Complementary Functional Organization of Neuronal Activity Patterns in the Perirhinal, Lateral Entorhinal, and Medial Entorhinal Cortices

• Published in: The Journal of neuroscience Vol. 36; no. 13; pp. 3660 - 3675
• Main Authors: Keene, Christopher S, Bladon, John, McKenzie, Sam, Liu, Cindy D, O'Keefe, Joseph, Eichenbaum, Howard
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 30.03.2016
• Subjects: Action Potentials - physiology; Analysis of Variance; Animals; Bayes Theorem; Brain Mapping; Cues; Entorhinal Cortex - cytology; Hippocampus - cytology; Male; Models, Neurological; Nerve Net - physiology; Neurons - physiology; Photic Stimulation; Rats; Rats, Long-Evans; Space Perception - physiology; lateral entorhinal cortex; memory; hippocampus; medial entorhinal cortex; perirhinal cortex
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/jneurosci.4368-15.2016

It is commonly conceived that the cortical areas of the hippocampal region are functionally divided into the perirhinal cortex (PRC) and the lateral entorhinal cortex (LEC), which selectively process object information; and the medial entorhinal cortex (MEC), which selectively processes spatial information. Contrary to this notion, in rats performing a task that demands both object and spatial information processing, single neurons in PRC, LEC, and MEC, including those in both superficial and deep cortical areas and in grid, border, and head direction cells of MEC, have a highly similar range of selectivity to object and spatial dimensions of the task. By contrast, representational similarity analysis of population activity reveals a key distinction in the organization of information in these areas, such that PRC and LEC populations prioritize object over location information, whereas MEC populations prioritize location over object information. These findings bring to the hippocampal system a growing emphasis on population analyses as a powerful tool for characterizing neural representations supporting cognition and memory. Contrary to the common view that brain regions in the "what" and "where" streams distinctly process object and spatial cues, respectively, we found that both streams encode both object and spatial information but distinctly organize memories for objects and space. Specifically, perirhinal cortex and lateral entorhinal cortex represent objects and, within the object-specific representations, the locations where they occur. Conversely, medial entorhinal cortex represents relevant locations and, within those spatial representations, the objects that occupy them. Furthermore, these findings reach beyond simple notions of perirhinal cortex and lateral entorhinal cortex neurons as object detectors and MEC neurons as position detectors, and point to a more complex organization of memory representations within the medial temporal lobe system.