Field repetition and local mapping in the hippocampus and medial entorhinal cortex

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 will (a) highlight some of the navigation difficulties encountered by humans in repetitive environments, (b) summarise literature demonstrating that place and grid cells represent local and not global space, and (c) attempt to explain the origin of these phenomena. We argue that the repetition of firing fields can be a useful tool for understanding of 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

Irregular distribution of grid cell firing fields in rats exploring a 3D volumetric space

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

Contribution of Cerebellar Sensorimotor Adaptation to Hippocampal Spatial Memory

Complementing its primary role in motor control, cerebellar learning has also a bottom-up influence on cognitive functions, where high-level representations build up from elementary sensorimotor memories. In this paper we examine the cerebellar contribution to both procedural and declarative components of spatial cognition. To do so, we model a functional interplay between the cerebellum and the hippocampal formation during goal-oriented navigation. We reinterpret and complete existing genetic behavioural observations by means of quantitative accounts that cross-link synaptic plasticity mechanisms, single cell and population coding properties, and behavioural responses. In contrast to earlier hypotheses positing only a purely procedural impact of cerebellar adaptation deficits, our results suggest a cerebellar involvement in high-level aspects of behaviour. In particular, we propose that cerebellar learning mechanisms may influence hippocampal place fields, by contributing to the path integration process. Our simulations predict differences in place-cell discharge properties between normal mice and L7-PKCI mutant mice lacking long-term depression at cerebellar parallel fibre-Purkinje cell synapses. On the behavioural level, these results suggest that, by influencing the accuracy of hippocampal spatial codes, cerebellar deficits may impact the exploration-exploitation balance during spatial navigation

Cerebellar adaptation deficits reduce the rate of acquisition and the accuracy of hippocampal place field representations in the MWM.

<p><b>A–C.</b> Time course and accuracy of the hippocampal spatial map (measured in the whole environment) in simulated controls and mutants. The bar diagram in C shows the grand mean of the spatial code accuracy averaged over the entire training. <b>D–I.</b> Time course and accuracy of spatial map in the peripheral area (D–F) and the central region (G–I) of the MWM.</p

Cerebellar adaptation deficits impact the exploratory behaviour of simulated L7-PKCI mice.

<p>Time course of the spatial representation accuracy as a function of exploration time for both simulated controls and mutants undertaking a free-exploration task.</p

Insensitivity of place cells to the value of spatial goals in a two-choice flexible navigation task

International audienceHippocampal 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 foroptimizing 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 placefields and dissociates spatial goal from reward consumption. The two goals varied in the amount of reward provided, allowing assessment ofwhether the rats factored goal value into their navigational choice and of possible neural correlates of this value. Rats successfully learned thetask, indicating goal localization, and they preferred higher-value goals, indicating processing of goal value. Replicating previous findings, therewas 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 generaloverrepresentation of goals by place fields, an observation that we extended to CA3 place cells. Importantly, place cells were not modulated bygoal 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

The hypothesis of a cerebellar influence on path integration, and hence on hippocampal place coding, accounts for all L7-PKCIs' spatial navigation impairments observed experimentally.

<p>Occupancy maps in the MWM. Three-dimensional diagrams of the mean time spent by control and mutant mice at each location of the maze at different training phases (days, 1, 3, 5, 7 and 10). A grid of resolution 31 × 31 (each grid cell is 5 × 5 cm) samples spatial locations. The value associated to each grid cell is the normalised time spent in the cell region with respect to the duration of each trial, averaged over all day trials and over all animals of a group.</p

Cerebellar microcomplex model.

<p><b>A.</b> A simplified scheme of the cerebellar microcomplex (adapted from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0032560#pone.0032560-Medina2" target="_blank">[114]</a>). Information enters the cerebellum via two neural pathways: the mossy fibres convey multimodal sensorimotor signals, whereas climbing fibres are assumed to convey error-related information. Granule cells process and transmit sensorimotor inputs to Purkinje cells. Error-related signals also converge onto Purkinje cell synapses, which undergo long-term modifications (i.e. long-term potentiation, LTP, and depression, LTD). <b>B.</b> Model cerebellar microcomplex circuit. Each box indicates a population of spiking neurons. The same cerebellar circuit implements both forward (dark gray inputs) and inverse (white inputs) internal models.</p

Model architecture and simulated navigation protocols.

<p><b>A.</b> Overview of the connectionist model implementing a functional coupling between cerebellar and hippocampal networks. Note that arrows indicate functional projections, which do not necessarily correspond to direct anatomical pathways. <b>B.</b> The simulated Morris watermaze <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0032560#pone.0032560-Morris1" target="_blank">[26]</a> consists of a circular maze of cm in diameter. <b>C.</b> The simulated Starmaze <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0032560#pone.0032560-RondiReig2" target="_blank">[54]</a> is also a circular maze ( cm in diameter) but it contains alleys ( cm in width) forming a central pentagonal ring with radiating arms from each vertex. Both tasks require simulated animals to reach an escape platform ( cm in diameter) hidden below the surface of opaque water at a fixed location (black dashed cylinder). At each trial, animals start from one location that is randomly drawn from four possible starting locations (black stars). In both tasks animals can use available visual landmarks (coloured stars) as well as self-motion cues to learn allocentric spatial representations.</p