Biogenic amines play major roles in the regulation of behavior in vertebrates and invertebrates. Previous studies in honey bees and fruit-flies Drosophila suggested that octopamine (OA, invertebrate counterpart of noradrenaline) and dopamine (DA) participate in appetitive olfactory conditioning with sucrose reward and aversive olfactory conditioning with electric shock punishment, respectively. In order to determine whether the effects of the two chatecholamines on electric shock and sugar learning can be generalized to other kinds of appetitive and aversive reinforcers, we studied the effects of OA and DA receptor antagonists on appetitive olfactory learning with water reward, and aversive olfactory learning with saline punishment in the cricket Gryllus bimaculatus. Crickets injected with epinastine or mianserin, OA receptor antagonists, into the hemolymph exhibited an impairment of appetitive learning with water reward, while aversive learning with saline punishment remained intact. In contrast, fluphenazine, chlorpromazine or spiperone, DA receptor antagonists, impaired aversive learning without affecting appetitive learning. This finding, combined with findings in previous studies, suggests that the octopaminergic reward system and dopaminergic punishment system participate in insect olfactory learning with various appetitive and aversive reinforcements.
Background: In insect classical conditioning, octopamine (the invertebrate counterpart of noradrenaline) or dopamine has been suggested to mediate reinforcing properties of appetitive or aversive unconditioned stimulus, respectively. However, the roles of octopaminergic and dopaminergic neurons in memory recall have remained unclear.
Insects, like vertebrates, have considerable ability to associate visual, olfactory or other sensory signals with reward or punishment. Previous studies in crickets, honey bees and fruit-flies have suggested that octopamine (OA, invertebrate counterpart of noradrenaline) and dopamine (DA) mediate various kinds of reward and punishment signals in olfactory learning. However, whether the roles of OA and DA in mediating positive and negative reinforcing signals can be generalized to learning of sensory signals other than odors remained unknown. Here we first established a visual learning paradigm in which to associate a visual pattern with water reward or saline punishment for crickets and found that memory after aversive conditioning decayed much faster than that after appetitive conditioning. Then, we pharmacologically studied the roles of OA and DA in appetitive and aversive forms of visual learning. 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 with saline punishment was unaffected. By contrast, fluphenazine, chlorpromazine or spiperone, DA receptor antagonists, completely impaired aversive learning without affecting appetitive learning. The results demonstrate that OA and DA participate in reward and punishment conditioning in visual learning. This finding, together with results of previous studies on the roles of OA and DA in olfactory learning, suggests ubiquitous roles of the octopaminergic reward system and dopaminergic punishment system in insect learning.
Cyclic AMP pathway plays an essential role in formation of long-term memory (LTM). In some species, the nitric oxide (NO)-cyclic GMP pathway has been found to act in parallel and complementary to the cAMP pathway for LTM formation. Here we describe a new role of the NO-cGMP pathway, namely, stimulation of the cAMP pathway to induce LTM. We have studied the signaling cascade underlying LTM formation by systematically coinjecting various "LTM-inducing" and "LTM-blocking" drugs in crickets. Multiple-trial olfactory conditioning led to LTM that lasted for several days, while memory induced by single-trial conditioning decayed away within several hours. Injection of inhibitors of the enzyme forming NO, cGMP, or cAMP into the hemolymph prior to multiple-trial conditioning blocked LTM, whereas injection of an NO donor, cGMP analog, or cAMP analog prior to single-trial conditioning induced LTM. Induction of LTM by injection of an NO donor or cGMP analog paired with single-trial conditioning was blocked by inhibitors of the cAMP pathway, but induction of LTM by a cAMP analog was unaffected by inhibitors of the NO-cGMP pathway. Inhibitors of cyclic nucleotide-gated channel (CNG channel) or calmodulin-blocked induction of LTM by cGMP analog paired with single-trial conditioning, but they did not affect induction of LTM by cAMP analog. Our findings suggest that the cAMP pathway is a downstream target of the NO-cGMP pathway for the formation of LTM, and that the CNG channel and calcium-calmodulin intervene between the NO-cGMP pathway and the cAMP pathway.In both vertebrates and invertebrates, nervous systems store information for short-term memory (STM) and long-term memory (LTM) by changing the strength of their synaptic connections (Kandel 2001). Studies in many species, including mollusca Aplysia, fruitflies Drosophila, and mice, suggest that STM storage is accompanied by transient changes in the strength of synaptic connections by covalent modifications of pre-existing proteins and that LTM storage, in contrast, is accompanied by enduring changes in synaptic strength that require transcription and translation of genes (Montarolo et al. 1986;DeZazzo and Tully 1995). In all of these species, formation of LTM requires an increase in intracellular cAMP and recruitment of the cAMP-dependent protein kinase (PKA) that phosphorylates the transcription factor, cAMP-responsive element-binding protein (CREB) (Bartsch et al. 1995;Yin et al. 1995;Abel et al. 1997).The roles of the cAMP pathway in the formation of LTM are often supplemented by other signaling pathways, most notably by the nitric oxide (NO)-cGMP signaling pathway (Lewin and Walters 1999;Lu et al. 1999). NO is a membrane-permeable molecule that functions in intercellular signaling in the brain (Garthwaite et al. 1988). In mice, NO contributes to late-phase longterm potentiation of synaptic transmission by stimulating soluble guanylate cyclase in target cells, and the resulting increase in cGMP concentration stimulates cGMP-dependent protein kinase (PKG), which acts in p...
The nitric oxide (NO)-cGMP signaling system and cAMP system play critical roles in formation of multiple-trial induced, protein synthesis-dependent long-term memory (LTM) in many vertebrates and invertebrates. The relationship between the NO-cGMP system and cAMP system, however, remains controversial. In honey bees, the two systems have been suggested to converge on protein kinase A (PKA), based on the finding in vitro that cGMP activates PKA when sub-optimal dose of cAMP is present. In crickets, however, we have suggested that NO-cGMP pathway operates on PKA via activation of adenylyl cyclase and production of cAMP for LTM formation. To resolve this issue, we compared the effect of multiple-trial conditioning against the effect of an externally applied cGMP analog for LTM formation in crickets, in the presence of sub-optimal dose of cAMP analog and in condition in which adenylyl cyclase was inhibited. The obtained results suggest that an externally applied cGMP analog activates PKA when sub-optimal dose of cAMP analog is present, as is suggested in honey bees, but cGMP produced by multiple-trial conditioning cannot activate PKA even when sub-optimal dose of cAMP analog is present, thus indicating that cGMP produced by multiple-trial conditioning is not accessible to PKA. We conclude that the NO-cGMP system stimulates the cAMP system for LTM formation. We propose that LTM is formed by an interplay of two classes of neurons, namely, NO-producing neurons regulating LTM formation and NO-receptive neurons that are more directly involved in formation of long-term synaptic plasticity underlying LTM formation.3 Main textRecent studies have suggested that many of the molecular mechanisms underlying learning and memory are conserved among vertebrates and invertebrates, the most convincing evidence for which has been obtained by the study of the mechanisms of the formation of LTM [7]. LTM is defined as a protein synthesis-dependent phase of memory lasting for day to a lifetime. It is usually formed by multiple pairing trials but not by a single trial. It has been demonstrated that the cAMP signaling system plays critical roles in producing LTM, or long-term synaptic plasticity considered to underlie LTM formation, in mammals [1], insects [6,19] and mollusks [2]. In all of these animals, production of cAMP stimulates PKA, and this activates the transcription factor CREB (cAMP element-binding protein). Activation of CREB leads to a protein synthesis-dependent long-term synaptic plasticity that underlies LTM formation [7,20].The NO-cGMP system also plays critical roles in the formation of LTM in mammals [9], honey bees [15,16], crickets [14] and mollusks [8]. NO is a membrane-permeable intercellular signaling molecule produced by NO synthase (NOS).NO diffuses into neighboring cells and stimulates soluble guanylyl cyclase, and produced cGMP plays various physiological roles [5], including induction of LTM in many animals.In crickets, we have reported that the NO-cGMP system and cAMP system play major roles in formatio...
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