Extensive Cortical Connectivity of the Human Hippocampal Memory System: Beyond the “What” and “Where” Dual Stream Model

Abstract

The human hippocampus is involved in forming new memories: damage impairs memory. The dual stream model suggests that object “what” representations from ventral stream temporal cortex project to the hippocampus via the perirhinal and then lateral entorhinal cortex, and spatial “where” representations from the dorsal parietal stream via the parahippocampal gyrus and then medial entorhinal cortex. The hippocampus can then associate these inputs to form episodic memories of what happened where. Diffusion tractography was used to reveal the direct connections of hippocampal system areas in humans. This provides evidence that the human hippocampus has extensive direct cortical connections, with connections that bypass the entorhinal cortex to connect with the perirhinal and parahippocampal cortex, with the temporal pole, with the posterior and retrosplenial cingulate cortex, and even with early sensory cortical areas. The connections are less hierarchical and segregated than in the dual stream model. This provides a foundation for a conceptualization for how the hippocampal memory system connects with the cerebral cortex and operates in humans. One implication is that prehippocampal cortical areas such as the parahippocampal TF and TH subregions and perirhinal cortices may implement specialized computations that can benefit from inputs from the dorsal and ventral streams.

Structural connectivity-based segmentation of the human entorhinal cortex

“…These authors further argue that existing data in monkeys substantiate this notion ( Doan et al., 2019 ). This is in line with new findings in humans indicating that the hippocampal-entorhinal-neocortical connections are far more complex than a pure segregation into “where” and “what” pathways ( Huang et al., 2021 ).…”

Structural connectivity-based segmentation of the human entorhinal cortex

“…These authors further argue that existing data in monkeys substantiate this notion (Doan, Lagartos-Donate, Nilssen, Ohara, & Witter, 2019). This is in line with new findings in humans indicating that the hippocampal-entorhinalneocortical connections are far more complex than a pure segregation into "where" and "what" pathways (C.-C. Huang, Rolls, Hsu, Feng, & Lin, 2021).…”

Introduction to the special issue on extrahippocampal contributions to hippocampal‐dependent memory

“…In this model, the socalled "what" and "where" pathways from the perirhinal cortex to the lateral entorhinal cortex and the postrhinal cortex to the medial entorhinal cortex, respectively, converge in the hippocampus and this gives rise to episodic memory formation (Eichenbaum et al, 2007). While this theory has merit and continues to influence the field, others have noted that the theory oversimplifies the neuroanatomical connections of the cortical inputs to the hippocampus (Huang et al, 2021;Nilssen et al, 2019) and parahippocampal regions (Agster & Burwell, 2013;Furtak et al, 2007;Kerr et al, 2007), and thus the neurobiological basis of memory. In this issue, two review papers reassess the dual stream theory of the medial temporal lobe memory system.…”