PT - JOURNAL ARTICLE AU - Bethany E. Frost AU - Sean K. Martin AU - Matheus Cafalchio AU - Md Nurul Islam AU - John P. Aggleton AU - Shane M. O'Mara TI - Anterior Thalamic Inputs are Required for Subiculum Spatial Coding, with Associated Consequences for Hippocampal Spatial Memory AID - 10.1523/JNEUROSCI.2868-20.2021 DP - 2021 Jun 15 TA - The Journal of Neuroscience PG - JN-RM-2868-20 4099 - http://www.jneurosci.org/content/early/2021/06/15/JNEUROSCI.2868-20.2021.short 4100 - http://www.jneurosci.org/content/early/2021/06/15/JNEUROSCI.2868-20.2021.full AB - Just as hippocampal lesions are principally responsible for ‘temporal lobe’ amnesia, lesions affecting the anterior thalamic nuclei seem principally responsible for a similar loss of memory, ‘diencephalic’ amnesia. Compared to the former, the causes of diencephalic amnesia have remained elusive. A potential clue comes from how the two sites are interconnected, as within the hippocampal formation, only the subiculum has direct, reciprocal connections with the anterior thalamic nuclei. We found that both permanent and reversible anterior thalamic nuclei lesions in male rats cause a cessation of subicular spatial signalling, reduce spatial memory performance to chance, but leave hippocampal CA1 place cells largely unaffected. We suggest that a core element of diencephalic amnesia stems from the information loss in hippocampal output regions following anterior thalamic pathology.Significance Statement:At present, we know little about interactions between temporal lobe and diencephalic memory systems. Here, we focussed on the subiculum, as the sole hippocampal formation region directly interconnected with the anterior thalamic nuclei. We combined reversible and permanent lesions of the anterior thalamic nuclei, electrophysiological recordings of the subiculum, and behavioural analyses. Our results were striking and clear: following permanent thalamic lesions, the diverse spatial signals normally found in the subiculum (including place cells, grid cells, and head-direction cells) all disappeared. Anterior thalamic lesions had no discernible impact on hippocampal CA1 place fields. Thus, spatial firing activity within the subiculum requires anterior thalamic function, as does successful spatial memory performance. Our findings provide a key missing part of the much bigger puzzle concerning why anterior thalamic damage is so catastrophic for spatial memory in rodents and episodic memory in humans.