The analysis of neurons that exhibit receptive fields dependent on an organism's spatial location, such as grid, place or boundary cells typically begins by mapping their activity in space using ...firing rate maps. However, mapping approaches are varied and depend on multiple tuning parameters that are usually chosen qualitatively by the experimenter and thus vary significantly across studies. Small changes in parameters such as these can impact results significantly, yet, to date a quantitative investigation of firing rate maps has not been attempted. Using simulated datasets, we examined how tuning parameters, recording duration and firing field size affect the accuracy of spatial maps generated using the most widely used approaches. For each approach we found a clear subset of parameters which yielded low-error firing rate maps and isolated the parameters yielding 1) the least error possible and 2) the Pareto-optimal parameter set which balanced error, computation time, place field detection accuracy and the extrapolation of missing values. Smoothed bivariate histograms and averaged shifted histograms were consistently associated with the fastest computation times while still providing accurate maps. Adaptive smoothing and binning approaches were found to compensate for low positional sampling the most effectively. Kernel smoothed density estimation also compensated for low sampling well and resulted in accurate maps, but it was also among the slowest methods tested. Overall, the bivariate histogram, coupled with spatial smoothing, is likely the most desirable method in the majority of cases.
The representation of space in the brain Grieves, Roddy M.; Jeffery, Kate J.
Behavioural processes,
February 2017, 2017-Feb, 2017-02-00, 20170201, Letnik:
135
Journal Article
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•Animals appear to possess an internal representation of space or ‘cognitive map’.•Three neurons are thought to form the basis of this map: place, head direction and grid cells.•There ...are many other, less well understood types of spatially sensitive neuron.•A systems-level understanding of the brain requires that we also understand these neurons.•Here we review the spatially sensitive cells that are not place, head direction or grid cells.
Animals can navigate vast distances and often display behaviours or activities that indicate a detailed, internal spatial representation of their surrounding environment or a ‘cognitive map’. Over a century of behavioural research on spatial navigation in humans and animals has greatly increased our understanding of how this highly complex feat is achieved. In turn this has inspired half a century of electrophysiological spatial navigation and memory research which has further advanced our understanding of the brain. In particular, three functional cell types have been suggested to underlie cognitive mapping processes; place cells, head direction cells and grid cells. However, there are numerous other spatially modulated neurons in the brain. For a more complete understanding of the electrophysiological systems and behavioural processes underlying spatial navigation we must also examine these lesser understood neurons. In this review we will briefly summarise the literature surrounding place cells, head direction cells, grid cells and the evidence that these cells collectively form the neural basis of a cognitive map. We will then review literature covering many other spatially modulated neurons in the brain that perhaps further augment this cognitive map.
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.
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.
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.
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.
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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•Place fields repeat across parallel maze compartments, but not radial compartments•Lateral mammillary nuclei lesions increase field repetition in radial compartments•Head direction cells may drive place fields
Harland et al. show that lesions of the lateral mammillary nuclei, essential nodes in the head direction circuit, increase place field repetition across maze compartments facing different directions. This suggests that place cells and head direction cells work together to allow disambiguation of similar local environments.
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.
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.
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.
The hippocampus is thought to enable the encoding and retrieval of ongoing experience, the organization of that experience into structured representations like contexts, maps, and schemas, and the ...use of these structures to plan for the future. A central goal is to understand what the core computations supporting these functions are, and how these computations are realized in the collective action of single neurons. A potential access point into this issue is provided by 'splitter cells', hippocampal neurons that fire differentially on the overlapping segment of trajectories that differ in their past and/or future. However, the literature on splitter cells has been fragmented and confusing, owing to differences in terminology, behavioral tasks, and analysis methods across studies. In this review, we synthesize consistent findings from this literature, establish a common set of terms, and translate between single-cell and ensemble perspectives. Most importantly, we examine the combined findings through the lens of two major theoretical ideas about hippocampal function: representation of temporal context and latent state inference. We find that unique signature properties of each of these models are necessary to account for the data, but neither theory, by itself, explains all of its features. Specifically, the temporal gradedness of the splitter signal is strong support for temporal context, but is hard to explain using state models, while its flexibility and task-dependence is naturally accounted for using state inference, but poses a challenge otherwise. These theories suggest a number of avenues for future work, and we believe their application to splitter cells is a timely and informative domain for testing and refining theoretical ideas about hippocampal function.
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