Abstract
Some theories of memory propose that the hippocampus integrates the individual items and events of experience within a contextual or spatial framework. The hippocampus receives cortical input from two major pathways: the medial entorhinal cortex (MEC) and the lateral entorhinal cortex (LEC). During exploration in an open field, the firing fields of MEC grid cells form a periodically repeating, triangular array. In contrast, LEC neurons show little spatial selectivity, and it has been proposed that the LEC may provide non-spatial input to the hippocampus. Here, we recorded MEC and LEC neurons while rats explored an open field that contained discrete objects. LEC cells fired selectively at locations relative to the objects, whereas MEC cells were weakly influenced by the objects. These results provide the first direct demonstration of a double dissociation between LEC and MEC inputs to the hippocampus under conditions of exploration typically used to study hippocampal place cells.
Highlights
The hippocampus is critically involved in episodic memory in humans (Scoville and Milner, 1957; O’Keefe and Nadel, 1978; Vargha-Khadem et al, 1997; Squire et al, 2004) and “episodiclike” memory in animals – memory that requires an integration of the what, where, and when components of a memory (Clayton and Dickinson, 1998; Eichenbaum and Fortin, 2005)
SELECTIVITY OF lateral entorhinal cortex (LEC) AND medial entorhinal cortex (MEC) NEURONS IN THE PRESENCE OF OBJECTS Multiple single units were recorded from the superficial layers of LEC and MEC while rats foraged for food reward in a 1.2-m × 1.5-m box in the presence of objects (Figures 2A,B)
The distributions of spatial information scores from 75 LEC and 49 MEC neurons were not statistically different under these conditions (Figure 3A; LEC median = 0.34 bits/spike; MEC median = 0.36 bits/spike; Wilcoxon rank sum test, p = 0.947). This result is in stark contrast to previous studies that showed that, in the absence of objects, MEC conveyed much more spatial information than LEC in both simple (Hargreaves et al, 2005) and complex (Yoganarasimha et al, 2010) environments
Summary
The hippocampus is critically involved in episodic memory in humans (Scoville and Milner, 1957; O’Keefe and Nadel, 1978; Vargha-Khadem et al, 1997; Squire et al, 2004) and “episodiclike” memory in animals – memory that requires an integration of the what, where, and when components of a memory (Clayton and Dickinson, 1998; Eichenbaum and Fortin, 2005). Non-spatial inputs influence the activity of hippocampal cells (Wiener et al, 1989; Hampson et al, 1999; Wood et al, 1999; Rivard et al, 2004; LenckSantini et al, 2005), often by modulating the underlying place field of the cell (O’Keefe, 1976; Moita et al, 2003; Komorowski et al, 2009; Manns and Eichenbaum, 2009). The creation of such context-specific, “item + place” conjunctive representations may be the key contribution of the hippocampus to episodic memory. The MEC is connected strongly to other regions that demonstrate similar spatial firing properties, such as the subiculum, presubiculum, parasubiculum, and retrosplenial cortex (Chen et al, 1994; Taube, 1995; Sharp, 1997; Cho and Sharp, 2001; Hargreaves et al, 2007; Lever et al, 2009; Boccara et al, 2010; Knierim and Hamilton, 2011)
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