Abstract
Episodic memory requires information about objects to be integrated into a spatial framework. Place cells in the hippocampus encode spatial representations of objects that could be generated through signaling from the entorhinal cortex. Projections from lateral (LEC) and medial entorhinal cortex (MEC) to the hippocampus terminate in distal and proximal CA1, respectively. We recorded place cells in distal and proximal CA1 as rats explored an environment that contained objects. Place cells in distal CA1 demonstrated higher measures of spatial tuning, stability, and closer proximity of place fields to objects. Furthermore, remapping to object displacement was modulated by place field proximity to objects in distal, but not proximal CA1. Finally, representations of previous object locations were closer to those locations in distal CA1 than proximal CA1. Our data suggest that in cue-rich environments, LEC inputs to the hippocampus support spatial representations with higher spatial tuning, closer proximity to objects, and greater stability than those receiving inputs from MEC. This is consistent with functional segregation in the entorhinal-hippocampal circuits underlying object-place memory.
Highlights
Episodic memory is memory for past personal experiences
We recorded from place cells in distal and proximal CA1 (1,415 place fields across all trials [distal n = 1,158, proximal n = 257] from 249 units [distal n = 208, 5 animals; proximal n = 41, 3 animals]) as rats foraged in a square environment containing two different objects (Figure 1a,b; Table S1)
We first asked whether the increased spatial tuning in proximal CA1 relative to distal CA1 reported in empty environments (Henriksen et al, 2010) persists in an environment that contains objects (Figure 1c)
Summary
Episodic memory is memory for past personal experiences. Models of the neural circuits underlying episodic memory suggest that spatial input from medial entorhinal cortex (MEC) is combined with nonspatial item information from lateral entorhinal cortex (LEC) to form context-dependent memories within the hippocampus (Ainge et al, 2012; Ainge, Tamosiunaite, et al, 2007; Ainge, van der Meer, et al, 2007; Eichenbaum et al, 2012; Ferbinteanu & Shapiro, 2003; Hayman & Jeffery, 2008; Leutgeb et al, 2005; Manns & Eichenbaum, 2006). Object-location memory deficits are more pronounced in both MEC and LEC lesioned animals in more complex tasks that require memory for multiple object-location associations (Kuruvilla & Ainge, 2017; Rodo et al, 2017) These observations demonstrate that the entorhinal–hippocampal network is critical for associating objects with the locations in which they were experienced, and suggests functionally segregated subsystems within the network that integrate object and location information in different ways. This is consistent with the suggestion that different types of responses to objects are maintained in functionally separate entorhinal–hippocampal circuits Further support for this suggestion comes from studies showing distal CA1 is preferentially recruited to process information about objects (Hartzell et al, 2013; Ito & Schuman, 2012; Nakamura et al, 2013; Nakazawa et al, 2016), and place cells in proximal CA1 demonstrate higher spatial tuning and stability than place cells in distal CA1 in empty environments (Henriksen et al, 2010). Place fields generated in distal CA1 were closer to objects and locations where objects were previously experienced
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