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Investigating Learning and Memory in Humans  

Evangelia G. Chrysikou, Elizabeth Espinal, and Alexandra E. Kelly

Memory refers to the set of cognitive systems and the neural structures that support them that allow humans to learn from experience, leverage this knowledge to understand and guide behavior in the present, and use past memories to think about and plan for the future. Neuroscience research on learning and memory has leveraged advances in behavioral methods, structural and functional brain imaging, noninvasive brain stimulation, and lesion studies to evaluate synergies and dissociations among small- and large-scale neural networks in support of memory performance. Overall, this work has converged to a conceptualization of new memories as representations of distributed patterns of neural activity across cortical and subcortical brain systems that provide neural grounding of sensorimotor and perceptual experiences, actions, thoughts, and emotions, and which can be reinstated as a result of internal or external cues. Most of this literature has supported dissociations among working and long-term memory, as well as between procedural, episodic, and semantic memories. On the other hand, progress in human neuroscience methodologies has revealed the interdependence of these memory systems in the context of complex cognitive tasks and suggests a dynamic and highly interactive neural architecture underlying human learning and memory. Future neuroscience research is anticipated to focus on understanding the neural mechanisms supporting this interactivity at the cellular and systems levels, as well as investigating the time course of their engagement.

Article

Cephalopod Nervous System Organization  

Z. Yan Wang and Clifton W. Ragsdale

Over 700 species of cephalopods live in the Earth’s waters, occupying almost every marine zone, from the benthic deep to the open ocean to tidal waters. The greatly varied forms and charismatic behaviors of these animals have long fascinated humans. Cephalopods are short-lived, highly mobile predators with sophisticated brains that are the largest among the invertebrates. While cephalopod brains share a similar anatomical organization, the nervous systems of coleoids (octopus, squid, cuttlefish) and nautiloids all display important lineage-specific neural adaptations. The octopus brain, for example, has for its arms a well-developed tactile learning and memory system that is vestigial in, or absent from, that of other cephalopods. The unique anatomy of the squid giant fiber system enables rapid escape in the event of capture. The brain of the nautilus comprises fewer lobes than its coleoid counterparts, but contains olfactory system structures and circuits not yet identified in other cephalopods.

Article

Drosophila Reward Circuits  

John S. Hernandez, Tariq M. Brown, and Karla R. Kaun

The ability to sense and respond to a rewarding stimulus is a key advantage for animals in their natural environment. The circuits that mediate these responses are complex, and it has been difficult to identify the fundamental principles of reward structure and function. However, the well-characterized brain anatomy and sophisticated neurogenetic tools in Drosophila melanogaster make the fly an ideal model to understand the mechanisms through which reward is encoded. Drosophila find food, water, intoxicating substances, and social acts rewarding. Basic monoaminergic neurotransmitters, including dopamine (DA), serotonin (5-HT), and octopamine (OA), play a central role in encoding these rewards. DA is central to sensing, encoding, responding, and predicting reward, whereas 5-HT and OA carry information about the environment that influences DA circuit activity. In contrast, slower-acting neuromodulators such as hormones and neuropeptides play a key role in both encoding the pleasurable stimulus and modulating how the internal environment of the fly influences reward sensation and seeking. Recurring circuit motifs for reward signaling identified in Drosophila suggest that these key principles will help elucidate understanding of how reward circuits function in all animals.

Article

Crustacean Visual Circuits Underlying Behavior  

Daniel Tomsic and Julieta Sztarker

Decapod crustaceans, in particular semiterrestrial crabs, are highly visual animals that greatly rely on visual information. Their responsiveness to visual moving stimuli, with behavioral displays that can be easily and reliably elicited in the laboratory, together with their sturdiness for experimental manipulation and the accessibility of their nervous system for intracellular electrophysiological recordings in the intact animal, make decapod crustaceans excellent experimental subjects for investigating the neurobiology of visually guided behaviors. Investigations of crustaceans have elucidated the general structure of their eyes and some of their specializations, the anatomical organization of the main brain areas involved in visual processing and their retinotopic mapping of visual space, and the morphology, physiology, and stimulus feature preferences of a number of well-identified classes of neurons, with emphasis on motion-sensitive elements. This anatomical and physiological knowledge, in connection with results of behavioral experiments in the laboratory and the field, are revealing the neural circuits and computations involved in important visual behaviors, as well as the substrate and mechanisms underlying visual memories in decapod crustaceans.

Article

What Is a Neuronal Ensemble?  

Luis Carrillo-Reid and Rafael Yuste

Despite over a century of neuroscience research, the nature of the neural code, that is, how neuronal activity underlies motor, sensory, and cognitive functions, remains elusive. Understanding the causal relation between neuronal activity and behavior requires a new conceptual paradigm that considers groups of neurons, instead of individual neurons, as the functional building blocks of the brain. These “neuronal ensembles,” defined as groups of neurons with coordinated activity that are reliably recalled by sensory stimuli, motor programs, or cognitive states, could be basic modular functional units of neural circuits. This hypothesis is consistent with past and present neuroscience results and could provide a broader framework to more effectively decipher the neural code in normal brains and provide new insights into how abnormal brain activity could lead to mental and neurological disease.

Article

Behavioral Neuroendocrinology: Cognition  

Victoria Luine

The demonstration of steroid binding proteins in brain areas outside of the hypothalamus was a key neuroendocrine discovery in the 1980s. These findings suggested that gonadal hormones, estradiol and testosterone, may have additional functions besides controlling reproduction through the hypothalamic–pituitary–gonadal axis (HPG) and that glucocorticoids may also influence neural functions not related to the hypothalamic–pituitary–adrenal axis (HPA). In the past 30 years, since the early 1990s, a body of neuroendocrine studies in animals has provided evidence for these hypotheses, and in 2020, it is generally accepted that steroid hormones exert robust influences over cognition—both learning and memory. Gonadal hormones, predominantly estrogens, enhance learning and memory in rodents and humans and influence cognitive processes throughout the lifespan. Gonadal hormones bind to classical nuclear estrogen receptors and to membrane receptors to influence cognition. In contrast to the generally positive effects of gonadal hormones on learning and memory, adrenal hormones (glucocorticoids in rodents or cortisol in primates) released during chronic stress have adverse effects on cognition, causing impairments in both learning and memory. However, emerging evidence suggests that impairments may be limited only to males, as chronic stress in females does not usually impair cognition and, in many cases, enhances it. The cognitive resilience of females to stress may result from interactions between the HPG and HPA axis, with estrogens exerting neuroprotective effects against glucocorticoids at both the morphological and neurochemical level. Overall, knowledge of the biological underpinnings of hormonal effects on cognitive function has enormous implications for human health and well-being by providing novel tools for mitigating memory loss, for treating stress-related disorders, and for understanding the bases for resilience versus susceptibility to stress.

Article

The Role of Oxytocin and Vasopressin in the Neural Regulation of Social Behavior  

Heather K. Caldwell

Within the central nervous system, the neuropeptides oxytocin and vasopressin are key regulators of social behavior. While their effects can be nuanced, data suggest that they can influence behavior at multiple levels, including an individual’s personality/temperament, their social interactions in smaller groups (or one-on-one interactions), and their behavior in larger groups. At a mechanistic level, oxytocin and vasopressin help to integrate complex information—including aspects of an animal’s external and internal state—in order to shape behavioral output. Oxytocin and vasopressin help to modulate behaviors that bring animals together (i.e., cooperative behaviors) as well as behaviors that keep animals apart (i.e., competitive behaviors), with the modulatory effects often being species-, sex-, and context-dependent. While there continues to be extensive study of the function of these nonapeptides within individual brain nuclei, over the last two decades behavioral neuroendocrinologists have also made great strides in exploring their roles within larger brain networks that help to regulate social behavior. Looking forward, work on oxytocin and vasopressin will continue to shed light on how the neural regulation of social behaviors are similar, and/or dissimilar, within and between species and sexes, as well as provide insights into the neural chemistry that underlies behavioral differences in neurotypical and neurodivergent individuals.

Article

Caenorhabditis elegans Learning and Memory  

James S.H. Wong and Catharine H. Rankin

The nematode, Caenorhabditis elegans (C. elegans), is an organism useful for the study of learning and memory at the molecular, cellular, neural circuitry, and behavioral levels. Its genetic tractability, transparency, connectome, and accessibility for in vivo cellular and molecular analyses are a few of the characteristics that make the organism such a powerful system for investigating mechanisms of learning and memory. It is able to learn and remember across many sensory modalities, including mechanosensation, chemosensation, thermosensation, oxygen sensing, and carbon dioxide sensing. C. elegans habituates to mechanosensory stimuli, and shows short-, intermediate-, and long-term memory, and context conditioning for mechanosensory habituation. The organism also displays chemotaxis to various chemicals, such as diacetyl and sodium chloride. This behavior is associated with several forms of learning, including state-dependent learning, classical conditioning, and aversive learning. C. elegans also shows thermotactic learning in which it learns to associate a particular temperature with the presence or absence of food. In addition, both oxygen preference and carbon dioxide avoidance in C. elegans can be altered by experience, indicating that they have memory for the oxygen or carbon dioxide environment they were reared in. Many of the genes found to underlie learning and memory in C. elegans are homologous to genes involved in learning and memory in mammals; two examples are crh-1, which is the C. elegans homolog of the cAMP response element-binding protein (CREB), and glr-1, which encodes an AMPA glutamate receptor subunit. Both of these genes are involved in long-term memory for tap habituation, context conditioning in tap habituation, and chemosensory classical conditioning. C. elegans offers the advantage of having a very small nervous system (302 neurons), thus it is possible to understand what these conserved genes are doing at the level of single identified neurons. As many mechanisms of learning and memory in C. elegans appear to be similar in more complex organisms including humans, research with C. elegans aids our ever-growing understanding of the fundamental mechanisms of learning and memory across the animal kingdom.

Article

Spatial Cognition in Rodents  

Freyja Ólafsdóttir

Wayfinding, like other related spatial cognitive abilities, is a core function of all mobile animals. The past 50 years have a seen a plethora of research devoted to elucidating the neural basis of this function. This research has led to the identification of neuronal cell types—many of which can be found within the hippocampal area and afferent brain regions—that encode different spatial variables and together are thought to provide animals with a so-called “cognitive map.” Moreover, seminal research carried out over the past decade has identified a neural activity event—known as “replay”—that is thought to consolidate newly formed cognitive maps, so to commit them to long-term storage and support planning of goal-directed navigational trajectories in familiar, and perhaps novel, environments. Finally, this hippocampal spatial coding scheme has in recent years been postulated to extend to nonspatial domains, including episodic memory, suggesting it may play a general role in knowledge creation.

Article

Transcriptional Regulation Underlying Long-Term Sensitization in Aplysia  

Robert J. Calin-Jageman, Theresa Wilsterman, and Irina E. Calin-Jageman

The induction of a long-term memory requires both transcriptional change and neural plasticity. Many of the links between transcription and memory have been revealed through the study of long-term sensitization in the Aplysia genus of marine mollusks. Sensitization is a conserved, non-associative form of pain memory in which a painful stimulus produces an increase in arousal and defensive behavior. The neural circuits that help encode sensitization memory are well characterized, and sensitization can be simulated in neuronal cell cultures. One feature of sensitization in Aplysia is that only some training protocols initiate transcription and produce long-term memory; others produce only short-term memories. This occurs because the induction of long-term sensitization requires the activation of two signal-transduction pathways that regulate transcription: (a) a fast but transient activation of the cAMP/PKA pathway that activates the transcription factor CREB1 and (b) a delayed activation of the ERK isoform of MAPK that deactivates the transcriptional repressor CREB2. The effectiveness of different training protocols is based on the synchronization of these pathways. The cAMP/PKA and MAPK pathways are complex, involving extracellular and trans-synaptic signaling, feedback loops, and crosstalk. It has proven possible to model transcriptional activation with enough fidelity to generate in silico predictions for optimized learning, which has been validated in cell cultures and intact animals. Training protocols that successfully activate CREB1 while deactivating CREB2 produce a complex transcriptional cascade that helps encode long-term sensitization memory. The transcriptional cascade involves a focused wave of immediate-early transcriptional activations. This includes the activation of additional transcription factors, such as C/EBP, as well as effectors such as uch, sensorin, and tolloid/BMP-1. These early transcriptional changes close feedback loops that help extend and stabilize the early wave of transcriptional changes, triggering a broader late wave of transcriptional changes likely to alter neural signaling, increase protein production, transport mRNAs, and induce meta-plasticity. A small set of transcripts participate in both the early and late waves, and several of these (CREB1, synataxin, eIF4) play essential roles in completing the induction of long-term sensitization. Most transcriptional changes fade as sensitization memory is forgotten, but some changes persist beyond forgetting, including a long-lasting up-regulation of an inhibitory peptide transmitter that could foster forgetting. The maintenance of long-term sensitization may involve self-sustaining transcriptional feedback loops. In particular, CREB1 binds to its own promoter, producing a long-lasting increase in CREB1 mRNA, protein, and gene activation that is essential for sustaining cellular correlates of sensitization for at least 1 day after induction. Many aspects of the induction, stabilization, and maintenance of sensitization memory in Aplysia are conserved, suggesting that it will continue to be a fruitful, simpler system for understanding the physical basis of lasting memory.