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Roles of aminergic neurons in formation and recall of associative memory in crickets.

Mizunami M, Matsumoto Y - Front Behav Neurosci (2010)

Bottom Line: The former is called stimulus-response (S-R) connection and the latter is called stimulus-stimulus (S-S) connection by theorists studying classical conditioning in vertebrates.Results of our studies using a second-order conditioning procedure supported our model.We propose that insect classical conditioning involves the formation of S-S connection and its activation for memory recall, which are often called cognitive processes.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Life Science, Hokkaido University, Sapporo, Japan. mizunami@sci.hokudai.ac.jp

ABSTRACT
We review recent progress in the study of roles of octopaminergic (OA-ergic) and dopaminergic (DA-ergic) signaling in insect classical conditioning, focusing on our studies on crickets. Studies on olfactory learning in honey bees and fruit-flies have suggested that OA-ergic and DA-ergic neurons convey reinforcing signals of appetitive unconditioned stimulus (US) and aversive US, respectively. Our work suggested that this is applicable to olfactory, visual pattern, and color learning in crickets, indicating that this feature is ubiquitous in learning of various sensory stimuli. We also showed that aversive memory decayed much faster than did appetitive memory, and we proposed that this feature is common in insects and humans. Our study also suggested that activation of OA- or DA-ergic neurons is needed for appetitive or aversive memory recall, respectively. To account for this finding, we proposed a model in which it is assumed that two types of synaptic connections are strengthened by conditioning and are activated during memory recall, one type being connections from neurons representing conditioned stimulus (CS) to neurons inducing conditioned response and the other being connections from neurons representing CS to OA- or DA-ergic neurons representing appetitive or aversive US, respectively. The former is called stimulus-response (S-R) connection and the latter is called stimulus-stimulus (S-S) connection by theorists studying classical conditioning in vertebrates. Results of our studies using a second-order conditioning procedure supported our model. We propose that insect classical conditioning involves the formation of S-S connection and its activation for memory recall, which are often called cognitive processes.

No MeSH data available.


Related in: MedlinePlus

Effects of OA or DA receptor antagonists on appetitive and aversive visual pattern conditioning. (A) Effects of OA receptor antagonists. Six groups of crickets were each injected with 3 μl saline or saline containing 1 μM epinastine or 1 μM mianserin at 30 min before 8-trial appetitive (left) or before 12-trial aversive conditioning (right). (B) Effects of DA receptor antagonists. Six groups of crickets were each injected with 3 μl saline containing 500 μM fluphenazine, 500 μM chlorpromazine, or 500 μM spiperone at 30 min before 8-trial appetitive (left) or before 12-trial aversive conditioning (right). Preference indexes for rewarded visual pattern (in the case of appetitive conditioning) and those of unpunished visual pattern (in the case of aversive conditioning) before (white bars) and at 30 min after conditioning (black bars) are shown with mean ± SEM. The number of animals is shown at each data point. The results of statistical comparison before and after conditioning (WCX test) and between experimental and saline-injected control groups (M–W test) are shown as asterisks (p < 0.05; p < 0.01; p < 0.001, NS p > 0.05). Modified from Unoki et al. (2006).
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Figure 3: Effects of OA or DA receptor antagonists on appetitive and aversive visual pattern conditioning. (A) Effects of OA receptor antagonists. Six groups of crickets were each injected with 3 μl saline or saline containing 1 μM epinastine or 1 μM mianserin at 30 min before 8-trial appetitive (left) or before 12-trial aversive conditioning (right). (B) Effects of DA receptor antagonists. Six groups of crickets were each injected with 3 μl saline containing 500 μM fluphenazine, 500 μM chlorpromazine, or 500 μM spiperone at 30 min before 8-trial appetitive (left) or before 12-trial aversive conditioning (right). Preference indexes for rewarded visual pattern (in the case of appetitive conditioning) and those of unpunished visual pattern (in the case of aversive conditioning) before (white bars) and at 30 min after conditioning (black bars) are shown with mean ± SEM. The number of animals is shown at each data point. The results of statistical comparison before and after conditioning (WCX test) and between experimental and saline-injected control groups (M–W test) are shown as asterisks (p < 0.05; p < 0.01; p < 0.001, NS p > 0.05). Modified from Unoki et al. (2006).

Mentions: We next studied the effect of OA and DA receptor antagonists on appetitive and aversive conditioning of visual pattern (Unoki et al., 2006) and color (Nakatani et al., 2009). Crickets injected with epinastine or mianserin, OA receptor antagonists, into the hemolymph exhibited a complete impairment of appetitive learning to associate a visual pattern with water reward, but aversive learning to associate a visual pattern with sodium chloride punishment was unaffected (Figure 3A). In contrast, fluphenazine, chlorpromazine, or spiperone, DA receptor antagonists, completely impaired aversive learning but not appetitive learning (Figure 3B). We also found the same for color learning: OA receptor antagonists impaired appetitive color learning with water reward without affecting aversive color learning with sodium chloride punishment. In contrast, DA receptor antagonists impaired aversive color learning without affecting appetitive color learning (Nakatani et al., 2009). These findings indicate that the roles of OA-ergic and DA-ergic neurons in conveying information about appetitive and aversive US, respectively, are ubiquitous in learning of odor, visual pattern and color stimuli, suggesting that these neurons serve as the general reward or punishment system for insect learning.


Roles of aminergic neurons in formation and recall of associative memory in crickets.

Mizunami M, Matsumoto Y - Front Behav Neurosci (2010)

Effects of OA or DA receptor antagonists on appetitive and aversive visual pattern conditioning. (A) Effects of OA receptor antagonists. Six groups of crickets were each injected with 3 μl saline or saline containing 1 μM epinastine or 1 μM mianserin at 30 min before 8-trial appetitive (left) or before 12-trial aversive conditioning (right). (B) Effects of DA receptor antagonists. Six groups of crickets were each injected with 3 μl saline containing 500 μM fluphenazine, 500 μM chlorpromazine, or 500 μM spiperone at 30 min before 8-trial appetitive (left) or before 12-trial aversive conditioning (right). Preference indexes for rewarded visual pattern (in the case of appetitive conditioning) and those of unpunished visual pattern (in the case of aversive conditioning) before (white bars) and at 30 min after conditioning (black bars) are shown with mean ± SEM. The number of animals is shown at each data point. The results of statistical comparison before and after conditioning (WCX test) and between experimental and saline-injected control groups (M–W test) are shown as asterisks (p < 0.05; p < 0.01; p < 0.001, NS p > 0.05). Modified from Unoki et al. (2006).
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Related In: Results  -  Collection

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Figure 3: Effects of OA or DA receptor antagonists on appetitive and aversive visual pattern conditioning. (A) Effects of OA receptor antagonists. Six groups of crickets were each injected with 3 μl saline or saline containing 1 μM epinastine or 1 μM mianserin at 30 min before 8-trial appetitive (left) or before 12-trial aversive conditioning (right). (B) Effects of DA receptor antagonists. Six groups of crickets were each injected with 3 μl saline containing 500 μM fluphenazine, 500 μM chlorpromazine, or 500 μM spiperone at 30 min before 8-trial appetitive (left) or before 12-trial aversive conditioning (right). Preference indexes for rewarded visual pattern (in the case of appetitive conditioning) and those of unpunished visual pattern (in the case of aversive conditioning) before (white bars) and at 30 min after conditioning (black bars) are shown with mean ± SEM. The number of animals is shown at each data point. The results of statistical comparison before and after conditioning (WCX test) and between experimental and saline-injected control groups (M–W test) are shown as asterisks (p < 0.05; p < 0.01; p < 0.001, NS p > 0.05). Modified from Unoki et al. (2006).
Mentions: We next studied the effect of OA and DA receptor antagonists on appetitive and aversive conditioning of visual pattern (Unoki et al., 2006) and color (Nakatani et al., 2009). Crickets injected with epinastine or mianserin, OA receptor antagonists, into the hemolymph exhibited a complete impairment of appetitive learning to associate a visual pattern with water reward, but aversive learning to associate a visual pattern with sodium chloride punishment was unaffected (Figure 3A). In contrast, fluphenazine, chlorpromazine, or spiperone, DA receptor antagonists, completely impaired aversive learning but not appetitive learning (Figure 3B). We also found the same for color learning: OA receptor antagonists impaired appetitive color learning with water reward without affecting aversive color learning with sodium chloride punishment. In contrast, DA receptor antagonists impaired aversive color learning without affecting appetitive color learning (Nakatani et al., 2009). These findings indicate that the roles of OA-ergic and DA-ergic neurons in conveying information about appetitive and aversive US, respectively, are ubiquitous in learning of odor, visual pattern and color stimuli, suggesting that these neurons serve as the general reward or punishment system for insect learning.

Bottom Line: The former is called stimulus-response (S-R) connection and the latter is called stimulus-stimulus (S-S) connection by theorists studying classical conditioning in vertebrates.Results of our studies using a second-order conditioning procedure supported our model.We propose that insect classical conditioning involves the formation of S-S connection and its activation for memory recall, which are often called cognitive processes.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Life Science, Hokkaido University, Sapporo, Japan. mizunami@sci.hokudai.ac.jp

ABSTRACT
We review recent progress in the study of roles of octopaminergic (OA-ergic) and dopaminergic (DA-ergic) signaling in insect classical conditioning, focusing on our studies on crickets. Studies on olfactory learning in honey bees and fruit-flies have suggested that OA-ergic and DA-ergic neurons convey reinforcing signals of appetitive unconditioned stimulus (US) and aversive US, respectively. Our work suggested that this is applicable to olfactory, visual pattern, and color learning in crickets, indicating that this feature is ubiquitous in learning of various sensory stimuli. We also showed that aversive memory decayed much faster than did appetitive memory, and we proposed that this feature is common in insects and humans. Our study also suggested that activation of OA- or DA-ergic neurons is needed for appetitive or aversive memory recall, respectively. To account for this finding, we proposed a model in which it is assumed that two types of synaptic connections are strengthened by conditioning and are activated during memory recall, one type being connections from neurons representing conditioned stimulus (CS) to neurons inducing conditioned response and the other being connections from neurons representing CS to OA- or DA-ergic neurons representing appetitive or aversive US, respectively. The former is called stimulus-response (S-R) connection and the latter is called stimulus-stimulus (S-S) connection by theorists studying classical conditioning in vertebrates. Results of our studies using a second-order conditioning procedure supported our model. We propose that insect classical conditioning involves the formation of S-S connection and its activation for memory recall, which are often called cognitive processes.

No MeSH data available.


Related in: MedlinePlus