsReferences |
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Insects live in constantly changing environments, where the availability of food sources varies with the seasons. Therefore, the ability to learn to associate a certain cue with an abundant food source must be of great significance for insects (Mizunami et al., 1999
). However, most
previous studies on olfactory learning in insects have been restricted to the honey bee
Apis mellifera and the fruitfly Drosophila melanogaster. It is obvious
that studies in only two species are not sufficient to understand fully the principles of
olfactory learning and its neural mechanisms.
Recently, we found that the cricket Gryllus bimaculatus (Matsumoto and Mizunami, 2000) and the cockroach
Periplaneta americana (Sakura and
Mizunami, 2001;
Sakura et al., 2002;
Watanabe et al., 2003) have a
developed capacity for olfactory learning. Here we review recent progress on the
olfactory learning capabilities of the crickets, which provide a solid basis for future
studies of neural mechanisms of olfactory learning and memory.
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Long-term retention of olfactory memory |
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TopIntroductionLong-term retention of olfactory...Temporal determinants of...Context-dependent olfactory...Conclusion and future...AcknowledgementsReferences |
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Convincing reports of lifetime memory retention in insects have been limited to adults of social Hymenoptera. We have studied the time span of olfactory memory retention in the cricket (Matsumoto and Mizunami, 2002b
). Third- or fourth-instar cricket nymphs were trained to associate one
odor with water and another odor with saline solution. At 6 and 10 weeks after training,
adult crickets exhibited significantly greater preferences for the odor associated with
water over that associated with saline solution. The learned preference was altered when
they were given reversal training at 6 weeks after initial training. We conclude that
crickets are capable of retaining olfactory memory practically for their lifetime and of
easily rewriting it in accordance with experience. |
Temporal determinants of olfactory memory |
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TopIntroductionLong-term retention of olfactory...Temporal determinants of...Context-dependent olfactory...Conclusion and future...AcknowledgementsReferences |
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We studied the time relationship between the conditioned stimulus (CS) and unconditioned stimulus (US) to determine long-term olfactory memory retention in the cricket (Matsumoto and Mizunami, 2002a
). Crickets underwent appetitive, aversive or differential conditioning
trials. In appetitive and aversive conditioning trials, odors of peppermint essence and
vanilla essence were paired with a water reward and NaCl solution, respectively. In
differential conditioning trials, peppermint odor was paired with water and vanilla was
paired with saline solution. The odor preference of crickets was tested before and at 2
h, 1 day and 4 days after training by allowing them to choose between peppermint or
vanilla sources. Differential and appetitive conditioning led to long-lasting memory with
no significant decay from 2 h to 4 days after training, but memory formed by aversive
conditioning had completely diminished 1 day after training. Studies using a differential
conditioning procedure have shown that: (i) only four trials were sufficient to attain a
saturated level of conditioning; (ii) conditioning was achieved when the conditioning
stimulus was presented immediately or at 5 s before the onset of presentation of the US;
(iii) the optimal intervals between trials were 2–5 min; and (iv) anesthetic
treatment with CO2 given immediately after training resulted in memory
disruption but anesthesia-resistant memory was fully developed 20 min after training. It
is concluded that differential conditioning procedure is especially effective for
inducing this capability.
The dependency of memory retention on de novo brain protein synthesis was
studied by injecting the protein synthesis inhibitor cycloheximide (CHX) into the head
capsule (Matsumoto et al.,
2003). Injection of CHX inhibited 3H-leucine incorporation into brain
proteins by >90% for 3 h. Crickets were trained to associate peppermint odor
with water and vanilla odor with NaCl solution and were injected with CHX before or at
different times after training. Memory retention up to 3–4 h after training was
unaffected by CHX injection. However, the level of retention at 6–8 h after
training was lowered when CHX was injected. CHX dissociates two phases of olfactory
memory in crickets: an earlier protein-synthesis-independent phase (<4 h) and a later
(>5 h) protein-synthesis-dependent phase.
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Context-dependent olfactory learning |
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TopIntroductionLong-term retention of olfactory...Temporal determinants of...Context-dependent olfactory...Conclusion and future...AcknowledgementsReferences |
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Conditioning in mammals often depends on the general ‘context’ in which association between CS and US occurs. In insects, the capacity for context-dependent learning has been demonstrated for visual pattern discrimination learning and for learning of the position of a visual target (see discussion in Matsumoto and Mizunami, 2004
).
However, no context-dependent form of olfactory learning, which is useful for the study
of underlying neural processes, has been established in any insects.
We studied the capability of the cricket to select one of a pair of odors and to
avoid the other in one context and to do the opposite in another context (Matsumoto and Mizunami, 2004). One group of crickets was
trained to associate one of a pair of odors (CS1) with water reward (appetitive
unconditioned stimulus, US+) and another odor (CS2) with saline solution (aversive
US, US–) under illumination and to associate CS1 with US– and CS2 with
US+ in the dark (Figure
1). Another group of crickets received
training of the opposite stimulus arrangement. One day after the training for 3 days, the
former group significantly preferred CS1 over CS2 under illumination, but preferred CS2
over CS1 in the dark and the latter group exhibited the opposite odor preference. Results
of control experiments showed that background light conditions had no significant effects
on memory formation or retrieval unless it was explicitly associated with US during
training. Thus, the visual context affected learning performance only when crickets were
required to use it to disambiguate the meaning of CSs and to predict USs.
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An important question to be addressed in our ongoing studies is areas of the insect brain in which the olfactory CS pathway, the gustatory US pathway and the visual contextual stimulus pathway converge to form context-dependent olfactory memory.
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Conclusion and future perspectives |
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TopIntroductionLong-term retention of olfactory...Temporal determinants of...Context-dependent olfactory...Conclusion and future...AcknowledgementsReferences |
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These results show that crickets have an excellent capacity for olfactory learning, characterized by quick acquisition, long retention and easy re-writing of memory. Crickets can be easily used for detailed pharmacological and electrophysiological studies and may emerge as excellent subjects for the study of the neural basis of olfactory learning.
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Acknowledgements |
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TopIntroductionLong-term retention of olfactory...Temporal determinants of...Context-dependent olfactory...Conclusion and future...AcknowledgementsReferences |
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This study was supported by grants from the Japanese Ministry of Promotion of Science to Y.M. and the Ministry of Education, Science, Culture, Sports and Technology of Japan to M.M.
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References |
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TopIntroductionLong-term retention of olfactory...Temporal determinants of...Context-dependent olfactory...Conclusion and future...AcknowledgementsReferences |
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Matsumoto, Y. and Mizunami, M. (2000) Olfactory learning in the cricket Gryllus bimaculatus. J. Exp. Biol., 203, 2581–2588.[Abstract]
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Sakura, M. and Mizunami, M. (2001) Olfactory learning and memory in the cockroach Periplaneta americana. Zool. Sci., 18, 21–28.[CrossRef]
Sakura, M., Okada, R. and Mizunami, M. (2002) Olfactory discrimination of structurally similar alcohols by cockroaches. J. Comp. Physiol. A, 188, 787–797.[CrossRef]
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