RESUMEN
Much of our understanding of navigation comes from the study of individual species, often with specific tasks tailored to those species. Here, we provide a novel experimental and analytic framework integrating across humans, rats, and simulated reinforcement learning (RL) agents to interrogate the dynamics of behavior during spatial navigation. We developed a novel open-field navigation task ("Tartarus maze") requiring dynamic adaptation (shortcuts and detours) to frequently changing obstructions on the path to a hidden goal. Humans and rats were remarkably similar in their trajectories. Both species showed the greatest similarity to RL agents utilizing a "successor representation," which creates a predictive map. Humans also displayed trajectory features similar to model-based RL agents, which implemented an optimal tree-search planning procedure. Our results help refine models seeking to explain mammalian navigation in dynamic environments and highlight the utility of modeling the behavior of different species to uncover the shared mechanisms that support behavior.
Asunto(s)
Navegación Espacial , Animales , Hipocampo , Humanos , Aprendizaje , Mamíferos , Ratas , Refuerzo en PsicologíaRESUMEN
We investigated how entorhinal grid cells encode volumetric space. On a horizontal surface, grid cells usually produce multiple, spatially focal, approximately circular firing fields that are evenly sized and spaced to form a regular, close-packed, hexagonal array. This spatial regularity has been suggested to underlie navigational computations. In three dimensions, theoretically the equivalent firing pattern would be a regular, hexagonal close packing of evenly sized spherical fields. In the present study, we report that, in rats foraging in a cubic lattice, grid cells maintained normal temporal firing characteristics and produced spatially stable firing fields. However, although most grid fields were ellipsoid, they were sparser, larger, more variably sized and irregularly arranged, even when only fields abutting the lower surface (equivalent to the floor) were considered. Thus, grid self-organization is shaped by the environment's structure and/or movement affordances, and grids may not need to be regular to support spatial computations.
Asunto(s)
Potenciales de Acción/fisiología , Corteza Entorrinal/fisiología , Conducta Exploratoria/fisiología , Células de Red/fisiología , Modelos Neurológicos , Percepción Espacial/fisiología , Animales , Corteza Entorrinal/citología , Masculino , RatasRESUMEN
We investigated how access to the vertical dimension influences the natural exploratory and foraging behaviour of rats. Using high-accuracy three-dimensional tracking of position in two- and three-dimensional environments, we sought to determine (i) how rats navigated through the environments with respect to gravity, (ii) where rats chose to form their home bases in volumetric space, and (iii) how they navigated to and from these home bases. To evaluate how horizontal biases may affect these behaviours, we compared a 3D maze where animals preferred to move horizontally to a different 3D configuration where all axes were equally energetically costly to traverse. Additionally, we compared home base formation in two-dimensional arenas with and without walls to the three-dimensional climbing mazes. We report that many behaviours exhibited by rats in horizontal spaces naturally extend to fully volumetric ones, such as home base formation and foraging excursions. We also provide further evidence for the strong differentiation of the horizontal and vertical axes: rats showed a horizontal movement bias, they formed home bases mainly in the bottom layers of both mazes and they generally solved the vertical component of return trajectories before and faster than the horizontal component. We explain the bias towards horizontal movements in terms of energy conservation, while the locations of home bases are explained from an information gathering view as a method for correcting self-localisation.
Asunto(s)
Percepción Espacial , Conducta Espacial , Animales , Sesgo , Movimiento , RatasRESUMEN
Place cells are spatially modulated neurons found in the hippocampus that underlie spatial memory and navigation: how these neurons represent 3D space is crucial for a full understanding of spatial cognition. We wirelessly recorded place cells in rats as they explored a cubic lattice climbing frame which could be aligned or tilted with respect to gravity. Place cells represented the entire volume of the mazes: their activity tended to be aligned with the maze axes, and when it was more difficult for the animals to move vertically the cells represented space less accurately and less stably. These results demonstrate that even surface-dwelling animals represent 3D space and suggests there is a fundamental relationship between environment structure, gravity, movement and spatial memory.
Asunto(s)
Células de Lugar/fisiología , Percepción Espacial/fisiología , Memoria Espacial/fisiología , Animales , Gravitación , Aprendizaje por Laberinto , Ratas , Telemetría/métodosRESUMEN
Adult-born granule cells (GCs), a minor population of cells in the hippocampal dentate gyrus, are highly active during the first few weeks after functional integration into the neuronal network, distinguishing them from less active, older adult-born GCs and the major population of dentate GCs generated developmentally. To ascertain whether young and old GCs perform distinct memory functions, we created a transgenic mouse in which output of old GCs was specifically inhibited while leaving a substantial portion of young GCs intact. These mice exhibited enhanced or normal pattern separation between similar contexts, which was reduced following ablation of young GCs. Furthermore, these mutant mice exhibited deficits in rapid pattern completion. Therefore, pattern separation requires adult-born young GCs but not old GCs, and older GCs contribute to the rapid recall by pattern completion. Our data suggest that as adult-born GCs age, their function switches from pattern separation to rapid pattern completion.
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Envejecimiento , Giro Dentado/citología , Giro Dentado/fisiología , Animales , Emparejamiento Cromosómico , Giro Dentado/crecimiento & desarrollo , Proteínas Fluorescentes Verdes/genética , Hipocampo/fisiología , Memoria , Ratones , Ratones TransgénicosRESUMEN
The idea that an already consolidated memory can become destabilized after recall and requires a process of reconsolidation to maintain it for subsequent use has gained much credence over the past decade. Experimental studies in rodents have shown pharmacological, genetic, or injurious manipulation at the time of memory reactivation can disrupt the already consolidated memory. Despite the force of experimental data showing this phenomenon, a number of questions have remained unanswered and no consensus has emerged as to the conditions under which a memory can be disrupted following reactivation. To date most rodent studies of reconsolidation are based on negatively reinforced memories, in particular fear-associated memories, while the storage and stability of forms of memory that do not rely on explicit reinforcement have been less often studied. In this review, we focus on recognition memory, a paradigm widely used in humans to probe declarative memory. We briefly outline recent advances in our understanding of the processes and brain circuits involved in recognition memory and review the evidence that recognition memory can undergo reconsolidation upon reactivation. We also review recent findings suggesting that some molecular mechanisms underlying consolidation of recognition memory are similarly recruited after recall to ensure memory stability, while others are more specifically engaged in consolidation or reconsolidation. Finally, we provide novel data on the role of Rsk2, a mental retardation gene, and of the transcription factor zif268/egr1 in reconsolidation of object-location memory, and offer suggestions as to how assessing the activation of certain molecular mechanisms following recall in recognition memory may help understand the relative importance of different aspects of remodeling or updating long-lasting memories.
RESUMEN
Recent work on the neural substrate of spatial memory strongly suggests the existence of a neuronal network dedicated to the coding of spatial information and allowing the subject to orient in space. This network includes place cells of the hippocampus, head direction cells which are found in several brain regions and particularly the post-subiculum, and grid cells in the entorhinal cortex. Several recently discovered features of place cell activity shed light on how the hippocampus contributes to memory construction. For instance, learning a novel environment relies on a dynamic population code in which place cell activity suddenly changes towards stable states built during previous experience. We briefly review these properties to show how they constrain the hippocampal memory code.
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Hipocampo/fisiología , Memoria/fisiología , Percepción Espacial/fisiología , Animales , Mapeo Encefálico , Ambiente , Conducta Exploratoria , Hipocampo/citología , Humanos , Ratones , Red Nerviosa/fisiología , Neuronas/citología , Neuronas/fisiologíaRESUMEN
Zif268 is a transcriptional regulator that plays a crucial role in maintenance of the late phases of hippocampal long-term potentiation (LTP) and consolidation of spatial memories. Because the hippocampal place cell system is essential for long-term spatial memory, we tested the hypothesis that zif268 is required for long-term stability of hippocampal place cell representations by recording CA1 place cells in mice lacking zif268. We found that zif268 gene deletion destabilized the representation of a familiar environment after exposure to a novel environment and impaired the long-term (24 h), but not short-term (1 h), stability of newly formed representations. These impairments could be rescued by repeated exposure to the novel environment, however. These results indicate that zif268 contributes to the long-term stability of spatial representations in CA1 and support the notion that the long-term stability of place cell representations requires transcription-dependent mechanisms similar to those observed in LTP.
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Proteína 1 de la Respuesta de Crecimiento Precoz/deficiencia , Hipocampo/fisiología , Memoria/fisiología , Células Piramidales/fisiología , Animales , Mapeo Encefálico , Células Cultivadas , Proteína 1 de la Respuesta de Crecimiento Precoz/genética , Eliminación de Gen , Potenciación a Largo Plazo/genética , Ratones , Ratones Noqueados , Factores de TiempoRESUMEN
The purpose of the present experiment was to examine how distal cues and proximal objects interact to control firing fields. In a previous study, Shapiro et al. (1997) Hippocampus 7:624-642, suggested that hippocampal place cell firing is controlled by distal cues and proximal floor inserts in a flexible and hierarchical fashion. Control exerted by the combined set of cues prevailed over control by distal cues, which itself prevailed over control by proximal cues. Here, we examined the generality of this hierarchy in the use of cues. Place cells were recorded as rats performed a pellet chasing task on a platform containing three proximal objects, surrounded by a curtain where three visual stimuli were hung. A double rotation of distal and proximal cue sets producing a 180 degrees mismatch revealed noncoherent responses of place cells. Most fields were controlled by the configuration of proximal and distal cues (i.e., remapped). Less often, fields were controlled by specific cues with a majority being controlled by proximal cues, thus suggesting that response hierarchy is modulated by the environment. We finally examined the effect of removing one set of cues after the double rotation session. Half of the fields were controlled by the remaining cues while the other half remapped, thus suggesting a competition between pattern completion and pattern separation processes. Furthermore, cells that were controlled by the remaining cues were mainly those that had remapped in the double rotation session. Our results are compatible with the idea that the flexibility of the place cell system results from an interaction between the sensory properties of individual cell and the attractor networks properties of the whole place cell population.
Asunto(s)
Potenciales de Acción/fisiología , Hipocampo/fisiología , Memoria/fisiología , Vías Nerviosas/fisiología , Neuronas/fisiología , Percepción Espacial/fisiología , Animales , Señales (Psicología) , Hipocampo/anatomía & histología , Red Nerviosa/fisiología , Pruebas Neuropsicológicas , Orientación/fisiología , Estimulación Luminosa , Ratas , Rotación , Transmisión Sináptica/fisiologíaRESUMEN
BACKGROUND: Anecdotal observations and early airplane and helicopter tracking studies suggest that pigeons sometimes follow large roads and use landmarks as turning points during their homeward journey. However, technical limitations in tracking pigeon routes have prevented proof. RESULTS: Here, we present experimental and statistical evidence for this strategy from the analysis of 216 GPS-recorded pigeon tracks over distances up to 50 km. Experienced pigeons released from familiar sites during 3 years around Rome, Italy, were significantly attracted to highways and a railway track running toward home, in many cases without anything forcing them to follow such guide-rails. Birds often broke off from the highways when these veered away from home, but many continued their flight along the highway until a major junction, even when the detour added substantially to their journey. The degree of road following increased with repeated releases but not flight length. Significant road following (in 40%-50% of the tracks) was mainly observed from release sites along northwest-southeast axis. CONCLUSIONS: Our data demonstrate the existence of a learned road-following homing strategy of pigeons and the use of particular topographical points for final navigation to the loft. Apparently, the better-directed early stages of the flight compensated the added final detour. During early and middle stages of the flight, following large and distinct roads is likely to reflect stabilization of a compass course rather than the presence of a mental roadmap. A cognitive (roadmap) component manifested by repeated crossing of preferred topographical points, including highway exits, is more likely when pigeons approach the loft area. However, it might only be expected in pigeons raised in an area characterized by navigationally relevant highway systems.