Behavioral correlates of the distributed coding of spatial context.

Hippocampal place cells respond heterogeneously to elemental changes of a compound spatial context, suggesting that they form a distributed code of context, whereby context information is shared across a population of neurons. The question arises as to what this distributed code might be useful for. The present study explored two possibilities: one, that it allows contexts with common elements to be disambiguated, and the other, that it allows a given context to be associated with more than one outcome. We used two naturalistic measures of context processing in rats, rearing and thigmotaxis (boundary-hugging), to explore how rats responded to contextual novelty and to relate this to the behavior of place cells. In experiment 1, rats showed dishabituation of rearing to a novel reconfiguration of familiar context elements, suggesting that they perceived the reconfiguration as novel, a behavior that parallels that of place cells in a similar situation. In experiment 2, rats were trained in a place preference task on an open-field arena. A change in the arena context triggered renewed thigmotaxis, and yet navigation continued unimpaired, indicating simultaneous representation of both the altered contextual and constant spatial cues. Place cells similarly exhibited a dual population of responses, consistent with the hypothesis that their activity underlies spatial behavior. Together, these experiments suggest that heterogeneous context encoding (or "partial remapping") by place cells may function to allow the flexible assignment of associations to contexts, a faculty that could be useful in episodic memory encoding.

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 degrees) 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.

Context-independent directional cue learning by hippocampal place cells.

In a symmetrical environment possessing no other polarizing visual cues, the spatially localized firing of hippocampal place cells can be primarily orientated by a reliable distal visual stimulus, such as a white cue card. However, if such a directional cue is made unreliable by being frequently moved in full view of the rat, the rat's internal sense of direction comes, over the course of a few days, to control the orientation of place fields instead. We investigated whether this simple form of 'cue-instability' learning would transfer to a new context, in which the firing patterns of the place cells become reorganized and in which a new spatial representation is thus active. We found that after cue-instability learning, the 'remapped' place field representation in the new environment was also orientated by the internal sense of direction of the rat rather than by the cue card, showing that the cue learning generalized from one context (and hence spatial representation) to another. This contrasts with another kind of place cell learning, in which the cells can acquire the ability to discriminate two spatial locations in one context but do not transfer this discrimination to a new context. We discuss the different effects of context changes on learned place cell activity in terms of the possible architecture of the inputs to place cells.

Responses of dorsal subicular neurons of rats during object exploration in an extended environment.

The subiculum receives a direct projection from the perirhinal cortex, a cortical area whose neurons are responsive to the novelty or familiarity of objects encountered in the environment. We made recordings of subicular neuronal activity while male adult Wistar rats conducted object exploration tasks, which have been previously shown to cause changes in the exploratory behaviour of rats and which are dependent upon the integrity of structures within the hippocampal formation. In the current study, the exploratory behaviour of the rats was also modified in a manner consistent with them perceiving the novelty and familiarity of the objects used as part of the apparatus. Subicular cell firing, however, appeared to correlate best not with object novelty or familiarity, but with the concurrent location and speed of the rats within the task environment. These findings are discussed in light of previously reported 'object-responsive' subicular firing correlates.

A proposed architecture for the neural representation of spatial context.

The role of context in guiding animal behavior has attracted increasing attention in recent years, but little is known about what constitutes a context, nor how and where in the brain it is represented. Contextual stimuli can take many forms, but of particular importance are those that collectively define a particular place or situation. The representation of place has been linked to the hippocampus, because its principal neurons ('place cells') are spatially responsive; behavioral experiments also implicate this structure in the processing of contextual stimuli. Together, these findings suggest a hippocampal role in representing 'spatial context'. The present article outlines a proposed architecture for the encoding of spatial context in which spatial inputs to place cells are modulated (or 'gated') by non-spatial stimuli. We discuss recent experimental evidence that spatial context is population-coded, a property which could allow both discrimination between overlapping contexts and generalization across them, and thus provide a foundation for animals' capacity for flexible context-linked place learning.

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.

Heterogeneous modulation of place cell firing by changes in context.

Hippocampal place cells show spatially localized activity that can be modulated by both geometric information (e.g., the distances and directions of features in the environment) and nongeometric information (e.g., colors, odors, and possibly behaviors). Nongeometric information may allow the discrimination of different spatial contexts. Understanding how nongeometric (or contextual) information affects hippocampal activity is important in light of proposals that the hippocampus may play a role in constructing a representation of spatial context. We investigated the contextual modulation of place cell activity by recording hippocampal place cells while rats foraged in compound contexts comprising black or white color paired with lemon or vanilla odor. Some cells responded to the color or odor changes alone, but most responded to varying combinations of both. Thus, we demonstrate, for the first time, that there is a heterogeneous input by contextual inputs into the hippocampus. We propose a model of contextual remapping of place cells in which the geometric inputs are selectively activated by subsets of contextual stimuli. Because it appears that different place cells are affected by different subsets of contextual stimuli, the representation of the entire context would require activity at the population level, supporting a role for the hippocampus in constructing a representation of spatial context.

Analysis of recordings of single-unit firing and population activity in the dorsal subiculum of unrestrained, freely moving rats.

We examined neuronal activity in the dorsal subiculum of unrestrained, male adult Wistar rats, which were implanted with a moveable eight-electrode microdrive. The subiculum is the primary hippocampal formation output area and is comparatively uninvestigated neurophysiologically. We compared subicular unit activity and the subicular EEG while rats occupied a small, restricted environment and also correlated neuronal activity with the ongoing behavior of the animal. Units were separated using their electrophysiological characteristics into bursting units, regular spiking units, theta-modulated units, and fast spiking units. The bursting and regular spiking unit classes are similar to hippocampal CA1 units, whereas the fast spiking units appear to be interneurons. Bursting units were variable in their behavior: some units bursted regularly, and others bursted only occasionally. Theta-modulated units have not been described before; these were similar to regular spiking units in all respects except that they increased their firing significantly when theta oscillations were present in the simultaneous EEG record. Subicular EEG was similar to hippocampal EEG, with theta oscillations dominating "alert, moving" behaviors, while large amplitude irregular activity (LIA), which included sharp waves, predominated when theta oscillations were not present, mainly during "alert, still" and "quiet" behaviors. A relatively small proportion of subicular recordings (approximately 32%) were phase-locked to theta; this is a smaller proportion than in areas from which the subiculum takes major inputs. The relative lack of entrainment of subicular neurons by this important intrinsic rhythm is suggestive of a limit to which theta might be capable of affecting both subicular and hippocampal information processing more generally.