The Postsubiculum and Spatial Learning: The Role of Postsubicular Synaptic Activity and Synaptic Plasticity in Hippocampal Place Cell, Object, and Object-Location Memory

Abstract

Visual landmarks exert stimulus control over spatial behavior and the spatially tuned firing of place, head-direction, and grid cells in the rodent. However, the neural site of convergence for representations of landmarks and representations of space has yet to be identified. A potential site of plasticity underlying associations with landmarks is the postsubiculum. To test this, we blocked glutamatergic transmission in the rat postsubiculum with CNQX, or NMDA receptor-dependent plasticity with D-AP5. These infusions were sufficient to block evoked potentials from the lateral dorsal thalamus and long-term depression following tetanization of this input to the postsubiculum, respectively. In a second experiment, CNQX disrupted the stability of rat hippocampal place cell fields in a familiar environment. In a novel environment, blockade of plasticity with D-AP5 in the postsubiculum did not block the formation of a stable place field map following a 6 h delay. In a final behavioral experiment, postsubicular infusions of both compounds blocked object-location memory in the rat, but did not affect object recognition memory. These results suggest that the postsubiculum is necessary for the recognition of familiar environments, and that NMDA receptor-dependent plasticity in the postsubiculum is required for the formation of new object-place associations that support recognition memory. However, plasticity in the postsubiculum is not necessary for the formation of new spatial maps.

Subcortical connections of the perirhinal, postrhinal, and entorhinal cortices of the rat. I. afferents

“…It is also strongly and reciprocally connected with the dorsal presubiculum, also called the postsubiculum (Agster and Burwell, ). The dorsal presubiculum is necessary for object location memory and for recognizing familiar environments (Bett et al, ). Overall, this pattern of connectivity positions the POR for contextual learning and memory and online representation of the current local context.…”

Hippocampal and subicular efferents and afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat

“…The dorsal presubiculum is known to process information about head direction and landmarks [reviewed in 95]. Inactivations of presubiculum disrupted performance on object location tasks and disrupted place fields recorded from dorsal hippocampus [96]. Lesions of the presubiculum and parasubiculum impaired performance on spatial working memory and object location [34], but this could be attributed to presubicular damage as the efferents and afferents of the pre and parasubiculum are distinctly different [97].…”

Opposing and Complementary Topographic Connectivity Gradients Revealed by Quantitative Analysis of Canonical and Noncanonical Hippocampal CA1 Inputs

“…Based on the present data, one would predict that proximal CA1 neurons, clearly dominated by these two inputs, would exhibit similar properties. Adding to this proposition, proximal CA1 also receives a greater density of presubiculum inputs, and temporary inactivation of presubiculum is known to degrade place-specific firing of CA1 neurons in familiar environments ( Bett et al, 2013 ). Thus, presubiculum and parasubiculum may significantly contribute to place-specific firing in proximal CA1.…”