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A fundamental property of place cells in the hippocampus is the anchoring of their firing fields to salient landmarks within the environment. However, it is unclear how such information reaches the hippocampus. In the current experiment, we tested the hypothesis that the stimulus control exerted by distal visual landmarks requires input from the medial entorhinal cortex (MEC). Place cells were recorded from mice with ibotenic acid lesions of the MEC (n = 7) and from sham-lesioned mice (n = 6) following 90° rotations of either distal landmarks or proximal cues in a cue- controlled environment. We found that lesions of the MEC impaired the anchoring of place fields to distal landmarks, but not proximal cues. We also observed that, relative to sham-lesioned mice, place cells in animals with MEC lesions exhibited significantly reduced spatial information and increased sparsity. These results support the view that distal landmark information reaches the hippocampus via the MEC, but that proximal cue information can do so via an alternative neural pathway.
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Corteza Entorrinal , Células de Lugar , Ratones , Animales , Corteza Entorrinal/patología , Hipocampo/patología , Vías Nerviosas , Señales (Psicología)RESUMEN
This study aimed to investigate differences in physical activity (PA) patterns and the associations between objectively measured 24-h movement behaviors and musculoskeletal measures (muscle strength, muscle mass, physical performance, and bone mineral density) in a high-income and a low-income community. This cross-sectional study recruited independent living older adults aged 60-85 years from high-income Scottish (n = 150) and low-income South African (n = 138) settings. Participants completed demographic and health questionnaires, and testing included body composition and bone mineral density (dual energy X-ray absorptiometry), physical performance (grip strength, gait speed), and PA (accelerometry). Participants accumulated similar amounts of weekly total PA, however, the Scottish cohort engaged in more moderate-to-vigorous intensity PA (MVPA) and sedentary behavior (SB), while the South African cohort spent more time sleeping and in light intensity PA (LPA). From compositional data analysis, more time spent in MVPA relative to the other movement behaviors was positively associated with higher muscle mass (p < 0.001) and strength (p = 0.001) in the Scottish cohort. Conversely, more time spent in MVPA was associated with faster gait speed (p < 0.001) and greater hip bone mineral density (p = 0.011) in the South African cohort. Our findings confirm the beneficial role of MVPA in both high- and low-income cohorts, however, the relationship MVPA had with components of musculoskeletal health in older adults differed between settings.
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Ejercicio Físico , Conducta Sedentaria , Acelerometría , Anciano , Anciano de 80 o más Años , Estudios Transversales , Humanos , Persona de Mediana Edad , EscociaRESUMEN
OBJECTIVE: Head direction cell and place cell spatially tuned firing is often anchored to salient visual landmarks on the periphery of a recording environment. What is less well understood is whether structural features of an environment, such as orientation of a maze sub-compartment or a polarizing barrier, can likewise control spatial firing. METHOD: We recorded from 54 head direction cells in the medial entorhinal cortex and subicular region of male Lister Hooded rats while they explored an apparatus with four parallel or four radially arranged compartments (Experiment 1). In Experiment 2, we recorded from 130 place cells (in Lister- and Long-Evans Hooded rats) and 30 head direction cells with 90° rotations of a cue card and a barrier in a single environment (Experiment 2). RESULTS: We found that head direction cells maintained a similar preferred firing direction across four separate maze compartments even when these faced different directions (Experiment 1). However, in an environment with a single compartment, we observed that both a barrier and a cue card exerted comparable amounts of stimulus control over head direction cells and place cells (Experiment 2). CONCLUSION: The maintenance of a stable directional orientation across maze compartments suggests that the head direction cell system has the capacity to provide a global directional reference that allows the animal to distinguish otherwise similar maze compartments based on the compartment's orientation. A barrier is, however, capable of controlling spatially tuned firing in an environment in which it is the sole polarizing feature.
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Células de Lugar , Animales , Cabeza , Hipocampo , Masculino , Neuronas , Orientación , Ratas , Ratas Long-Evans , Percepción EspacialRESUMEN
The distribution of attention between competing processing demands can have dramatic real-world consequences, however little is known about how limited attentional resources are distributed during real-world behaviour. Here we employ mobile EEG to characterise the allocation of attention across multiple sensory-cognitive processing demands during naturalistic movement. We used a neural marker of attention, the Event-Related Potential (ERP) P300 effect, to show that attention to targets is reduced when human participants walk compared to when they stand still. In a second experiment, we show that this reduction in attention is not caused by the act of walking per se. A third experiment identified the independent processing demands driving reduced attention to target stimuli during motion. ERP data reveals that the reduction in attention seen during walking reflects the linear and additive sum of the processing demands produced by visual and inertial stimulation. The mobile cognition approach used here shows how limited resources are precisely re-allocated according to the sensory processing demands that occur during real-world behaviour.
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Atención/fisiología , Cognición/fisiología , Electroencefalografía , Potenciales Relacionados con Evento P300/fisiología , Adolescente , Adulto , Femenino , Humanos , Masculino , Persona de Mediana EdadRESUMEN
Previous results suggest that directional information from the head direction cell circuit may inform hippocampal place cell firing when an animal is confronted with visually identical environments. To investigate whether such information might also be essential for spatial behavior, we tested adult, male Lister Hooded rats that had received either bilateral lateral mammillary nuclei (LMN) lesions or sham lesions on a four-way, conditional odor-location discrimination in compartments arranged at 60° to one another. We found that significantly fewer rats in the LMN lesion group were able to learn the task compared to the Sham group. We also found that the extent of the behavioral impairment was highly correlated with the degree of tissue loss in the LMN resulting from the lesion. Animals with LMN lesions were also impaired in a nonmatching-to-sample task in a T maze, and the extent of impairment likewise depended on the extent of the lesion. Performance in the odor-location and T-maze tasks was not affected by tissue loss in the medial mammillary nuclei. Together, these results indicate that the LMN, a key node in the head direction circuit, is critical for solving a spatial task that requires a directional discrimination. (PsycINFO Database Record (c) 2019 APA, all rights reserved).
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Conducta Espacial/fisiología , Procesamiento Espacial/fisiología , Potenciales de Acción , Animales , Cabeza/fisiología , Masculino , Tubérculos Mamilares/lesiones , Tubérculos Mamilares/fisiopatología , Vías Nerviosas/fisiología , Neuronas/metabolismo , Neuronas/fisiología , Ratas , Ratas Endogámicas , Tálamo/lesionesRESUMEN
The head direction cell system is an interconnected set of brain structures containing neurons whose firing is directionally tuned. The robust representation of allocentric direction by head direction cells suggests that they provide a neural compass for the animal. However, evidence linking head direction cells and spatial behavior has been mixed. Whereas damage to the hippocampus yields profound deficits in a range of spatial tasks, lesions to the head direction cell system often yield milder impairments in spatial behavior. In addition, correlational approaches have shown a correspondence between head direction cells and spatial behavior in some tasks, but not others. These mixed effects may be explained in part by a new view of the head direction cell system arising from recent demonstrations of at least two types of head direction cells: 'traditional' cells, and a second class of 'sensory' cells driven by polarising features of an environment. The recognition of different kinds of head direction cells now allows a nuanced assessment of this system's role in guiding navigation.
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Cabeza/fisiología , Red Nerviosa/fisiología , Propiocepción/fisiología , Conducta Espacial/fisiología , Animales , HumanosRESUMEN
A central question in neuroscience and psychology is how the mammalian brain represents the outside world and enables interaction with it. Significant progress on this question has been made in the domain of spatial cognition, where a consistent network of brain regions that represent external space has been identified in both humans and rodents. In rodents, much of the work to date has been done in situations where the animal is free to move about naturally. By contrast, the majority of work carried out to date in humans is static, due to limitations imposed by traditional laboratory based imaging techniques. In recent years, significant progress has been made in bridging the gap between animal and human work by employing virtual reality (VR) technology to simulate aspects of real-world navigation. Despite this progress, the VR studies often fail to fully simulate important aspects of real-world navigation, where information derived from self-motion is integrated with representations of environmental features and task goals. In the current review article, we provide a brief overview of animal and human imaging work to date, focusing on commonalties and differences in findings across species. Following on from this we discuss VR studies of spatial cognition, outlining limitations and developments, before introducing mobile brain imaging techniques and describe technical challenges and solutions for real-world recording. Finally, we discuss how these advances in mobile brain imaging technology, provide an unprecedented opportunity to illuminate how the brain represents complex multifaceted information during naturalistic navigation.
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A key challenge for animals is recognising locations and navigating between them. These capacities are varied: we can remember where our car is parked at the mall, rats are able to remember where their nest location is while foraging for food morsels, and bats are able to fly directly to a favourite fruit tree 20 kilometers from their home cave. These spatial abilities, whether commonplace or remarkable, raise fundamental questions. First, how do animals find their way? Second, how does the brain represent the outside world? In this Primer, we will address both questions from the perspective of rodent cognition and neuroscience.
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Cognición , Roedores/psicología , Navegación Espacial , Animales , Roedores/fisiologíaRESUMEN
A central tenet of systems neuroscience is that the mammalian hippocampus provides a cognitive map of the environment. This view is supported by the finding of place cells, neurons whose firing is tuned to specific locations in an animal's environment, within this brain region. Recent work, however, has shown that these cells repeat their firing fields across visually identical maze compartments [1, 2]. This repetition is not observed if these compartments face different directions, suggesting that place cells use a directional input to differentiate otherwise similar local environments [3, 4]. A clear candidate for this input is the head direction cell system. To test this, we disrupted the head direction cell system by lesioning the lateral mammillary nuclei and then recorded place cells as rats explored multiple, connected compartments, oriented in the same or in different directions. As shown previously, we found that place cells in control animals exhibited repeated fields in compartments arranged in parallel, but not in compartments facing different directions. In contrast, the place cells of animals with lesions of the head direction cell system exhibited repeating fields in both conditions. Thus, directional information provided by the head direction cell system appears essential for the angular disambiguation by place cells of visually identical compartments.
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Conducta Exploratoria , Hipocampo/fisiología , Tubérculos Mamilares/fisiopatología , Células de Lugar/fisiología , Animales , Cabeza/fisiología , Masculino , RatasRESUMEN
Hippocampal place cells support spatial cognition and are thought to form the neural substrate of a global "cognitive map." A widely held view is that parts of the hippocampus also underlie the ability to separate patterns or to provide different neural codes for distinct environments. However, a number of studies have shown that in environments composed of multiple, repeating compartments, place cells and other spatially modulated neurons show the same activity in each local area. This repetition of firing fields may reflect pattern completion and may make it difficult for animals to distinguish similar local environments. In this review we 1) highlight some of the navigation difficulties encountered by humans in repetitive environments, 2) summarize literature demonstrating that place and grid cells represent local and not global space, and 3) attempt to explain the origin of these phenomena. We argue that the repetition of firing fields can be a useful tool for understanding the relationship between grid cells in the entorhinal cortex and place cells in the hippocampus, the spatial inputs shared by these cells, and the propagation of spatially related signals through these structures.
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Mapeo Encefálico , Corteza Entorrinal/fisiología , Hipocampo/fisiología , Aprendizaje Espacial , Animales , Corteza Entorrinal/citología , Hipocampo/citología , Humanos , Neuronas/fisiología , Memoria ImplícitaRESUMEN
Hippocampal place cells fire at different rates when a rodent runs through a given location on its way to different destinations. However, it is unclear whether such firing represents the animal's intended destination or the execution of a specific trajectory. To distinguish between these possibilities, Lister Hooded rats (n = 8) were trained to navigate from a start box to three goal locations via four partially overlapping routes. Two of these led to the same goal location. Of the cells that fired on these two routes, 95.8% showed route-dependent firing (firing on only one route), whereas only two cells (4.2%) showed goal-dependent firing (firing similarly on both routes). In addition, route-dependent place cells over-represented the less discriminable routes, and place cells in general over-represented the start location. These results indicate that place cell firing on overlapping routes reflects the animal's route, not its goals, and that this firing may aid spatial discrimination.
How does the brain represent the outside world? One way of answering this question is to study the brains of rats, because the basic plan of a rodent's brain is similar to that of other mammals, such as humans. For example, the brains of rodents and humans both contain a structure called the hippocampus, which plays important roles in navigation and spatial memory. Cells within the hippocampus called place cells support these processes by firing electrical impulses whenever the animal occupies a specific location. When a rat runs along a corridor in a maze, its place cells often fire as it approaches a choice point. A given place cell will typically fire before the rat chooses a path leading towards one particular location, but not before choices that lead to other locations. The firing that occurs prior to the choice point is termed "prospective firing". However, it is not known whether the prospective firing of place cells represents the rat's final destination, or the specific route the animal takes to get there. To address this question, Grieves et al. designed a maze in which two different paths from a starting corridor led to the same goal location. If place cells represent the goal location, they should fire whichever route the rat chooses. However, if they represent the specific path the rat takes to the goal, they should fire on one or the other route, but not both. Grieves et al. found that almost all place cells with prospective activity in the starting corridor fired on a single route, as opposed to firing on both routes to the common goal. This suggests that the prospective firing in the hippocampus reflects the route the animal will take, rather than its intended destination. A future challenge will be to understand how the way the hippocampus codes routes interacts with brain circuits that code for intended goals, and how the activity of these circuits influences the animal's ability to navigate.
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Hipocampo/fisiología , Orientación Espacial , Células de Lugar/fisiología , Potenciales de Acción , Animales , Locomoción , RatasRESUMEN
There is a growing body of evidence that important aspects of human cognition have been marginalized, or overlooked, by traditional cognitive science. In particular, the use of laboratory-based experiments in which stimuli are artificial, and response options are fixed, inevitably results in findings that are less ecologically valid in relation to real-world behavior. In the present review we highlight the opportunities provided by a range of new mobile technologies that allow traditionally lab-bound measurements to now be collected during natural interactions with the world. We begin by outlining the theoretical support that mobile approaches receive from the development of embodied accounts of cognition, and we review the widening evidence that illustrates the importance of examining cognitive processes in their context. As we acknowledge, in practice, the development of mobile approaches brings with it fresh challenges, and will undoubtedly require innovation in paradigm design and analysis. If successful, however, the mobile cognition approach will offer novel insights in a range of areas, including understanding the cognitive processes underlying navigation through space and the role of attention during natural behavior. We argue that the development of real-world mobile cognition offers both increased ecological validity, and the opportunity to examine the interactions between perception, cognition and action-rather than examining each in isolation.
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Recent studies have shown that place cells in the hippocampus possess firing fields that repeat in physically similar, parallel environments. These results imply that it should be difficult for animals to distinguish parallel environments at a behavioral level. To test this, we trained rats on a novel odor-location task in an environment with four parallel compartments which had previously been shown to yield place field repetition. A second group of animals was trained on the same task, but with the compartments arranged in different directions, an arrangement we hypothesised would yield less place field repetition. Learning of the odor-location task in the parallel compartments was significantly impaired relative to learning in the radially arranged compartments. Fewer animals acquired the full discrimination in the parallel compartments compared to those trained in the radial compartments, and the former also required many more sessions to reach criterion compared to the latter. To confirm that the arrangement of compartments yielded differences in place cell repetition, in a separate group of animals we recorded from CA1 place cells in both environments. We found that CA1 place cells exhibited repeated fields across four parallel local compartments, but did not do so when the same compartments were arranged radially. To confirm that the differences in place field repetition across the parallel and radial compartments depended on their angular arrangement, and not incidental differences in access to an extra-maze visual landmark, we repeated the recordings in a second set of rats in the absence of the orientation landmark. We found, once again, that place fields showed repetition in parallel compartments, and did not do so in radially arranged compartments. Thus place field repetition, or lack thereof, in these compartments was not dependent on extra-maze cues. Together, these results imply that place field repetition constrains spatial learning.
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Región CA1 Hipocampal/fisiología , Ambiente , Neuronas/fisiología , Aprendizaje Espacial/fisiología , Potenciales de Acción , Animales , Estudios de Cohortes , Discriminación en Psicología/fisiología , Electrodos Implantados , Masculino , Pruebas Neuropsicológicas , Odorantes , Percepción Olfatoria/fisiología , Estimulación Física , Ratas , Procesamiento de Señales Asistido por ComputadorRESUMEN
The head direction system is composed of neurons found in a number of connected brain areas that fire in a sharply tuned, directional way. The function of this system, however, has not been fully established. To assess this, we devised a novel spatial landmark task, comparable to the paradigms in which stimulus control has been assessed for spatially tuned neurons. The task took place in a large cylinder and required rats to dig in a specific sand cup, from among 16 alternatives, to obtain a food reward. The reinforced cup was in a fixed location relative to a salient landmark, and probe sessions confirmed that the landmark exerted stimulus control over the rats' cup choices. To assess the contribution of the head direction cell system to this memory task, half of the animals received ibotenic acid infusions into the lateral mammillary nuclei (LMN), an essential node in the head direction network, while the other received sham lesions. No differences were observed in performance of this task between the 2 groups. Animals with LMN lesions were impaired, however, in reversal learning on a water maze task. These results suggest that the LMN, and potentially the head direction cell system, are not essential for the use of visual landmarks to guide spatial behavior.
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Tubérculos Mamilares/fisiología , Aprendizaje por Laberinto/fisiología , Memoria Espacial/fisiología , Navegación Espacial/fisiología , Animales , Agonistas de Aminoácidos Excitadores/toxicidad , Alimentos , Cabeza , Ácido Iboténico/toxicidad , Masculino , Tubérculos Mamilares/efectos de los fármacos , Tubérculos Mamilares/patología , Neuronas , Pruebas Neuropsicológicas , Ratas , Aprendizaje Inverso/fisiología , AguaRESUMEN
The discovery of place cells by John O'Keefe in the early 1970s was a breakthrough not just for systems neuroscience, but also for psychology: place fields provided a clear neural substrate for the notion of a cognitive map, a construct devised to explain rat learning and spatial cognition. However, is the robust location-related firing of place cells still best conceptualised as a cognitive map? In this commentary, we reassess this view of hippocampus function in light of subsequent findings on place cells. We argue that as place fields encode local space, and as they are modulated by ongoing behavior, the representation they provide may be more cognitive than map-like.
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Mapeo Encefálico , Cognición/fisiología , Hipocampo/fisiología , Neuronas/fisiología , Percepción Espacial/fisiología , Animales , Humanos , RatasRESUMEN
Two recent studies have shown that neurons which fire in a compass-like way--head direction cells--are present before rat pups open their eyes. Upon eye opening, the firing direction of these cells is anchored rapidly to visual landmarks.
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In decision-making, an immediate reward is usually preferred to a delayed reward, even if the latter is larger. We tested whether the hippocampus is necessary for this form of temporal discounting, and for vicarious trial-and-error at the decision point. Rats were trained on a recently developed, adjustable delay-discounting task (Papale et al. (2012) Cogn Affect Behav Neurosci 12:513-526), which featured a choice between a small, nearly immediate reward, and a larger, delayed reward. Rats then received either hippocampus or sham lesions. Animals with hippocampus lesions adjusted the delay for the larger reward to a level similar to that of sham-lesioned animals, suggesting a similar valuation capacity. However, the hippocampus lesion group spent significantly longer investigating the small and large rewards in the first part of the sessions, and were less sensitive to changes in the amount of reward in the large reward maze arm. Both sham- and hippocampus-lesioned rats showed a greater amount of vicarious trial-and-error on trials in which the delay was adjusted. In a nonadjusting version of the delay discounting task, animals with hippocampus lesions showed more variability in their preference for a larger reward that was delayed by 10 s compared with sham-lesioned animals. To verify the lesion behaviorally, rat were subsequently trained on a water maze task, and rats with hippocampus lesions were significantly impaired compared with sham-lesioned animals. The findings on the delay discounting tasks suggest that damage to the hippocampus may impair the detection of reward magnitude.
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Descuento por Demora/fisiología , Hipocampo/fisiología , Animales , Hipocampo/fisiopatología , Masculino , Aprendizaje por Laberinto , Pruebas Neuropsicológicas , Ratas , Recompensa , Factores de TiempoRESUMEN
In this commentary, we highlight a difficulty for metric navigation arising from recent data with grid and place cells: the integration of piecemeal representations of space in environments with repeated boundaries. Put simply, it is unclear how place and grid cells might provide a global representation of distance when their fields appear to represent repeated boundaries within an environment. One implication of this is that the capacity for spatial inferences may be limited.