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Roles of octopamine and dopamine in appetitive and aversive memory acquisition studied in olfactory conditioning of maxillary palpi extension response in crickets.

Matsumoto Y, Matsumoto CS, Wakuda R, Ichihara S, Mizunami M - Front Behav Neurosci (2015)

Bottom Line: In fruit-flies, however, it was concluded that dopamine mediates both appetitive and aversive reinforcement, which differs from our suggestion in crickets.Crickets extended their maxillary palpi and vigorously swung them when they perceived some odors, and we found that crickets that received pairing of an odor with water reward or sodium chloride punishment exhibited an increase or decrease in percentages of maxillary palpi extension responses to the odor.Using this procedure, we found that octopamine and dopamine receptor antagonists impair acquisition of appetitive and aversive learning, respectively.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Science, Hokkaido University Sapporo, Japan ; Faculty of Liberal Arts, Tokyo Medical and Dental University Ichikawa, Japan.

ABSTRACT
Elucidation of reinforcing mechanisms for associative learning is an important subject in neuroscience. Based on results of our previous pharmacological studies in crickets, we suggested that octopamine and dopamine mediate reward and punishment signals, respectively, in associative learning. In fruit-flies, however, it was concluded that dopamine mediates both appetitive and aversive reinforcement, which differs from our suggestion in crickets. In our previous studies, the effect of conditioning was tested at 30 min after training or later, due to limitations of our experimental procedures, and thus the possibility that octopamine and dopamine were not needed for initial acquisition of learning was not ruled out. In this study we first established a conditioning procedure to enable us to evaluate acquisition performance in crickets. Crickets extended their maxillary palpi and vigorously swung them when they perceived some odors, and we found that crickets that received pairing of an odor with water reward or sodium chloride punishment exhibited an increase or decrease in percentages of maxillary palpi extension responses to the odor. Using this procedure, we found that octopamine and dopamine receptor antagonists impair acquisition of appetitive and aversive learning, respectively. This finding suggests that neurotransmitters mediating appetitive reinforcement differ in crickets and fruit-flies.

No MeSH data available.


Related in: MedlinePlus

Differential aversive olfactory conditioning of MER with sodium chloride US. (A) Acquisition performance. Percentages of MER to an odor paired with 20% sodium chloride solution (paired odor, open circle) and those to an odor presented alone (unpaired odor, filled circle) in each conditioning trial are shown. Crickets were subjected to six pairing trials to associate an odor with sodium chloride solution (aversive US) and to presentation of another odor without pairing with the US with 5-min intervals, and percentages of MERs to the paired odor (gray graph) and the unpaired odor (black graph) were compared. The number of animals tested is shown in parentheses. (B) Retention performance at 1-day after conditioning. Percentages of MERs to the paired odor (white bar) and the unpaired odor (black bar) are shown. Percentage of MER to the paired odor was significantly lower than that to the unpaired odor. *p < 0.05; **p < 0.01.
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Figure 3: Differential aversive olfactory conditioning of MER with sodium chloride US. (A) Acquisition performance. Percentages of MER to an odor paired with 20% sodium chloride solution (paired odor, open circle) and those to an odor presented alone (unpaired odor, filled circle) in each conditioning trial are shown. Crickets were subjected to six pairing trials to associate an odor with sodium chloride solution (aversive US) and to presentation of another odor without pairing with the US with 5-min intervals, and percentages of MERs to the paired odor (gray graph) and the unpaired odor (black graph) were compared. The number of animals tested is shown in parentheses. (B) Retention performance at 1-day after conditioning. Percentages of MERs to the paired odor (white bar) and the unpaired odor (black bar) are shown. Percentage of MER to the paired odor was significantly lower than that to the unpaired odor. *p < 0.05; **p < 0.01.

Mentions: We first attempted to establish a procedure for aversive olfactory conditioning of MER. We used a high concentration (20%) of sodium chloride solution as aversive US and vanilla and maple odors as CSs. We observed that repeated presentation of these odors alone without pairing with US led to a slight decrease of %MER to the odor (see Figure 3A). Therefore, in order to discriminate pairing-specific decrement of %MER (associative conditioning effect) from this non-associative effect (habituation), we used a differential conditioning procedure in which one of the two odors (vanilla and maple odors) was paired with US (paired odor; CS) and another odor was presented alone (unpaired odor) to allow comparison of MERs to the CS and the unpaired odor. The odors were presented six times each in a pseudo-random sequence and with 5-min ITIs. Percentages of MER to vanilla odor and those to maple odor were similarly high (>70%) in the first trials, and acquisition and retention performances of the vanilla CS group did not differ from those of the maple CS group (Supplementary Figure S1). Therefore, data from the two subgroups, vanilla CS group and maple CS group, were pooled. Percentage of MER to the CS significantly decreased with increase in the number of trials (Figure 3A, Cochran's Q-test: χ2 = 38, df = 5, p = 0.00000032). For the unpaired odor, we observed a slight decrease of %MER by repeated presentation of the odor, although the difference was not statistically significant (Cochran's Q-test: χ2 = 5.1, df = 5, p = 0.41). Percentages of MER to the CS did not significantly differ from that to the unpaired odor in the 1st trial (McNemar's test: χ2 = 0.0, df = 1, p = 1.0) and in the 2nd trial (χ2 = 2.3, p = 0.13), but it was significantly greater than that to the unpaired odor in the 3rd (χ2 = 6.8, p = 0.0094), 4th (χ2 = 4.9, p = 0.027), 5th (χ2 = 4.2, p = 0.041), and 6th trials (χ2 = 7.1, p = 0.0077). Thus, we conclude that the decrease of %MER to the paired odor is pairing-specific.


Roles of octopamine and dopamine in appetitive and aversive memory acquisition studied in olfactory conditioning of maxillary palpi extension response in crickets.

Matsumoto Y, Matsumoto CS, Wakuda R, Ichihara S, Mizunami M - Front Behav Neurosci (2015)

Differential aversive olfactory conditioning of MER with sodium chloride US. (A) Acquisition performance. Percentages of MER to an odor paired with 20% sodium chloride solution (paired odor, open circle) and those to an odor presented alone (unpaired odor, filled circle) in each conditioning trial are shown. Crickets were subjected to six pairing trials to associate an odor with sodium chloride solution (aversive US) and to presentation of another odor without pairing with the US with 5-min intervals, and percentages of MERs to the paired odor (gray graph) and the unpaired odor (black graph) were compared. The number of animals tested is shown in parentheses. (B) Retention performance at 1-day after conditioning. Percentages of MERs to the paired odor (white bar) and the unpaired odor (black bar) are shown. Percentage of MER to the paired odor was significantly lower than that to the unpaired odor. *p < 0.05; **p < 0.01.
© Copyright Policy
Related In: Results  -  Collection

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Figure 3: Differential aversive olfactory conditioning of MER with sodium chloride US. (A) Acquisition performance. Percentages of MER to an odor paired with 20% sodium chloride solution (paired odor, open circle) and those to an odor presented alone (unpaired odor, filled circle) in each conditioning trial are shown. Crickets were subjected to six pairing trials to associate an odor with sodium chloride solution (aversive US) and to presentation of another odor without pairing with the US with 5-min intervals, and percentages of MERs to the paired odor (gray graph) and the unpaired odor (black graph) were compared. The number of animals tested is shown in parentheses. (B) Retention performance at 1-day after conditioning. Percentages of MERs to the paired odor (white bar) and the unpaired odor (black bar) are shown. Percentage of MER to the paired odor was significantly lower than that to the unpaired odor. *p < 0.05; **p < 0.01.
Mentions: We first attempted to establish a procedure for aversive olfactory conditioning of MER. We used a high concentration (20%) of sodium chloride solution as aversive US and vanilla and maple odors as CSs. We observed that repeated presentation of these odors alone without pairing with US led to a slight decrease of %MER to the odor (see Figure 3A). Therefore, in order to discriminate pairing-specific decrement of %MER (associative conditioning effect) from this non-associative effect (habituation), we used a differential conditioning procedure in which one of the two odors (vanilla and maple odors) was paired with US (paired odor; CS) and another odor was presented alone (unpaired odor) to allow comparison of MERs to the CS and the unpaired odor. The odors were presented six times each in a pseudo-random sequence and with 5-min ITIs. Percentages of MER to vanilla odor and those to maple odor were similarly high (>70%) in the first trials, and acquisition and retention performances of the vanilla CS group did not differ from those of the maple CS group (Supplementary Figure S1). Therefore, data from the two subgroups, vanilla CS group and maple CS group, were pooled. Percentage of MER to the CS significantly decreased with increase in the number of trials (Figure 3A, Cochran's Q-test: χ2 = 38, df = 5, p = 0.00000032). For the unpaired odor, we observed a slight decrease of %MER by repeated presentation of the odor, although the difference was not statistically significant (Cochran's Q-test: χ2 = 5.1, df = 5, p = 0.41). Percentages of MER to the CS did not significantly differ from that to the unpaired odor in the 1st trial (McNemar's test: χ2 = 0.0, df = 1, p = 1.0) and in the 2nd trial (χ2 = 2.3, p = 0.13), but it was significantly greater than that to the unpaired odor in the 3rd (χ2 = 6.8, p = 0.0094), 4th (χ2 = 4.9, p = 0.027), 5th (χ2 = 4.2, p = 0.041), and 6th trials (χ2 = 7.1, p = 0.0077). Thus, we conclude that the decrease of %MER to the paired odor is pairing-specific.

Bottom Line: In fruit-flies, however, it was concluded that dopamine mediates both appetitive and aversive reinforcement, which differs from our suggestion in crickets.Crickets extended their maxillary palpi and vigorously swung them when they perceived some odors, and we found that crickets that received pairing of an odor with water reward or sodium chloride punishment exhibited an increase or decrease in percentages of maxillary palpi extension responses to the odor.Using this procedure, we found that octopamine and dopamine receptor antagonists impair acquisition of appetitive and aversive learning, respectively.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Science, Hokkaido University Sapporo, Japan ; Faculty of Liberal Arts, Tokyo Medical and Dental University Ichikawa, Japan.

ABSTRACT
Elucidation of reinforcing mechanisms for associative learning is an important subject in neuroscience. Based on results of our previous pharmacological studies in crickets, we suggested that octopamine and dopamine mediate reward and punishment signals, respectively, in associative learning. In fruit-flies, however, it was concluded that dopamine mediates both appetitive and aversive reinforcement, which differs from our suggestion in crickets. In our previous studies, the effect of conditioning was tested at 30 min after training or later, due to limitations of our experimental procedures, and thus the possibility that octopamine and dopamine were not needed for initial acquisition of learning was not ruled out. In this study we first established a conditioning procedure to enable us to evaluate acquisition performance in crickets. Crickets extended their maxillary palpi and vigorously swung them when they perceived some odors, and we found that crickets that received pairing of an odor with water reward or sodium chloride punishment exhibited an increase or decrease in percentages of maxillary palpi extension responses to the odor. Using this procedure, we found that octopamine and dopamine receptor antagonists impair acquisition of appetitive and aversive learning, respectively. This finding suggests that neurotransmitters mediating appetitive reinforcement differ in crickets and fruit-flies.

No MeSH data available.


Related in: MedlinePlus