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Trace conditioning in insects-keep the trace!

Dylla KV, Galili DS, Szyszka P, Lüdke A - Front Physiol (2013)

Bottom Line: It is still unknown how the brain encodes CS traces and how they are associated with a US in trace conditioning.In this review we summarize the recent progress in insect trace conditioning on the behavioral and physiological level and emphasize similarities and differences compared to delay conditioning.Moreover, we examine proposed molecular and computational models and reassess different experimental approaches used for trace conditioning.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Neurobiology, University of Konstanz Konstanz, Germany.

ABSTRACT
Trace conditioning is a form of associative learning that can be induced by presenting a conditioned stimulus (CS) and an unconditioned stimulus (US) following each other, but separated by a temporal gap. This gap distinguishes trace conditioning from classical delay conditioning, where the CS and US overlap. To bridge the temporal gap between both stimuli and to form an association between CS and US in trace conditioning, the brain must keep a neural representation of the CS after its termination-a stimulus trace. Behavioral and physiological studies on trace and delay conditioning revealed similarities between the two forms of learning, like similar memory decay and similar odor identity perception in invertebrates. On the other hand differences were reported also, like the requirement of distinct brain structures in vertebrates or disparities in molecular mechanisms in both vertebrates and invertebrates. For example, in commonly used vertebrate conditioning paradigms the hippocampus is necessary for trace but not for delay conditioning, and Drosophila delay conditioning requires the Rutabaga adenylyl cyclase (Rut-AC), which is dispensable in trace conditioning. It is still unknown how the brain encodes CS traces and how they are associated with a US in trace conditioning. Insects serve as powerful models to address the mechanisms underlying trace conditioning, due to their simple brain anatomy, behavioral accessibility and established methods of genetic interference. In this review we summarize the recent progress in insect trace conditioning on the behavioral and physiological level and emphasize similarities and differences compared to delay conditioning. Moreover, we examine proposed molecular and computational models and reassess different experimental approaches used for trace conditioning.

No MeSH data available.


Related in: MedlinePlus

Molecular requirements for trace conditioning and four non-exclusive models of possible coincidence detection. (A) Cellular and molecular requirements which were shown to contribute to Drosophila olfactory trace conditioning. Shuai et al. (2011) found that the targeted inhibition of Rac in the mushroom bodies increased trace-dependent memory formation. Also D1 dopamine receptor (DA1) expression in mushroom bodies was required for trace conditioning, as shown by rescue experiments (Shuai et al., 2011). Trace conditioning does not require the Rutabaga adenylyl cyclase (Rut-AC; Shuai et al., 2011), but delay and trace conditioning simulations both induced synergistic increases of cAMP (Tomchik and Davis, 2009). (B) Educated guesses about coincidence detection in delay conditioning might also apply to trace conditioning. (i) Presynaptic coincidence detection by an adenylyl cyclase (AC; shown in red). In the presynaptic neuron, the CS induces Ca2+ influx and Ca2+ binds to calmodulin (CaM). The US activates G protein-coupled monoaminergic receptors (GPCR) which activate the associated G protein (Gα). When Ca2+/CaM complex and activated G protein (Gα*) co-occur, the AC is activated more strongly than if they appear alone. This leads to an increased production of cAMP and to activation of protein kinase A (PKA) which enhances presynaptic transmitter release (Heisenberg, 2003). (ii) Postsynaptic coincidence detection by the N-methyl-D-aspartate-type glutamate (NMDA) receptor (shown in blue). The CS leads to presynaptic release of glutamate (Glu) which binds to the postsynaptic NMDA receptor. The US, on the other hand, induces the depolarization of the postsynaptic membrane, which allows for the removal of the Mg2+ block from the NMDA receptor channel. Opening of the NMDA receptor channel for Ca2+ influx is only possible when the CS and the US signal coincide. An elevation of the intracellular Ca2+ level leads to the activation of several kinases, inducing synaptic plasticity. The NMDA receptor is involved in delay conditioning in Drosophila (Miyashita et al., 2012) and was also shown to be involved in trace conditioning in vertebrates (Gilmartin and Helmstetter, 2010; Czerniawski et al., 2012). A possible role in insect trace conditioning has not yet been investigated. (iii) Radish (shown in green) is involved in a Rut-AC independent pathway (Isabel et al., 2004; Folkers et al., 2006) and might contribute to trace conditioning. (iv) Gilgamesh (Gish) (shown in purple), a casein kinase I γ homolog in flies, is required for short-term memory formation in Drosophila olfactory delay conditioning, functioning independently of Rut-AC and the cAMP pathway (Tan et al., 2010). Hypothetically, Gish mediates increased Ca2+ influx upon CS–US coincidence and thus might be a pathway for Rut-AC independent trace conditioning.
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Figure 3: Molecular requirements for trace conditioning and four non-exclusive models of possible coincidence detection. (A) Cellular and molecular requirements which were shown to contribute to Drosophila olfactory trace conditioning. Shuai et al. (2011) found that the targeted inhibition of Rac in the mushroom bodies increased trace-dependent memory formation. Also D1 dopamine receptor (DA1) expression in mushroom bodies was required for trace conditioning, as shown by rescue experiments (Shuai et al., 2011). Trace conditioning does not require the Rutabaga adenylyl cyclase (Rut-AC; Shuai et al., 2011), but delay and trace conditioning simulations both induced synergistic increases of cAMP (Tomchik and Davis, 2009). (B) Educated guesses about coincidence detection in delay conditioning might also apply to trace conditioning. (i) Presynaptic coincidence detection by an adenylyl cyclase (AC; shown in red). In the presynaptic neuron, the CS induces Ca2+ influx and Ca2+ binds to calmodulin (CaM). The US activates G protein-coupled monoaminergic receptors (GPCR) which activate the associated G protein (Gα). When Ca2+/CaM complex and activated G protein (Gα*) co-occur, the AC is activated more strongly than if they appear alone. This leads to an increased production of cAMP and to activation of protein kinase A (PKA) which enhances presynaptic transmitter release (Heisenberg, 2003). (ii) Postsynaptic coincidence detection by the N-methyl-D-aspartate-type glutamate (NMDA) receptor (shown in blue). The CS leads to presynaptic release of glutamate (Glu) which binds to the postsynaptic NMDA receptor. The US, on the other hand, induces the depolarization of the postsynaptic membrane, which allows for the removal of the Mg2+ block from the NMDA receptor channel. Opening of the NMDA receptor channel for Ca2+ influx is only possible when the CS and the US signal coincide. An elevation of the intracellular Ca2+ level leads to the activation of several kinases, inducing synaptic plasticity. The NMDA receptor is involved in delay conditioning in Drosophila (Miyashita et al., 2012) and was also shown to be involved in trace conditioning in vertebrates (Gilmartin and Helmstetter, 2010; Czerniawski et al., 2012). A possible role in insect trace conditioning has not yet been investigated. (iii) Radish (shown in green) is involved in a Rut-AC independent pathway (Isabel et al., 2004; Folkers et al., 2006) and might contribute to trace conditioning. (iv) Gilgamesh (Gish) (shown in purple), a casein kinase I γ homolog in flies, is required for short-term memory formation in Drosophila olfactory delay conditioning, functioning independently of Rut-AC and the cAMP pathway (Tan et al., 2010). Hypothetically, Gish mediates increased Ca2+ influx upon CS–US coincidence and thus might be a pathway for Rut-AC independent trace conditioning.

Mentions: Recently, genetic and physiological studies in Drosophila gave insights into the molecular requirements of both conditioning forms (Tomchik and Davis, 2009; Shuai et al., 2011). Trace conditioning does not involve the Rutabaga adenylyl cyclase (Rut-AC; Figure 3A; Shuai et al., 2011), which is required for delay conditioning (Duerr and Quinn, 1982; Dudai et al., 1983). Furthermore, the inhibition of Rac enhanced learning performance in Drosophila trace conditioning, while delay conditioning remained unaffected (Shuai et al., 2011).


Trace conditioning in insects-keep the trace!

Dylla KV, Galili DS, Szyszka P, Lüdke A - Front Physiol (2013)

Molecular requirements for trace conditioning and four non-exclusive models of possible coincidence detection. (A) Cellular and molecular requirements which were shown to contribute to Drosophila olfactory trace conditioning. Shuai et al. (2011) found that the targeted inhibition of Rac in the mushroom bodies increased trace-dependent memory formation. Also D1 dopamine receptor (DA1) expression in mushroom bodies was required for trace conditioning, as shown by rescue experiments (Shuai et al., 2011). Trace conditioning does not require the Rutabaga adenylyl cyclase (Rut-AC; Shuai et al., 2011), but delay and trace conditioning simulations both induced synergistic increases of cAMP (Tomchik and Davis, 2009). (B) Educated guesses about coincidence detection in delay conditioning might also apply to trace conditioning. (i) Presynaptic coincidence detection by an adenylyl cyclase (AC; shown in red). In the presynaptic neuron, the CS induces Ca2+ influx and Ca2+ binds to calmodulin (CaM). The US activates G protein-coupled monoaminergic receptors (GPCR) which activate the associated G protein (Gα). When Ca2+/CaM complex and activated G protein (Gα*) co-occur, the AC is activated more strongly than if they appear alone. This leads to an increased production of cAMP and to activation of protein kinase A (PKA) which enhances presynaptic transmitter release (Heisenberg, 2003). (ii) Postsynaptic coincidence detection by the N-methyl-D-aspartate-type glutamate (NMDA) receptor (shown in blue). The CS leads to presynaptic release of glutamate (Glu) which binds to the postsynaptic NMDA receptor. The US, on the other hand, induces the depolarization of the postsynaptic membrane, which allows for the removal of the Mg2+ block from the NMDA receptor channel. Opening of the NMDA receptor channel for Ca2+ influx is only possible when the CS and the US signal coincide. An elevation of the intracellular Ca2+ level leads to the activation of several kinases, inducing synaptic plasticity. The NMDA receptor is involved in delay conditioning in Drosophila (Miyashita et al., 2012) and was also shown to be involved in trace conditioning in vertebrates (Gilmartin and Helmstetter, 2010; Czerniawski et al., 2012). A possible role in insect trace conditioning has not yet been investigated. (iii) Radish (shown in green) is involved in a Rut-AC independent pathway (Isabel et al., 2004; Folkers et al., 2006) and might contribute to trace conditioning. (iv) Gilgamesh (Gish) (shown in purple), a casein kinase I γ homolog in flies, is required for short-term memory formation in Drosophila olfactory delay conditioning, functioning independently of Rut-AC and the cAMP pathway (Tan et al., 2010). Hypothetically, Gish mediates increased Ca2+ influx upon CS–US coincidence and thus might be a pathway for Rut-AC independent trace conditioning.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3750952&req=5

Figure 3: Molecular requirements for trace conditioning and four non-exclusive models of possible coincidence detection. (A) Cellular and molecular requirements which were shown to contribute to Drosophila olfactory trace conditioning. Shuai et al. (2011) found that the targeted inhibition of Rac in the mushroom bodies increased trace-dependent memory formation. Also D1 dopamine receptor (DA1) expression in mushroom bodies was required for trace conditioning, as shown by rescue experiments (Shuai et al., 2011). Trace conditioning does not require the Rutabaga adenylyl cyclase (Rut-AC; Shuai et al., 2011), but delay and trace conditioning simulations both induced synergistic increases of cAMP (Tomchik and Davis, 2009). (B) Educated guesses about coincidence detection in delay conditioning might also apply to trace conditioning. (i) Presynaptic coincidence detection by an adenylyl cyclase (AC; shown in red). In the presynaptic neuron, the CS induces Ca2+ influx and Ca2+ binds to calmodulin (CaM). The US activates G protein-coupled monoaminergic receptors (GPCR) which activate the associated G protein (Gα). When Ca2+/CaM complex and activated G protein (Gα*) co-occur, the AC is activated more strongly than if they appear alone. This leads to an increased production of cAMP and to activation of protein kinase A (PKA) which enhances presynaptic transmitter release (Heisenberg, 2003). (ii) Postsynaptic coincidence detection by the N-methyl-D-aspartate-type glutamate (NMDA) receptor (shown in blue). The CS leads to presynaptic release of glutamate (Glu) which binds to the postsynaptic NMDA receptor. The US, on the other hand, induces the depolarization of the postsynaptic membrane, which allows for the removal of the Mg2+ block from the NMDA receptor channel. Opening of the NMDA receptor channel for Ca2+ influx is only possible when the CS and the US signal coincide. An elevation of the intracellular Ca2+ level leads to the activation of several kinases, inducing synaptic plasticity. The NMDA receptor is involved in delay conditioning in Drosophila (Miyashita et al., 2012) and was also shown to be involved in trace conditioning in vertebrates (Gilmartin and Helmstetter, 2010; Czerniawski et al., 2012). A possible role in insect trace conditioning has not yet been investigated. (iii) Radish (shown in green) is involved in a Rut-AC independent pathway (Isabel et al., 2004; Folkers et al., 2006) and might contribute to trace conditioning. (iv) Gilgamesh (Gish) (shown in purple), a casein kinase I γ homolog in flies, is required for short-term memory formation in Drosophila olfactory delay conditioning, functioning independently of Rut-AC and the cAMP pathway (Tan et al., 2010). Hypothetically, Gish mediates increased Ca2+ influx upon CS–US coincidence and thus might be a pathway for Rut-AC independent trace conditioning.
Mentions: Recently, genetic and physiological studies in Drosophila gave insights into the molecular requirements of both conditioning forms (Tomchik and Davis, 2009; Shuai et al., 2011). Trace conditioning does not involve the Rutabaga adenylyl cyclase (Rut-AC; Figure 3A; Shuai et al., 2011), which is required for delay conditioning (Duerr and Quinn, 1982; Dudai et al., 1983). Furthermore, the inhibition of Rac enhanced learning performance in Drosophila trace conditioning, while delay conditioning remained unaffected (Shuai et al., 2011).

Bottom Line: It is still unknown how the brain encodes CS traces and how they are associated with a US in trace conditioning.In this review we summarize the recent progress in insect trace conditioning on the behavioral and physiological level and emphasize similarities and differences compared to delay conditioning.Moreover, we examine proposed molecular and computational models and reassess different experimental approaches used for trace conditioning.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Neurobiology, University of Konstanz Konstanz, Germany.

ABSTRACT
Trace conditioning is a form of associative learning that can be induced by presenting a conditioned stimulus (CS) and an unconditioned stimulus (US) following each other, but separated by a temporal gap. This gap distinguishes trace conditioning from classical delay conditioning, where the CS and US overlap. To bridge the temporal gap between both stimuli and to form an association between CS and US in trace conditioning, the brain must keep a neural representation of the CS after its termination-a stimulus trace. Behavioral and physiological studies on trace and delay conditioning revealed similarities between the two forms of learning, like similar memory decay and similar odor identity perception in invertebrates. On the other hand differences were reported also, like the requirement of distinct brain structures in vertebrates or disparities in molecular mechanisms in both vertebrates and invertebrates. For example, in commonly used vertebrate conditioning paradigms the hippocampus is necessary for trace but not for delay conditioning, and Drosophila delay conditioning requires the Rutabaga adenylyl cyclase (Rut-AC), which is dispensable in trace conditioning. It is still unknown how the brain encodes CS traces and how they are associated with a US in trace conditioning. Insects serve as powerful models to address the mechanisms underlying trace conditioning, due to their simple brain anatomy, behavioral accessibility and established methods of genetic interference. In this review we summarize the recent progress in insect trace conditioning on the behavioral and physiological level and emphasize similarities and differences compared to delay conditioning. Moreover, we examine proposed molecular and computational models and reassess different experimental approaches used for trace conditioning.

No MeSH data available.


Related in: MedlinePlus