Kathryn J. Jeffery

Context-specific acquisition of location discrimination by hippocampal place cells.

The spatially localized firing of rodent hippocampal place cells is strongly determined by the local geometry of the environment. Over time, however, the cells can acquire additional inputs, including inputs from more distal cues. This is manifest as a change in firing pattern (‘remapping’) when the new inputs are manipulated. Place cells also reorganize their firing in response to non‐geometric changes in ‘context’, such as a change in the colour or odour of the environment. The present study investigated whether the new inputs acquired by place cells in one context were still available to the cells when they expressed their altered firing patterns in a new context. We found that the acquired information did not transfer to the new context, suggesting that the context inputs and the acquired inputs must interact somewhere upstream of the place cells themselves. We present a model of one possible such interaction, and of how such an interaction could be modified by experience in a Hebbian manner, thus explaining the context specificity of the new learning.

LTP and spatial learning—Where to next?

Hebb suggested, in 1949, that memories could be stored by forming associative connections between neurons if the criterion for increasing the connection strength between them be that they were active simultaneously. Much attention has been devoted towards trying to determine a) if there is a physiological substrate of such a rule, and b) if so, whether the phenomenon participates in real‐life memory formation. The discovery of the electrically induced increase in synaptic strength known as long‐term potentiation (LTP), in the early 1970s, demonstrated that a neural version of the Hebb rule could be observed under laboratory conditions in the hippocampus, a structure important for some types of learning. However, a quarter of a century later, the evidence linking LTP to learning and memory is still contradictory. The purpose of the present article is to review and assess the types of approach that have been taken in trying to determine whether hippocampal synaptic plasticity participates in memory formation. Hippocampus 7:95–110, 1997.

How Heterogeneous Place Cell Responding Arises From Homogeneous Grids—A Contextual Gating Hypothesis

How entorhinal grids generate hippocampal place fields remains unknown. The simplest hypothesis—that grids of different scales are added together—cannot explain a number of place field phenomena, such as (1) Summed grids form a repeating, dispersed activation pattern whereas place fields are focal and nonrepeating; (2) Grid cells are active in all environments but place cells only in some, and (3) Partial environmental changes cause either heterogeneous (“partial”) remapping in place cells whereas they result in all‐or‐nothing “realignment” remapping in grid cells. We propose that this dissociation between grid cell and place cell behavior arises in the entorhinal‐dentate projection. By our view, the grid‐cell/place‐cell projection is modulated by context, both organizationally and activationally. Organizationally, we propose that when the animal first enters a new environment, the relatively homogeneous input from the grid cells becomes spatially clustered by Hebbian processes in the dendritic tree so that inputs active in the same context and having overlapping fields come to terminate on the same sub‐branches of the tree. Activationally, when the animal re‐enters the now‐familiar environment, active contextual inputs select (by virtue of their clustered terminations) which parts of the dendritic tree, and therefore which grid cells, drive the granule cell. Assuming this pattern of projections, our model successfully produces focal hippocampal place fields that remap appropriately to contextual changes.

Place Field Repetition and Purely Local Remapping in a Multicompartment Environment

Hippocampal place cells support spatial memory using sensory information from the environment and self-motion information to localize their firing fields. Currently, there is disagreement about whether CA1 place cells can use pure self-motion information to disambiguate different compartments in environments containing multiple visually identical compartments. Some studies report that place cells can disambiguate different compartments, while others report that they do not. Furthermore, while numerous studies have examined remapping, there has been little examination of remapping in different subregions of a single environment. Is remapping purely local or do place fields in neighboring, unaffected, regions detect the change? We recorded place cells as rats foraged across a 4-compartment environment and report 3 new findings. First, we find that, unlike studies in which rats foraged in 2 compartments, place fields showed a high degree of spatial repetition with a slight degree of rate-based discrimination. Second, this repetition does not diminish with extended experience. Third, remapping was found to be purely local for both geometric change and contextual change. Our results reveal the limited capacity of the path integrator to drive pattern separation in hippocampal representations, and suggest that doorways may play a privileged role in segmenting the neural representation of space.

A role for terrain slope in orienting hippocampal place fields

The three-dimensional topography of the environment is a potentially important source of orienting information for animals, but little is known about how such features affect either navigational behaviour or the neural representation of place. One component of the neural place representation comprises the hippocampal place cells, which show location-specific firing that can be oriented by directional cues in the environment. The present study investigated whether a simple topographical feature, terrain slope, could provide such orienting information to place cells. Place cells were recorded as rats explored a tilted (30°) square box located in the centre of a dark, curtained and visually symmetrical circular enclosure. The orientation of the tilted surface was varied, first in conjunction with that of a visible cue card (to stabilise the system) and then in the absence of the cue card, when the slope of the box was the only remaining stable polarising cue in the environment. In the latter condition, place fields continued to be reliably oriented by the slope. Thus, terrain slope provides sufficient orienting information to set and probably maintain the orientation of the hippocampal place system. This may explain previous behavioural observations that spatial orientation is improved when slope information is available.

Geometric Cues Influence Head Direction Cells Only Weakly in Nondisoriented Rats

The influential hypothesis that environmental geometry is critical for spatial orientation has been extensively tested behaviorally, and yet findings have been conflicting. Head direction (HD) cells, the neural correlate of the sense of direction, offer a window into the processes underlying directional orientation and may help clarify the issue. In the present study, HD cells were recorded as rats foraged in enclosures of varying geometry, with or without simultaneous manipulation of landmarks and self-motion cues (path integration). All geometric enclosures had single-order rotational symmetry and thus completely polarized the environment. They also had unique features, such as corners, which could, in principle, act as landmarks. Despite these strongly polarizing geometric cues, HD cells in nondisoriented rats never rotated with these shapes. In contrast, when a cue card (white or gray) was added to one wall, HD cells readily rotated with the enclosure. When path integration was disrupted by disorienting the rat, HD cells rotated with the enclosure even without the landmark. Collectively, these findings indicate that geometry exerts little or no influence on heading computations in nondisoriented rats, but it can do so in disoriented rats. We suggest that geometric processing is only a weak influence, providing a backup system for heading calculations and recruited only under conditions of disorientation.

Weighted cue integration in the rodent head direction system

How the brain combines information from different sensory modalities and of differing reliability is an important and still-unanswered question. Using the head direction (HD) system as a model, we explored the resolution of conflicts between landmarks and background cues. Sensory cue integration models predict averaging of the two cues, whereas attractor models predict capture of the signal by the dominant cue. We found that a visual landmark mostly captured the HD signal at low conflicts: however, there was an increasing propensity for the cells to integrate the cues thereafter. A large conflict presented to naive rats resulted in greater visual cue capture (less integration) than in experienced rats, revealing an effect of experience. We propose that weighted cue integration in HD cells arises from dynamic plasticity of the feed-forward inputs to the network, causing within-trial spatial redistribution of the visual inputs onto the ring. This suggests that an attractor network can implement decision processes about cue reliability using simple architecture and learning rules, thus providing a potential neural substrate for weighted cue integration.

Place Cells, Grid Cells, Attractors, and Remapping

Place and grid cells are thought to use a mixture of external sensory information and internal attractor dynamics to organize their activity. Attractor dynamics may explain both why neurons react coherently following sufficiently large changes to the environment (discrete attractors) and how firing patterns move smoothly from one representation to the next as an animal moves through space (continuous attractors). However, some features of place cell behavior, such as the sometimes independent responsiveness of place cells to environmental change (called “remapping”), seem hard to reconcile with attractor dynamics. This paper suggests that the explanation may be found in an anatomical separation of the two attractor systems coupled with a dynamic contextual modulation of the connection matrix between the two systems, with new learning being back-propagated into the matrix. Such a scheme could explain how place cells sometimes behave coherently and sometimes independently.

Theoretical accounts of spatial learning: A neurobiological view (commentary on Pearce, 2009)

Theories of learning have historically taken, as their starting point, the assumption that learning processes have universal applicability. This position has been argued on grounds of parsimony, but has received two significant challenges: first, from the observation that some kinds of learning, such as spatial learning, seem to obey different rules from others, and second, that some kinds of learning take place in processing modules that are separate from each other. These challenges arose in the behavioural literature but have since received considerable support from neurobiological studies, particularly single neuron studies of spatial learning, confirming that there are indeed separable (albeit highly intercommunicating) processing modules in the brain, which may not always interact (within or between themselves) according to classic associative principles. On the basis of these neurobiological data, reviewed here, it is argued that rather than assuming universality of associative rules, it is more parsimonious to assume sets of locally operating rules, each specialized for a particular domain. By this view, although almost all learning is associative in one way or another, the behavioural-level characterization of the rules governing learning may vary depending on which neural modules are involved in a given behaviour. Neurobiological studies, in tandem with behavioural studies, can help reveal the nature of these modules and the local rules by which they interact.

A theoretical account of cue averaging in the rodent head direction system

Head direction (HD) cell responses are thought to be derived from a combination of internal (or idiothetic) and external (or allothetic) sources of information. Recent work from the Jeffery laboratory shows that the relative influence of visual versus vestibular inputs upon the HD cell response depends on the disparity between these sources. In this paper, we present simulation results from a model designed to explain these observations. The model accurately replicates the Knight et al. data. We suggest that cue conflict resolution is critically dependent on plastic remapping of visual information onto the HD cell layer. This remap results in a shift in preferred directions of a subset of HD cells, which is then inherited by the rest of the cells during path integration. Thus, we demonstrate how, over a period of several minutes, a visual landmark may gain cue control. Furthermore, simulation results show that weaker visual landmarks fail to gain cue control as readily. We therefore suggest a second longer term plasticity in visual projections onto HD cell areas, through which landmarks with an inconsistent relationship to idiothetic information are made less salient, significantly hindering their ability to gain cue control. Our results provide a mechanism for reliability-weighted cue averaging that may pertain to other neural systems in addition to the HD system.