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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

Conventional and new models of classical conditioning in insects. (A) A model proposed to account for the roles of intrinsic and extrinsic neurons of the mushroom body in olfactory conditioning in fruit-flies (Schwaerzel et al., 2003). OA-ergic or DA-ergic neurons (“OA/DA” neurons) convey signals for appetitive or aversive US, respectively. “CS” neurons, which convey signals for CS, make synaptic connections with “CR” neurons that induce the conditioned response (CR), the efficacy of the connection being strengthened by conditioning. “OA/DA” neurons make synaptic connections with axon terminals of “CS” neurons. (B) A new model of classical conditioning, termed Mizunami–Unoki model. The model assumes that efficacy of synaptic transmission from “CS” neurons to “OA/DA” neurons is strengthened by conditioning and that coincident activation of “OA/DA” neurons and “CS” neurons is needed to activate “CR” neurons to lead to a CR (AND gate). (C) Mizunami–Unoki model to account for second-order conditioning, in which an odor (CS1) is paired with water or sodium chloride solution and a visual pattern (CS2) is paired with the odor (CS1), as indicated in the inset. The model predicts that pairing of CS1 and US at the first conditioning stage results in enhancement of synapses from “CS1” neurons to “OA/DA” neurons, and activation of the synapses (by CS1) at the second conditioning stage leads to simultaneous activation of “OA/DA” and “CS2” neurons, and this leads to enhancement of synaptic transmission from “CS2” neurons to “OA/DA” neurons and to “CR” neurons. Modified from Mizunami et al. (2009).
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Figure 6: Conventional and new models of classical conditioning in insects. (A) A model proposed to account for the roles of intrinsic and extrinsic neurons of the mushroom body in olfactory conditioning in fruit-flies (Schwaerzel et al., 2003). OA-ergic or DA-ergic neurons (“OA/DA” neurons) convey signals for appetitive or aversive US, respectively. “CS” neurons, which convey signals for CS, make synaptic connections with “CR” neurons that induce the conditioned response (CR), the efficacy of the connection being strengthened by conditioning. “OA/DA” neurons make synaptic connections with axon terminals of “CS” neurons. (B) A new model of classical conditioning, termed Mizunami–Unoki model. The model assumes that efficacy of synaptic transmission from “CS” neurons to “OA/DA” neurons is strengthened by conditioning and that coincident activation of “OA/DA” neurons and “CS” neurons is needed to activate “CR” neurons to lead to a CR (AND gate). (C) Mizunami–Unoki model to account for second-order conditioning, in which an odor (CS1) is paired with water or sodium chloride solution and a visual pattern (CS2) is paired with the odor (CS1), as indicated in the inset. The model predicts that pairing of CS1 and US at the first conditioning stage results in enhancement of synapses from “CS1” neurons to “OA/DA” neurons, and activation of the synapses (by CS1) at the second conditioning stage leads to simultaneous activation of “OA/DA” and “CS2” neurons, and this leads to enhancement of synaptic transmission from “CS2” neurons to “OA/DA” neurons and to “CR” neurons. Modified from Mizunami et al. (2009).

Mentions: We noticed that our findings are not consistent with conventional neural models of insect classical conditioning. Figure 6A depicts perhaps the best model proposed to account for the roles of extrinsic and intrinsic neurons of mushroom bodies in olfactory conditioning in the fruit-fly Drosophila (Schwaerzel et al., 2003). This model assumes that (1) “CS” neurons (intrinsic neurons of the mushroom body, called Kenyon cells) that convey signals about a CS make synaptic connections with dendrites of “CR” neurons (efferent (output) neurons of the mushroom body lobe), activation of which leads to a CR (conditioned response) that mimics UR (unconditioned response), but these synaptic connections are silent or very weak before conditioning, (2) OA- or DA-ergic efferent neurons projecting to the lobes (“OA/DA” neurons), which convey signals for appetitive or aversive US, respectively, make synaptic connections with axon terminals of “CS” neurons, and (3) the efficacy of the synaptic transmission from “CS” neurons to “CR” neurons that induces a conditioned response (CS–CR or S–R connection) is strengthened by coincident activation of “CS” neurons and “OA/DA” neurons during conditioning (assuming Kandelian synaptic plasticity; see Abrams and Kandel, 1988). In short, this model assumes that presentation of a CS after conditioning activates the CS–CR or S–R connection to induce a CR. Thus, this model is characterized as an S–R model (Figure 7A), following terminology in studies on classical conditioning in higher vertebrates (Rescorla, 1988; Pickens and Holland, 2004; Holland, 2008). It can be pointed out that the S–R model accounts for most forms of classical conditioning in invertebrates, including classical conditioning of gill withdrawal reflex in the mollusk Aplysia, where pairing of a gentle tactile stimulus to the siphon (CS) and a strong tactile stimulus to the gill (US) results in an enhancement of the efficacy of synaptic transmission from siphon sensory neuron to gill motor neuron (Abrams and Kandel, 1988; Kandel, 2001; Roberts and Glanzman, 2003), which is characterized as an S–R connection. The model by Schwaerzel et al. (2003), however, is inconsistent with our findings because it predicts that activation of OA- or DA-ergic neurons is not required for appetitive or aversive memory recall, respectively.


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

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

Conventional and new models of classical conditioning in insects. (A) A model proposed to account for the roles of intrinsic and extrinsic neurons of the mushroom body in olfactory conditioning in fruit-flies (Schwaerzel et al., 2003). OA-ergic or DA-ergic neurons (“OA/DA” neurons) convey signals for appetitive or aversive US, respectively. “CS” neurons, which convey signals for CS, make synaptic connections with “CR” neurons that induce the conditioned response (CR), the efficacy of the connection being strengthened by conditioning. “OA/DA” neurons make synaptic connections with axon terminals of “CS” neurons. (B) A new model of classical conditioning, termed Mizunami–Unoki model. The model assumes that efficacy of synaptic transmission from “CS” neurons to “OA/DA” neurons is strengthened by conditioning and that coincident activation of “OA/DA” neurons and “CS” neurons is needed to activate “CR” neurons to lead to a CR (AND gate). (C) Mizunami–Unoki model to account for second-order conditioning, in which an odor (CS1) is paired with water or sodium chloride solution and a visual pattern (CS2) is paired with the odor (CS1), as indicated in the inset. The model predicts that pairing of CS1 and US at the first conditioning stage results in enhancement of synapses from “CS1” neurons to “OA/DA” neurons, and activation of the synapses (by CS1) at the second conditioning stage leads to simultaneous activation of “OA/DA” and “CS2” neurons, and this leads to enhancement of synaptic transmission from “CS2” neurons to “OA/DA” neurons and to “CR” neurons. Modified from Mizunami et al. (2009).
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Related In: Results  -  Collection

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Figure 6: Conventional and new models of classical conditioning in insects. (A) A model proposed to account for the roles of intrinsic and extrinsic neurons of the mushroom body in olfactory conditioning in fruit-flies (Schwaerzel et al., 2003). OA-ergic or DA-ergic neurons (“OA/DA” neurons) convey signals for appetitive or aversive US, respectively. “CS” neurons, which convey signals for CS, make synaptic connections with “CR” neurons that induce the conditioned response (CR), the efficacy of the connection being strengthened by conditioning. “OA/DA” neurons make synaptic connections with axon terminals of “CS” neurons. (B) A new model of classical conditioning, termed Mizunami–Unoki model. The model assumes that efficacy of synaptic transmission from “CS” neurons to “OA/DA” neurons is strengthened by conditioning and that coincident activation of “OA/DA” neurons and “CS” neurons is needed to activate “CR” neurons to lead to a CR (AND gate). (C) Mizunami–Unoki model to account for second-order conditioning, in which an odor (CS1) is paired with water or sodium chloride solution and a visual pattern (CS2) is paired with the odor (CS1), as indicated in the inset. The model predicts that pairing of CS1 and US at the first conditioning stage results in enhancement of synapses from “CS1” neurons to “OA/DA” neurons, and activation of the synapses (by CS1) at the second conditioning stage leads to simultaneous activation of “OA/DA” and “CS2” neurons, and this leads to enhancement of synaptic transmission from “CS2” neurons to “OA/DA” neurons and to “CR” neurons. Modified from Mizunami et al. (2009).
Mentions: We noticed that our findings are not consistent with conventional neural models of insect classical conditioning. Figure 6A depicts perhaps the best model proposed to account for the roles of extrinsic and intrinsic neurons of mushroom bodies in olfactory conditioning in the fruit-fly Drosophila (Schwaerzel et al., 2003). This model assumes that (1) “CS” neurons (intrinsic neurons of the mushroom body, called Kenyon cells) that convey signals about a CS make synaptic connections with dendrites of “CR” neurons (efferent (output) neurons of the mushroom body lobe), activation of which leads to a CR (conditioned response) that mimics UR (unconditioned response), but these synaptic connections are silent or very weak before conditioning, (2) OA- or DA-ergic efferent neurons projecting to the lobes (“OA/DA” neurons), which convey signals for appetitive or aversive US, respectively, make synaptic connections with axon terminals of “CS” neurons, and (3) the efficacy of the synaptic transmission from “CS” neurons to “CR” neurons that induces a conditioned response (CS–CR or S–R connection) is strengthened by coincident activation of “CS” neurons and “OA/DA” neurons during conditioning (assuming Kandelian synaptic plasticity; see Abrams and Kandel, 1988). In short, this model assumes that presentation of a CS after conditioning activates the CS–CR or S–R connection to induce a CR. Thus, this model is characterized as an S–R model (Figure 7A), following terminology in studies on classical conditioning in higher vertebrates (Rescorla, 1988; Pickens and Holland, 2004; Holland, 2008). It can be pointed out that the S–R model accounts for most forms of classical conditioning in invertebrates, including classical conditioning of gill withdrawal reflex in the mollusk Aplysia, where pairing of a gentle tactile stimulus to the siphon (CS) and a strong tactile stimulus to the gill (US) results in an enhancement of the efficacy of synaptic transmission from siphon sensory neuron to gill motor neuron (Abrams and Kandel, 1988; Kandel, 2001; Roberts and Glanzman, 2003), which is characterized as an S–R connection. The model by Schwaerzel et al. (2003), however, is inconsistent with our findings because it predicts that activation of OA- or DA-ergic neurons is not required for appetitive or aversive memory recall, respectively.

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