Precise spatial coding is preserved along the longitudinal hippocampal axis

Abstract

Compared with the dorsal hippocampus, relatively few studies have characterized neuronal responses in the ventral hippocampus. In particular, it is unclear whether and how cells in the ventral region represent space and/or respond to contextual changes. We recorded from dorsal and ventral CA1 neurons in freely moving mice exposed to manipulations of visuospatial and olfactory contexts. We found that ventral cells respond to alterations of the visuospatial environment such as exposure to novel local cues, cue rotations, and contextual expansion in similar ways to dorsal cells, with the exception of cue rotations. Furthermore, we found that ventral cells responded to odors much more strongly than dorsal cells, particularly to odors of high valence. Similar to earlier studies recording from the ventral hippocampus in CA3, we also found increased scaling of place cell field size along the longitudinal hippocampal axis. Although the increase in place field size observed toward the ventral pole has previously been taken to suggest a decrease in spatial information coded by ventral place cells, we hypothesized that a change in spatial scaling could instead signal a shift in representational coding that preserves the resolution of spatial information. To explore this possibility, we examined population activity using principal component analysis (PCA) and neural location reconstruction techniques. Our results suggest that ventral populations encode a distributed representation of space, and that the resolution of spatial information at the population level is comparable to that of dorsal populations of similar size. Finally, through the use of neural network modeling, we suggest that the redundancy in spatial representation along the longitudinal hippocampal axis may allow the hippocampus to overcome the conflict between memory interference and generalization inherent in neural network memory. Our results indicate that ventral population activity is well suited for generalization across locations and contexts.

Grid scale drives the scale and long-term stability of place maps

“…Even so, as grid spacing in ventral MEC is at least five times wider than spacing in dorsal MEC 47 and a general dorsal to ventral topography exists in the projections from MEC to CA1 48 , our simulations thus predict that, in the normal animal, ventral place cells should show more remapping than dorsal place cells when non-spatial cues change. This idea is consistent with experimental work demonstrating more remapping in ventral place cells after non-spatial manipulations, such as a change to the olfactory context 49 . Although we do not specify what anatomical sources might provide this unstable-spatial input, likely sources include the lateral entorhinal cortex, which encodes non-spatial contextual features 41 or the hippocampal CA2 region, where neurons gradually change their coding features to reflect the passage of hours to days 42 .…”

Hippocampus Contributions to Food Intake Control: Mnemonic, Neuroanatomical, and Endocrine Mechanisms

“…Efferent pathways arising from the vCA1 and vSub directly innervate the accessory olfactory bulb (61), suggesting a bidirectional modulation of olfactory processing in vHP neurons. Consistent with the preferential olfactory innervation of vHP vs. dHP, vCA1 neurons respond more strongly to aversive/avoided olfactory contextual cues compared to dCA1 neurons (49). …”

Memory integration constructs maps of space, time, and concepts

“…Place field gradients along the hippocampus axis may thus support integration of experiences at different spatial, temporal, and conceptual scales. For instance, large place fields in anterior hippocampus are well suited for integrating events that occur at different positions within the same environment, while smaller place fields in posterior hippocampus allow distinct coding of events experienced in the same environment [81]. It is possible that temporal representations may vary in scale along the hippocampal long axis in a similar manner to spatial representations, with larger timescales represented in anterior hippocampus and smaller timescales in posterior hippocampus [82].…”