Learning & memoryPub Date : 2024-06-11Print Date: 2024-05-01DOI: 10.1101/lm.053824.123
Barbara Webb
{"title":"Beyond prediction error: 25 years of modeling the associations formed in the insect mushroom body.","authors":"Barbara Webb","doi":"10.1101/lm.053824.123","DOIUrl":"10.1101/lm.053824.123","url":null,"abstract":"<p><p>The insect mushroom body has gained increasing attention as a system in which the computational basis of neural learning circuits can be unraveled. We now understand in detail the key locations in this circuit where synaptic associations are formed between sensory patterns and values leading to actions. However, the actual learning rule (or rules) implemented by neural activity and leading to synaptic change is still an open question. Here, I survey the diversity of answers that have been offered in computational models of this system over the past decades, including the recurring assumption-in line with top-down theories of associative learning-that the core function is to reduce prediction error. However, I will argue, a more bottom-up approach may ultimately reveal a richer algorithmic capacity in this still enigmatic brain neuropil.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":2.2,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199945/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306161","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2024-06-11Print Date: 2024-05-01DOI: 10.1101/lm.053825.123
Moshe Parnas, Julia E Manoim, Andrew C Lin
{"title":"Sensory encoding and memory in the mushroom body: signals, noise, and variability.","authors":"Moshe Parnas, Julia E Manoim, Andrew C Lin","doi":"10.1101/lm.053825.123","DOIUrl":"10.1101/lm.053825.123","url":null,"abstract":"<p><p>To survive in changing environments, animals need to learn to associate specific sensory stimuli with positive or negative valence. How do they form stimulus-specific memories to distinguish between positively/negatively associated stimuli and other irrelevant stimuli? Solving this task is one of the functions of the mushroom body, the associative memory center in insect brains. Here we summarize recent work on sensory encoding and memory in the <i>Drosophila</i> mushroom body, highlighting general principles such as pattern separation, sparse coding, noise and variability, coincidence detection, and spatially localized neuromodulation, and placing the mushroom body in comparative perspective with mammalian memory systems.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":2.2,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199953/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306208","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2024-06-11Print Date: 2024-05-01DOI: 10.1101/lm.054013.124
Oriane Turrel, Lili Gao, Stephan J Sigrist
{"title":"Presynaptic regulators in memory formation.","authors":"Oriane Turrel, Lili Gao, Stephan J Sigrist","doi":"10.1101/lm.054013.124","DOIUrl":"10.1101/lm.054013.124","url":null,"abstract":"<p><p>The intricate molecular and structural sequences guiding the formation and consolidation of memories within neuronal circuits remain largely elusive. In this study, we investigate the roles of two pivotal presynaptic regulators, the small GTPase Rab3, enriched at synaptic vesicles, and the cell adhesion protein Neurexin-1, in the formation of distinct memory phases within the <i>Drosophila</i> mushroom body Kenyon cells. Our findings suggest that both proteins play crucial roles in memory-supporting processes within the presynaptic terminal, operating within distinct plasticity modules. These modules likely encompass remodeling and maturation of existing active zones (AZs), as well as the formation of new AZs.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":2.2,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199941/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306205","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2024-06-11Print Date: 2024-05-01DOI: 10.1101/lm.053815.123
Caleb Larnerd, Neha Kachewar, Fred W Wolf
{"title":"<i>Drosophila</i> learning and memory centers and the actions of drugs of abuse.","authors":"Caleb Larnerd, Neha Kachewar, Fred W Wolf","doi":"10.1101/lm.053815.123","DOIUrl":"10.1101/lm.053815.123","url":null,"abstract":"<p><p>Drug addiction and the circuitry for learning and memory are intimately intertwined. Drugs of abuse create strong, inappropriate, and lasting memories that contribute to many of their destructive properties, such as continued use despite negative consequences and exceptionally high rates of relapse. Studies in <i>Drosophila melanogaster</i> are helping us understand how drugs of abuse, especially alcohol, create memories at the level of individual neurons and in the circuits where they function. <i>Drosophila</i> is a premier organism for identifying the mechanisms of learning and memory. <i>Drosophila</i> also respond to drugs of abuse in ways that remarkably parallel humans and rodent models. An emerging consensus is that, for alcohol, the mushroom bodies participate in the circuits that control acute drug sensitivity, not explicitly associative forms of plasticity such as tolerance, and classical associative memories of their rewarding and aversive properties. Moreover, it is becoming clear that drugs of abuse use the mushroom body circuitry differently from other behaviors, potentially providing a basis for their addictive properties.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":1.7,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199947/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306160","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2024-06-11Print Date: 2024-05-01DOI: 10.1101/lm.053823.123
Ruchira Basu, Thomas Preat, Pierre-Yves Plaçais
{"title":"Glial metabolism versatility regulates mushroom body-driven behavioral output in <i>Drosophila</i>.","authors":"Ruchira Basu, Thomas Preat, Pierre-Yves Plaçais","doi":"10.1101/lm.053823.123","DOIUrl":"10.1101/lm.053823.123","url":null,"abstract":"<p><p>Providing metabolic support to neurons is now recognized as a major function of glial cells that is conserved from invertebrates to vertebrates. However, research in this field has focused for more than two decades on the relevance of lactate and glial glycolysis for neuronal energy metabolism, while overlooking many other facets of glial metabolism and their impact on neuronal physiology, circuit activity, and behavior. Here, we review recent work that has unveiled new features of glial metabolism, especially in <i>Drosophila</i>, in the modulation of behavioral traits involving the mushroom bodies (MBs). These recent findings reveal that spatially and biochemically distinct modes of glucose-derived neuronal fueling are implemented within the MB in a memory type-specific manner. In addition, cortex glia are endowed with several antioxidant functions, whereas astrocytes can serve as pro-oxidant agents that are beneficial to redox signaling underlying long-term memory. Finally, glial fatty acid oxidation seems to play a dual fail-safe role: first, as a mode of energy production upon glucose shortage, and, second, as a factor underlying the clearance of excessive oxidative load during sleep. Altogether, these integrated studies performed in <i>Drosophila</i> indicate that glial metabolism has a deterministic role on behavior.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":1.7,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199944/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306202","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2024-06-11Print Date: 2024-05-01DOI: 10.1101/lm.053863.123
Ivy Chi Wai Chan, Nannan Chen, John Hernandez, Hagar Meltzer, Annie Park, Aaron Stahl
{"title":"Future avenues in <i>Drosophila</i> mushroom body research.","authors":"Ivy Chi Wai Chan, Nannan Chen, John Hernandez, Hagar Meltzer, Annie Park, Aaron Stahl","doi":"10.1101/lm.053863.123","DOIUrl":"10.1101/lm.053863.123","url":null,"abstract":"<p><p>How does the brain translate sensory information into complex behaviors? With relatively small neuronal numbers, readable behavioral outputs, and an unparalleled genetic toolkit, the <i>Drosophila</i> mushroom body (MB) offers an excellent model to address this question in the context of associative learning and memory. Recent technological breakthroughs, such as the freshly completed full-brain connectome, multiomics approaches, CRISPR-mediated gene editing, and machine learning techniques, led to major advancements in our understanding of the MB circuit at the molecular, structural, physiological, and functional levels. Despite significant progress in individual MB areas, the field still faces the fundamental challenge of resolving how these different levels combine and interact to ultimately control the behavior of an individual fly. In this review, we discuss various aspects of MB research, with a focus on the current knowledge gaps, and an outlook on the future methodological developments required to reach an overall view of the neurobiological basis of learning and memory.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":1.7,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199946/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306164","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2024-06-11Print Date: 2024-05-01DOI: 10.1101/lm.053810.123
Amoolya Sai Dwijesha, Akhila Eswaran, Jacob A Berry, Anna Phan
{"title":"Diverse memory paradigms in <i>Drosophila</i> reveal diverse neural mechanisms.","authors":"Amoolya Sai Dwijesha, Akhila Eswaran, Jacob A Berry, Anna Phan","doi":"10.1101/lm.053810.123","DOIUrl":"10.1101/lm.053810.123","url":null,"abstract":"<p><p>In this review, we aggregated the different types of learning and memory paradigms developed in adult <i>Drosophila</i> and attempted to assess the similarities and differences in the neural mechanisms supporting diverse types of memory. The simplest association memory assays are conditioning paradigms (olfactory, visual, and gustatory). A great deal of work has been done on these memories, revealing hundreds of genes and neural circuits supporting this memory. Variations of conditioning assays (reversal learning, trace conditioning, latent inhibition, and extinction) also reveal interesting memory mechanisms, whereas mechanisms supporting spatial memory (thermal maze, orientation memory, and heat box) and the conditioned suppression of innate behaviors (phototaxis, negative geotaxis, anemotaxis, and locomotion) remain largely unexplored. In recent years, there has been an increased interest in multisensory and multicomponent memories (context-dependent and cross-modal memory) and higher-order memory (sensory preconditioning and second-order conditioning). Some of this work has revealed how the intricate mushroom body (MB) neural circuitry can support more complex memories. Finally, the most complex memories are arguably those involving social memory: courtship conditioning and social learning (mate-copying and egg-laying behaviors). Currently, very little is known about the mechanisms supporting social memories. Overall, the MBs are important for association memories of multiple sensory modalities and multisensory integration, whereas the central complex is important for place, orientation, and navigation memories. Interestingly, several different types of memory appear to use similar or variants of the olfactory conditioning neural circuitry, which are repurposed in different ways.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":1.7,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199951/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306163","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2024-06-11Print Date: 2024-05-01DOI: 10.1101/lm.053922.124
Randolf Menzel, Jürgen Rybak
{"title":"Insights from the past: the work of Hans von Alten on the evolution of brain structure, ecological adaptation, and cognition in hymenopteran species.","authors":"Randolf Menzel, Jürgen Rybak","doi":"10.1101/lm.053922.124","DOIUrl":"10.1101/lm.053922.124","url":null,"abstract":"<p><p>In his treatise on arthropod brains, Hans von Alten (1910) focuses on a specific functional group of insects-the flying Hymenoptera-which exhibit a spectrum of lifestyles ranging from solitary to social. His work presents a distinctive comparative neuro-anatomical approach rooted in an eco-evolutionary and eco-behavioral background. We regard his publication as an exceptionally valuable source of information and seek to inspire the research community dedicated to the study of the insect brain to explore its insights further, even after more than 110 years. We have translated and annotated his work, expecting it to engage researchers not just with its remarkable drawings but also with its substantive content and exemplary research strategy. The present text is designed to complement von Alten's publication, situating it within the temporal context of nineteenth-century and early twentieth-century studies, and to draw connections to contemporary perspectives, especially concerning a central brain structure: the mushroom body.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":1.7,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199940/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306203","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2024-06-11Print Date: 2024-05-01DOI: 10.1101/lm.053997.124
Büşra Çoban, Haiko Poppinga, El Yazid Rachad, Bart Geurten, David Vasmer, Francisco Jesus Rodriguez Jimenez, Yogesh Gadgil, Stephan Hubertus Deimel, Idan Alyagor, Oren Schuldiner, Ilona C Grunwald Kadow, Thomas Dieter Riemensperger, Annekathrin Widmann, André Fiala
{"title":"The caloric value of food intake structurally adjusts a neuronal mushroom body circuit mediating olfactory learning in <i>Drosophila</i>.","authors":"Büşra Çoban, Haiko Poppinga, El Yazid Rachad, Bart Geurten, David Vasmer, Francisco Jesus Rodriguez Jimenez, Yogesh Gadgil, Stephan Hubertus Deimel, Idan Alyagor, Oren Schuldiner, Ilona C Grunwald Kadow, Thomas Dieter Riemensperger, Annekathrin Widmann, André Fiala","doi":"10.1101/lm.053997.124","DOIUrl":"10.1101/lm.053997.124","url":null,"abstract":"<p><p>Associative learning enables the adaptive adjustment of behavioral decisions based on acquired, predicted outcomes. The valence of what is learned is influenced not only by the learned stimuli and their temporal relations, but also by prior experiences and internal states. In this study, we used the fruit fly <i>Drosophila melanogaster</i> to demonstrate that neuronal circuits involved in associative olfactory learning undergo restructuring during extended periods of low-caloric food intake. Specifically, we observed a decrease in the connections between specific dopaminergic neurons (DANs) and Kenyon cells at distinct compartments of the mushroom body. This structural synaptic plasticity was contingent upon the presence of allatostatin A receptors in specific DANs and could be mimicked optogenetically by expressing a light-activated adenylate cyclase in exactly these DANs. Importantly, we found that this rearrangement in synaptic connections influenced aversive, punishment-induced olfactory learning but did not impact appetitive, reward-based learning. Whether induced by prolonged low-caloric conditions or optogenetic manipulation of cAMP levels, this synaptic rearrangement resulted in a reduction of aversive associative learning. Consequently, the balance between positive and negative reinforcing signals shifted, diminishing the ability to learn to avoid odor cues signaling negative outcomes. These results exemplify how a neuronal circuit required for learning and memory undergoes structural plasticity dependent on prior experiences of the nutritional value of food.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":2.2,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199950/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306209","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Learning & memoryPub Date : 2024-06-11Print Date: 2024-05-01DOI: 10.1101/lm.053894.123
Hans V Alten
{"title":"The Phylogeny of the Hymenopteran Brain.","authors":"Hans V Alten","doi":"10.1101/lm.053894.123","DOIUrl":"10.1101/lm.053894.123","url":null,"abstract":"","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":2.2,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199943/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306210","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}