Neuromodulatory pathways in learning and memory: Lessons from invertebrates (original) (raw)
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Neurobiology of Learning and Memory
2013
Studies in vertebrates and invertebrates have proved the instructive role that different biogenic amines play in the neural representation of rewards and punishments during associative learning. Results from diverse arthropods and using different learning paradigms initially agreed that dopamine (DA) is needed for aversive learning and octopamine (OA) is needed for appetitive learning. However, the notion that both amines constitute separate pathways for appetitive and aversive learning is changing. Here, we asked whether DA, so far only involved in aversive memory formation in honey bees, does also modulate appetitive memory. Using the well characterized appetitive olfactory conditioning of the proboscis extension reflex (PER), we show that DA impairs appetitive memory consolidation. In addition, we found that blocking DA receptors enhances appetitive memory. These results are consistent with the view that aversive and appetitive components interact during learning and memory forma...
The role of neuropeptides in learning: Insights from C. elegans
The International Journal of Biochemistry & Cell Biology, 2020
Learning is critical for survival as it provides the capacity to adapt to a changing environment. At the molecular and cellular level, learning leads to alterations within neural circuits that include synaptic rewiring and synaptic plasticity. These changes are mediated by signalling molecules known as neuromodulators. One such class of neuromodulators are neuropeptides, a diverse group of short peptides that primarily act through G protein-coupled receptors. There has been substantial progress in recent years on dissecting the role of neuropeptides in learning circuits using compact yet powerful invertebrate model systems. We will focus on insights gained using the nematode Caenorhabditis elegans, with its unparalleled genetic tractability, compact nervous system of ~300 neurons, high level of conservation with mammalian systems and amenability to a suite of behavioural analyses. Specifically, we will summarise recent 2 discoveries in C. elegans on the role of neuropeptides in non-associative and associative learning.
Memory consolidation and reconsolidation in an invertebrate model: The role of the GABAergic system
Neuroscience, 2009
Consolidation theory assumes that memories are labile during a limited time window after acquisition, but as time passes, memories become stable and resistant to amnesic agents. However, the vision of immutable memories after consolidation has been challenged. Thus, after the presentation of a reminder, the reactivated old memories become labile and again susceptible to amnesic treatments. This process implies a re-stabilization phase, usually referred to as reconsolidation.
2002
Experiments with invertebrates support the view that intracellular events subserving the consolidation phase of memory are preserved across evolution. Here, we investigate whether such evolutionary persistence extends to reconsolidation mechanisms, which have recently received special attention in vertebrate studies. For this purpose, the memory model of the crab Chasmagnathus is used. A visual danger stimulus (VDS) elicits crab escaping, which declines after a few stimulus presentations. The long-lasting retention of this decrement, called context-signal memory (CSM), is mediated by an association between contextual cues of the training site and the VDS. The present results show amnesia for CSM in crabs re-exposed at 24 hr (day 2) for 5 min to the learning context, 24 hr after training, and injected with one of two amnesic agents, then tested 24 hr later. Agents and timing were either 15 g of cycloheximide given between 1 hr before and 4 hr after re-exposure or 1 g/gm (ϩ)-5-methyl-10,11-dihydro-5H-dibenzo[a,d]cyclohepten-5,10imine given between 1 hr before and 2 hr after re-exposure. The amnesic effects are specific to behavior that occurs a long time after reactivation but not a short time after. No CSM deficit is produced by such agents when crabs are exposed to a context different from that of training. Findings are consistent with those reported for vertebrates, with both showing that reactivation induces a recapitulation of the postacquisition cascade of intracellular events. The agreement between results from such phylogenetically disparate animals suggests that evolution may have adopted a given molecular cascade as the preferred means of encoding experiences in the nervous system.
Molecular mechanisms of memory and learning
2009
The aim of the present review is to discuss the molecular mechanisms of learning and memory. The first part of the review investigates implicit memory in Aplysia, a marine snail, studied by Eric Kandel, the Nobel Prize winner. This form of learning can be broadly divided into two temporal phases, an early and a late phase. The molecular mechanisms of each phase will be analyzed in separate sections. The second part of the review investigates hippocampal-dependent explicit memory in ammals and the mechanism that underlies it, known as long-term potentiation (LTP). Similar to the molecular mechanisms in Aplysia, LTP is divided into an early and a late phase. However, LTP in mammals is a very complicated phenomenon that depends on the regulation of many molecular pathways. Moreover, the scientific community cannot always reach a consensus on the role of some of these molecular mechanisms in LTP. Nevertheless, it will be demonstrated that both explicit and implicit memory occur at a syn...
Toward elucidating diversity of neural mechanisms underlying insect learning
Zoological Letters, 2015
Insects are widely used as models to study neural mechanisms of learning and memory. Our recent studies on crickets, together with reports on other insect species, suggest that some fundamental differences exist in neural and molecular mechanisms of learning and memory among different species of insects, particularly between crickets and fruit flies. First, we suggested that in crickets octopamine (OA) and dopamine (DA) neurons convey reward and punishment signals, respectively, in associated learning. On the other hand, it has been reported that in fruit flies different sets of DA neurons convey reward or punishment signals. Secondly, we have suggested that in crickets OA and DA neurons participate in the retrieval of appetitive and aversive memories, respectively, while this is not the case in fruit flies. Thirdly, cyclic AMP signaling is critical for short-term memory formation in fruit flies, but not in crickets. Finally, nitric oxide-cyclic GMP signaling and calcium-calmodulin signaling are critical for long-term memory (LTM) formation in crickets, but such roles have not been reported in fruit flies. Not all of these differences can be ascribed to different experimental methods used in studies. We thus suggest that there are unexpected diversities in basic mechanisms of learning and memory among different insect species, especially between crickets and fruit flies. Studies on a larger number of insect species will help clarify the diversity of learning and memory mechanisms in relation to functional adaptation to the environment and evolutionary history.
2018
A common assumption from experiments that interfere with memory consolidation is that the resultant amnesia returns the brain of an animal to a tabula rasa state with respect to disturbed experience. However, recent studies in terrestrial snail classical conditioning revealed an odd phenomenon: animals were unable to relearn conditioned avoidance of specific food after this memory had been impaired by protein-synthesis inhibitors or N-methyl-D-aspartate (NMDA) receptor antagonists. Here we examined whether such specific memory reacquisition deficit can also be observed in vertebrate learning. We trained day-old chicks in a one-trial passive avoidance task by presenting them a bead of a specific color covered with a repellent substance, methyl anthranilate. Training was preceded by administration of the protein synthesis inhibitor anisomycin or the NMDA receptor antagonist MK-801. Both drugs produced permanent amnesia, and no spontaneous recovery of memory was observed. A second trai...
Learning & Memory, 2006
The terrestrial slug Limax is able to acquire short-term and long-term memories during aversive odor-taste associative learning. We investigated the effect of the selective serotonergic neurotoxin 5,7-dihydroxytryptamine (5,7-DHT) on memory. Behavioral studies indicated that 5,7-DHT impaired short-term memory but not long-term memory. HPLC (high-performance liquid chromatography) analysis revealed that 5,7-DHT significantly reduced serotonin content in the central nervous system. The present study suggests that acquisition, retention, and/or retrieval of short-term memory involves serotonin, and neither acquisition nor retrieval of long-term memory requires serotonin at a level as high as that required for short-term memory.