Learning & memoryPub Date : 2024-06-14Print Date: 2024-05-01DOI: 10.1101/lm.053919.124
Carlotta Pribbenow, David Owald
{"title":"Skewing information flow through pre- and postsynaptic plasticity in the mushroom bodies of <i>Drosophila</i>.","authors":"Carlotta Pribbenow, David Owald","doi":"10.1101/lm.053919.124","DOIUrl":"10.1101/lm.053919.124","url":null,"abstract":"<p><p>Animal brains need to store information to construct a representation of their environment. Knowledge of what happened in the past allows both vertebrates and invertebrates to predict future outcomes by recalling previous experience. Although invertebrate and vertebrate brains share common principles at the molecular, cellular, and circuit-architectural levels, there are also obvious differences as exemplified by the use of acetylcholine versus glutamate as the considered main excitatory neurotransmitters in the respective central nervous systems. Nonetheless, across central nervous systems, synaptic plasticity is thought to be a main substrate for memory storage. Therefore, how brain circuits and synaptic contacts change following learning is of fundamental interest for understanding brain computations tied to behavior in any animal. Recent progress has been made in understanding such plastic changes following olfactory associative learning in the mushroom bodies (MBs) of <i>Drosophila</i> A current framework of memory-guided behavioral selection is based on the MB skew model, in which antagonistic synaptic pathways are selectively changed in strength. Here, we review insights into plasticity at dedicated <i>Drosophila</i> MB output pathways and update what is known about the plasticity of both pre- and postsynaptic compartments of <i>Drosophila</i> MB neurons.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":1.8,"publicationDate":"2024-06-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199954/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141321143","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 : 2024-06-14Print Date: 2024-05-01DOI: 10.1101/lm.053816.123
Aaron Stahl, Seth M Tomchik
{"title":"Modeling neurodegenerative and neurodevelopmental disorders in the <i>Drosophila</i> mushroom body.","authors":"Aaron Stahl, Seth M Tomchik","doi":"10.1101/lm.053816.123","DOIUrl":"10.1101/lm.053816.123","url":null,"abstract":"<p><p>The common fruit fly <i>Drosophila melanogaster</i> provides a powerful platform to investigate the genetic, molecular, cellular, and neural circuit mechanisms of behavior. Research in this model system has shed light on multiple aspects of brain physiology and behavior, from fundamental neuronal function to complex behaviors. A major anatomical region that modulates complex behaviors is the mushroom body (MB). The MB integrates multimodal sensory information and is involved in behaviors ranging from sensory processing/responses to learning and memory. Many genes that underlie brain disorders are conserved, from flies to humans, and studies in <i>Drosophila</i> have contributed significantly to our understanding of the mechanisms of brain disorders. Genetic mutations that mimic human diseases-such as Fragile X syndrome, neurofibromatosis type 1, Parkinson's disease, and Alzheimer's disease-affect MB structure and function, altering behavior. Studies dissecting the effects of disease-causing mutations in the MB have identified key pathological mechanisms, and the development of a complete connectome promises to add a comprehensive anatomical framework for disease modeling. Here, we review <i>Drosophila</i> models of human neurodevelopmental and neurodegenerative disorders via the effects of their underlying mutations on MB structure, function, and the resulting behavioral alterations.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":1.8,"publicationDate":"2024-06-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199955/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141321142","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.053839.123
Mareike Selcho
{"title":"Octopamine in the mushroom body circuitry for learning and memory.","authors":"Mareike Selcho","doi":"10.1101/lm.053839.123","DOIUrl":"10.1101/lm.053839.123","url":null,"abstract":"<p><p>Octopamine, the functional analog of noradrenaline, modulates many different behaviors and physiological processes in invertebrates. In the central nervous system, a few octopaminergic neurons project throughout the brain and innervate almost all neuropils. The center of memory formation in insects, the mushroom bodies, receive octopaminergic innervations in all insects investigated so far. Different octopamine receptors, either increasing or decreasing cAMP or calcium levels in the cell, are localized in Kenyon cells, further supporting the release of octopamine in the mushroom bodies. In addition, different mushroom body (MB) output neurons, projection neurons, and dopaminergic PAM cells are targets of octopaminergic neurons, enabling the modulation of learning circuits at different neural sites. For some years, the theory persisted that octopamine mediates rewarding stimuli, whereas dopamine (DA) represents aversive stimuli. This simple picture has been challenged by the finding that DA is required for both appetitive and aversive learning. Furthermore, octopamine is also involved in aversive learning and a rather complex interaction between these biogenic amines seems to modulate learning and memory. This review summarizes the role of octopamine in MB function, focusing on the anatomical principles and the role of the biogenic amine in learning and memory.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":1.8,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199948/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306204","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.053915.124
Shawn Mahoney, Jay Hosler, Brian H Smith
{"title":"Reinforcement expectation in the honeybee (<i>Apis mellifera</i>): Can downshifts in reinforcement show conditioned inhibition?","authors":"Shawn Mahoney, Jay Hosler, Brian H Smith","doi":"10.1101/lm.053915.124","DOIUrl":"10.1101/lm.053915.124","url":null,"abstract":"<p><p>When animals learn the association of a conditioned stimulus (CS) with an unconditioned stimulus (US), later presentation of the CS invokes a representation of the US. When the expected US fails to occur, theoretical accounts predict that conditioned inhibition can accrue to any other stimuli that are associated with this change in the US. Empirical work with mammals has confirmed the existence of conditioned inhibition. But the way it is manifested, the conditions that produce it, and determining whether it is the opposite of excitatory conditioning are important considerations. Invertebrates can make valuable contributions to this literature because of the well-established conditioning protocols and access to the central nervous system (CNS) for studying neural underpinnings of behavior. Nevertheless, although conditioned inhibition has been reported, it has yet to be thoroughly investigated in invertebrates. Here, we evaluate the role of the US in producing conditioned inhibition by using proboscis extension response conditioning of the honeybee (<i>Apis mellifera</i>). Specifically, using variations of a \"feature-negative\" experimental design, we use downshifts in US intensity relative to US intensity used during initial excitatory conditioning to show that an odorant in an odor-odor mixture can become a conditioned inhibitor. We argue that some alternative interpretations to conditioned inhibition are unlikely. However, we show variation across individuals in how strongly they show conditioned inhibition, with some individuals possibly revealing a different means of learning about changes in reinforcement. We discuss how the resolution of these differences is needed to fully understand whether and how conditioned inhibition is manifested in the honeybee, and whether it can be extended to investigate how it is encoded in the CNS. It is also important for extension to other insect models. In particular, work like this will be important as more is revealed of the complexity of the insect brain from connectome projects.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":1.8,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199939/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306206","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.053827.123
André Fiala, Karla R Kaun
{"title":"What do the mushroom bodies do for the insect brain? Twenty-five years of progress.","authors":"André Fiala, Karla R Kaun","doi":"10.1101/lm.053827.123","DOIUrl":"10.1101/lm.053827.123","url":null,"abstract":"<p><p>In 1998, a special edition of <i>Learning & Memory</i> was published with a discrete focus of synthesizing the state of the field to provide an overview of the function of the insect mushroom body. While molecular neuroscience and optical imaging of larger brain areas were advancing, understanding the basic functioning of neuronal circuits, particularly in the context of the mushroom body, was rudimentary. In the past 25 years, technological innovations have allowed researchers to map and understand the in vivo function of the neuronal circuits of the mushroom body system, making it an ideal model for investigating the circuit basis of sensory encoding, memory formation, and behavioral decisions. Collaborative efforts within the community have played a crucial role, leading to an interactive connectome of the mushroom body and accessible genetic tools for studying mushroom body circuit function. Looking ahead, continued technological innovation and collaborative efforts are likely to further advance our understanding of the mushroom body and its role in behavior and cognition, providing insights that generalize to other brain structures and species.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":1.8,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199942/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306211","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.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":1.8,"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}
{"title":"Cognitive limits of larval <i>Drosophila</i>: testing for conditioned inhibition, sensory preconditioning, and second-order conditioning.","authors":"Edanur Sen, Amira El-Keredy, Nina Jacob, Nino Mancini, Gülüm Asnaz, Annekathrin Widmann, Bertram Gerber, Juliane Thoener","doi":"10.1101/lm.053726.122","DOIUrl":"10.1101/lm.053726.122","url":null,"abstract":"<p><p><i>Drosophila</i> larvae are an established model system for studying the mechanisms of innate and simple forms of learned behavior. They have about 10 times fewer neurons than adult flies, and it was the low total number of their neurons that allowed for an electron microscopic reconstruction of their brain at synaptic resolution. Regarding the mushroom body, a central brain structure for many forms of associative learning in insects, it turned out that more than half of the classes of synaptic connection had previously escaped attention. Understanding the function of these circuit motifs, subsequently confirmed in adult flies, is an important current research topic. In this context, we test larval <i>Drosophila</i> for their cognitive abilities in three tasks that are characteristically more complex than those previously studied. Our data provide evidence for (i) conditioned inhibition, as has previously been reported for adult flies and honeybees. Unlike what is described for adult flies and honeybees, however, our data do not provide evidence for (ii) sensory preconditioning or (iii) second-order conditioning in <i>Drosophila</i> larvae. We discuss the methodological features of our experiments as well as four specific aspects of the organization of the larval brain that may explain why these two forms of learning are observed in adult flies and honeybees, but not in larval <i>Drosophila</i>.</p>","PeriodicalId":18003,"journal":{"name":"Learning & memory","volume":"31 5","pages":""},"PeriodicalIF":1.8,"publicationDate":"2024-06-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11199949/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141306162","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":1.8,"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":1.8,"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":1.8,"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}