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A recent study by Hadler and colleagues uncovered a novel form of plasticity of gamma oscillations in an ex vivo hippocampal slice preparation which they term 'gamma potentiation'. We discuss the potential cellular mechanisms of this form of plasticity and its functional and translational implications.
Assuntos
Ritmo Gama , Hipocampo , Plasticidade Neuronal , Animais , Humanos , Ritmo Gama/fisiologia , Hipocampo/fisiologia , Plasticidade Neuronal/fisiologiaRESUMO
The study of navigation is informed by ethological data from many species, laboratory investigation at behavioural and neurobiological levels, and computational modelling. However, the data are often species-specific, making it challenging to develop general models of how biology supports behaviour. Wiener et al. outlined a framework for organizing the results across taxa, called the 'navigation toolbox' (Wiener et al. In Animal thinking: contemporary issues in comparative cognition (eds R Menzel, J Fischer), pp. 51-76). This framework proposes that spatial cognition is a hierarchical process in which sensory inputs at the lowest level are successively combined into ever-more complex representations, culminating in a metric or quasi-metric internal model of the world (cognitive map). Some animals, notably humans, also use symbolic representations to produce an external representation, such as a verbal description, signpost or map that allows communication of spatial information or instructions between individuals. Recently, new discoveries have extended our understanding of how spatial representations are constructed, highlighting that the hierarchical relationships are bidirectional, with higher levels feeding back to influence lower levels. In the light of these new developments, we revisit the navigation toolbox, elaborate it and incorporate new findings. The toolbox provides a common framework within which the results from different taxa can be described and compared, yielding a more detailed, mechanistic and generalized understanding of navigation.
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Cognição , Navegação Espacial , Humanos , Animais , Simulação por ComputadorRESUMO
The cognitive map, proposed by Tolman in the 1940s, is a hypothetical internal representation of space constructed by the brain to enable an animal to undertake flexible spatial behaviors such as navigation. The subsequent discovery of place cells in the hippocampus of rats suggested that such a map-like representation does exist, and also provided a tool with which to explore its properties. Single-neuron studies in rodents conducted in small singular spaces have suggested that the map is founded on a metric framework, preserving distances and directions in an abstract representational format. An open question is whether this metric structure pertains over extended, often complexly structured real-world space. The data reviewed here suggest that this is not the case. The emerging picture is that instead of being a single, unified construct, the map is a mosaic of fragments that are heterogeneous, variably metric, multiply scaled, and sometimes laid on top of each other. Important organizing factors within and between fragments include boundaries, context, compass direction, and gravity. The map functions not to provide a comprehensive and precise rendering of the environment but rather to support adaptive behavior, tailored to the species and situation.
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Encéfalo , Navegação Espacial , Ratos , Animais , Encéfalo/fisiologia , Hipocampo/fisiologia , Comportamento Espacial , Mapeamento Encefálico/veterinária , Cognição/fisiologia , Percepção Espacial/fisiologia , Navegação Espacial/fisiologia , MamíferosRESUMO
Effective self-localization requires that the brain can resolve ambiguities in incoming sensory information arising from self-similarities (symmetries) in the environment structure. We investigated how place cells use environmental cues to resolve the ambiguity of a rotationally symmetric environment, by recording from hippocampal CA1 in rats exploring a "2-box." This apparatus comprises two adjacent rectangular compartments, identical but with directionally opposed layouts (cue card at one end and central connecting doorway) and distinguished by their odor contexts (lemon vs. vanilla). Despite the structural and visual rotational symmetry of the boxes, no place cells rotated their place fields. The majority changed their firing fields (remapped) between boxes but some repeated them, maintaining a translational symmetry and thus adopting a relationship to the layout that was conditional on the odor. In general, the place field ensemble maintained a stable relationship to environment orientation as defined by the odors, but sometimes the whole ensemble rotated its firing en bloc, decoupling from the odor context cues. While the individual elements of these observations-odor remapping, place field repetition, ensemble rotation, and decoupling from context-have been reported in isolation, the combination in the one experiment is incompletely explained within current models. We redress this by proposing a model in which odor cues enter into a three-way association with layout cues and head direction, creating a configural context signal that facilitates two separate processes: place field orientation and place field positioning. This configuration can subsequently still function in the absence of one of its components, explaining the ensemble decoupling from odor. We speculate that these interactions occur in retrosplenial cortex, because it has previously been implicated in context processing, and all the relevant signals converge here.
Assuntos
Sinais (Psicologia) , Hipocampo , Ratos , Animais , Odorantes , Percepção EspacialRESUMO
The thalamus and cortex are anatomically interconnected, with the thalamus providing integral information for cortical functions. The anteroventral thalamic nucleus (AV) is reciprocally connected to retrosplenial cortex (RSC). Two distinct AV subfields, dorsomedial (AVDM) and ventrolateral (AVVL), project differentially to granular vs. dysgranular RSC, respectively. To probe if functional responses of AV neurons differ, we recorded single neurons and local field potentials from AVDM and AVVL in rats during foraging. We observed place cells (neurons modulated by spatial location) in both AVDM and AVVL. Additionally, we characterized neurons modulated by theta oscillations, heading direction, and a conjunction of these. Place cells and conjunctive Theta-by-Head direction cells were more prevalent in AVVL; more non-conjunctive theta and directional neurons were prevalent in AVDM. These findings add further evidence that there are two thalamocortical circuits connecting AV and RSC, and reveal that the signaling involves place information in addition to direction and theta.
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The neural coding of space centres on three foundational cell types: place cells, head direction cells and grid cells. One notable characteristic of these neurons is the symmetry properties of their spatial firing patterns. In symmetric environments, firing patterns are often also symmetric: for example, place cells show translational symmetry in aligned sub-compartments of a multi-compartment environment. A single head direction cell has a mirror-symmetric firing pattern, while a sub-class of head direction cells can show multi-fold rotational symmetries in multi-compartment environments, matching the symmetry of the recently experienced environment. The entorhinal grid cells are notable for the symmetry of their firing patterns in both rotational and translational domains. However, these symmetries are broken in a variety of situations. These symmetry-making and -breaking observations shed light on the underlying computations that generate these firing patterns, and also invite speculation as to whether they may have a functional role. This article outlines these findings and speculates on the consequences of the resultant firing symmetries and asymmetries for spatial coding and cognition. This article is part of a discussion meeting issue 'New approaches to 3D vision'.
Assuntos
Córtex Entorrinal , Percepção Espacial , Córtex Entorrinal/fisiologia , Percepção Espacial/fisiologia , Neurônios/fisiologia , Potenciais de Ação/fisiologiaRESUMO
We investigated how environment symmetry shapes the neural processing of direction by recording directionally tuned retrosplenial neurons in male Lister hooded rats exploring multicompartment environments that had different levels of global rotational symmetry. Our hypothesis built on prior observations of twofold symmetry in the directional tuning curves of rats in a globally twofold-symmetric environment. To test whether environment symmetry was the relevant factor shaping the directional responses, here we deployed the same apparatus (two connected rectangular boxes) plus one with fourfold symmetry (a 2 × 2 array of connected square boxes) and one with onefold symmetry (a circular open-field arena). Consistent with our hypothesis we found many neurons with tuning curve symmetries that mirrored these environment symmetries, having twofold, fourfold, or onefold symmetric tuning, respectively. Some cells expressed this pattern only globally (across the whole environment), maintaining singular tuning curves in each subcompartment. However, others also expressed it locally within each subcompartment. Because multidirectionality has not been reported in naive rats in single environmental compartments, this suggests an experience-dependent effect of global environment symmetry on local firing symmetry. An intermingled population of directional neurons were classic head direction cells with globally referenced directional tuning. These cells were electrophysiologically distinct, with narrower tuning curves and a burstier firing pattern. Thus, retrosplenial directional neurons can simultaneously encode overall head direction and local head direction (relative to compartment layout). Furthermore, they can learn about global environment symmetry and express this locally. This may be important for the encoding of environment structure beyond immediate perceptual reach.SIGNIFICANCE STATEMENT We investigated how environment symmetry shapes the neural code for space by recording directionally tuned neurons from the retrosplenial cortex of rats exploring single- or multicompartment environments having onefold, twofold, or fourfold rotational symmetry. We found that many cells expressed a symmetry in their head direction tuning curves that matched the corresponding global environment symmetry, indicating plasticity of their directional tuning. They were also electrophysiologically distinct from canonical head directional cells. Notably, following exploration of the global space, many multidirectionally tuned neurons encoded global environment symmetry, even in local subcompartments. Our results suggest that multidirectional head direction codes contribute to the cognitive mapping of the complex structure of multicompartmented spaces.
Assuntos
Giro do Cíngulo , Orientação , Ratos , Masculino , Animais , Orientação/fisiologia , Neurônios/fisiologia , AprendizagemRESUMO
We investigated the contribution of visual imagination to the cognitive mapping of a building when initial exploration was simulated either visually by using a passive video walk-through, or mentally by using verbal guidance. Building layout had repeating elements with either rotational or mirror symmetry. Cognitive mapping of the virtual building, determined using questionnaires and map drawings, was present following verbal guidance but inferior to that following video guidance. Mapping was not affected by the building's structural symmetry. However, notably, it correlated with small-scale mental rotation scores for both video and verbal guidance conditions. There was no difference between males and females. A common factor that may have influenced cognitive mapping was the availability of visual information about the relationships of the building elements, either directly perceived (during the video walk-through) or imagined (during the verbal walk-through and/or during recall). Differences in visual imagination, particularly mental rotation, may thus account for some of the individual variance in cognitive mapping of complex built environments, which is relevant to how designers provide navigation-relevant information.
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Our planet is experiencing severe and accelerating climate and ecological breakdown caused by human activity. As professional scientists, we are better placed than most to understand the data that evidence this fact. However, like most other people, we ignore this inconvenient truth and lead our daily lives, at home and at work, as if these facts weren't true. In particular, we overlook that our own neuroscientific research practices, from our laboratory experiments to our often global travel, help drive climate change and ecosystem damage. We also hold privileged positions of authority in our societies but rarely speak out. Here, we argue that to help society create a survivable future, we neuroscientists can and must play our part. In April 2021, we delivered a symposium at the British Neuroscience Association meeting outlining what we think neuroscientists can and should do to help stop climate breakdown. Building on our talks (Box 1), we here outline what the climate and ecological emergencies mean for us as neuroscientists. We highlight the psychological mechanisms that block us from taking action, and then outline what practical steps we can take to overcome these blocks and work towards sustainability. In particular, we review environmental issues in neuroscience research, scientific computing, and conferences. We also highlight the key advocacy roles we can all play in our institutions and in society more broadly. The need for sustainable change has never been more urgent, and we call on all (neuro)scientists to act with the utmost urgency.
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Retrosplenial cortex (RSC) lies at the interface between sensory and cognitive networks in the brain and mediates between these, although it is not yet known how. It has two distinct subregions, granular (gRSC) and dysgranular (dRSC). The present study investigated how these subregions differ with respect to their electrophysiology and thalamic connectivity, as a step towards understanding their functions. The gRSC is more closely connected to the hippocampal formation, in which theta-band local field potential oscillations are prominent. We, therefore, compared theta-rhythmic single-unit activity between the two RSC subregions and found, mostly in gRSC, a subpopulation of non-directional cells with spiking activity strongly entrained by theta oscillations, suggesting a stronger coupling of gRSC to the hippocampal system. We then used retrograde tracers to test for differential inputs to RSC from the anteroventral thalamus (AV). We found that gRSC and dRSC differ in their afferents from two AV subfields: dorsomedial (AVDM) and ventrolateral (AVVL). Specifically: (1) as a whole AV projects more strongly to gRSC; (2) AVVL targets both gRSC and dRSC, while AVDM provides a selective projection to gRSC, (3) the gRSC projection is layer-specific: AVDM targets specifically gRSC superficial layers. These same AV projections are topographically organized with ventral AV neurons innervating rostral RSC and dorsal AV neurons innervating caudal RSC. These combined results suggest the existence of two distinct but interacting RSC subcircuits: one connecting AVDM to gRSC that may comprise part of the cognitive hippocampal system, and the other connecting AVVL to both RSC regions that may link hippocampal and perceptual regions. We suggest that these subcircuits are distinct to allow for differential weighting during integration of converging sensory and cognitive computations: an integration that may take place in thalamus, RSC, or both.
Assuntos
Córtex Cerebral/fisiologia , Giro do Cíngulo/fisiologia , Vias Neurais/fisiologia , Tálamo/fisiologia , Animais , Eletroencefalografia , Giro do Cíngulo/anatomia & histologia , Masculino , Vias Neurais/anatomia & histologia , Ratos , Ritmo Teta/fisiologiaRESUMO
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.
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Potenciais de Ação/fisiologia , Córtex Entorrinal/fisiologia , Comportamento Exploratório/fisiologia , Células de Grade/fisiologia , Modelos Neurológicos , Percepção Espacial/fisiologia , Animais , Córtex Entorrinal/citologia , Masculino , RatosRESUMO
Study of the neural code for space in rodents has many insights to offer for how mammals, including humans, construct a mental representation of space. This code is centered on the hippocampal place cells, which are active in particular places in the environment. Place cells are informed by numerous other spatial cell types including grid cells, which provide a signal for distance and direction and are thought to help anchor the place cell signal. These neurons combine self-motion and environmental information to create and update their map-like representation. Study of their activity patterns in complex environments of varying structure has revealed that this "cognitive map" of space is not a fixed and rigid entity that permeates space, but rather is variably affected by the movement constraints of the environment. These findings are pointing toward a more flexible spatial code in which the map is adapted to the movement possibilities of the space. An as-yet-unanswered question is whether these different forms of representation have functional consequences, as suggested by an enactivist view of spatial cognition.
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Cognição , Neurônios , Animais , Hipocampo , Humanos , Movimento (Física) , Percepção EspacialRESUMO
Flexible navigation relies on a cognitive map of space, thought to be implemented by hippocampal place cells: neurons that exhibit location-specific firing. In connected environments, optimal navigation requires keeping track of one's location and of the available connections between subspaces. We examined whether the dorsal CA1 place cells of rats encode environmental connectivity in four geometrically identical boxes arranged in a square. Rats moved between boxes by pushing saloon-type doors that could be locked in one or both directions. Although rats demonstrated knowledge of environmental connectivity, their place cells did not respond to connectivity changes, nor did they represent doorways differently from other locations. Place cells coded location in a global reference frame, with a different map for each box and minimal repetitive fields despite the repetitive geometry. These results suggest that CA1 place cells provide a spatial map that does not explicitly include connectivity.
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Hipocampo/citologia , Células de Lugar , Percepção Espacial , Potenciais de Ação , Animais , Células de Lugar/citologia , RatosRESUMO
How did brains evolve to become so complex, and what is their future? Brains pose an explanatory challenge because entropy, which inexorably increases over time, is commonly associated with disorder and simplicity. Recently we showed how evolution is an entropic process, building structures - organisms - which themselves facilitate entropy growth. Here we suggest that key transitional points in evolution extended organisms' reach into space and time, opening channels into new regions of a complex multidimensional state space that also allow entropy to increase. Brain evolution enabled representation of space and time, which vastly enhances this process. Some of these channels lead to tiny, dead-ends in the state space: the persistence of complex life is thus not thermodynamically guaranteed.
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Encéfalo , Entropia , HumanosRESUMO
The world faces a climate emergency. Here, we consider the actions that can be taken by neuroscientists to tackle climate change. We encourage neuroscientists to put emissions reductions at the center of their everyday professional activities.
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Aviação , Pegada de Carbono , Mudança Climática , Neurociências , Justiça Social , Congressos como Assunto , Emergências , Humanos , Plásticos , Pesquisa , Projetos de Pesquisa , Emissões de Veículos , Gravação em Vídeo , Comunicação por VideoconferênciaRESUMO
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.
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Células de Lugar/fisiologia , Percepção Espacial/fisiologia , Memória Espacial/fisiologia , Animais , Gravitação , Aprendizagem em Labirinto , Ratos , Telemetria/métodosRESUMO
Entorhinal grid cells integrate sensory and self-motion inputs to provide a spatial metric of a characteristic scale. One function of this metric may be to help localize the firing fields of hippocampal place cells during formation and use of the hippocampal spatial representation ("cognitive map"). Of theoretical importance is the question of how this metric, and the resulting map, is configured in 3D space. We find here that when the body plane is vertical as rats climb a wall, grid cells produce stable, almost-circular grid-cell firing fields. This contrasts with previous findings when the body was aligned horizontally during vertical exploration, suggesting a role for the body plane in orienting the plane of the grid cell map. However, in the present experiment, the fields on the wall were fewer and larger, suggesting an altered or absent odometric (distance-measuring) process. Several physiological indices of running speed in the entorhinal cortex showed reduced gain, which may explain the enlarged grid pattern. Hippocampal place fields were found to be sparser but unchanged in size/shape. Together, these observations suggest that the orientation and scale of the grid cell map, at least on a surface, are determined by an interaction between egocentric information (the body plane) and allocentric information (the gravity axis). This may be mediated by the different sensory or locomotor information available on a vertical surface and means that the resulting map has different properties on a vertical plane than a horizontal plane (i.e., is anisotropic).
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Córtex Entorrinal/fisiologia , Células de Grade/fisiologia , Dimensão Vertical , Animais , Hipocampo/fisiologia , Masculino , Modelos Neurológicos , Orientação , Células de Lugar/fisiologia , Ratos , Percepção EspacialRESUMO
Hippocampal place cells show position-specific activity thought to reflect a self-localization signal. Several reports also point to some form of goal encoding by place cells. We investigated this by asking whether they also encode the value of spatial goals, which is crucial information for optimizing goal-directed navigation. We used a continuous place navigation task in which male rats navigate to one of two (freely chosen) unmarked locations and wait, triggering the release of reward, which is then located and consumed elsewhere. This allows sampling of place fields and dissociates spatial goal from reward consumption. The two goals varied in the amount of reward provided, allowing assessment of whether the rats factored goal value into their navigational choice and of possible neural correlates of this value. Rats successfully learned the task, indicating goal localization, and they preferred higher-value goals, indicating processing of goal value. Replicating previous findings, there was goal-related activity in the out-of-field firing of CA1 place cells, with a ramping-up of firing rate during the waiting period, but no general overrepresentation of goals by place fields, an observation that we extended to CA3 place cells. Importantly, place cells were not modulated by goal value. This suggests that dorsal hippocampal place cells encode space independently of its associated value despite the effect of that value on spatial behavior. Our findings are consistent with a model of place cells in which they provide a spontaneously constructed value-free spatial representation rather than encoding other navigationally relevant but nonspatial information.SIGNIFICANCE STATEMENT We investigated whether hippocampal place cells, which compute a self-localization signal, also encode the relative value of places, which is essential information for optimal navigation. When choosing between two spatial goals of different value, rats preferred the higher-value goal. We saw out-of-field goal firing in place cells, replicating previous observations that the cells are influenced by the goal, but their activity was not modulated by the value of these goals. Our results suggest that place cells do not encode all of the navigationally relevant aspects of a place, but instead form a value-free "map" that links to such aspects in other parts of the brain.