Abstract
The rodent hippocampus represents different spatial environments distinctly via changes in the pattern of "place cell" firing. It remains unclear, though, how spatial remapping in rodents relates more generally to human memory. Here participants retrieved four virtual reality environments with repeating or novel landmarks and configurations during high-resolution functional magnetic resonance imaging (fMRI). Both neural decoding performance and neural pattern similarity measures revealed environment-specific hippocampal neural codes. Conversely, an interfering spatial environment did not elicit neural codes specific to that environment, with neural activity patterns instead resembling those of competing environments, an effect linked to lower retrieval performance. We find that orthogonalized neural patterns accompany successful disambiguation of spatial environments while erroneous reinstatement of competing patterns characterized interference errors. These results provide the first evidence for environment-specific neural codes in the human hippocampus, suggesting that pattern separation/completion mechanisms play an important role in how we successfully retrieve memories.
Highlights
Place neurons (e.g. “place cells”) in the rodent hippocampus preferentially fire in a particular spatial location (O’Keefe and Dostrovsky, 1971), the combination of which provide a neural code for that spatial environment (O’Keefe and Nadel, 1978; Wilson and McNaughton, 1993; Muller and Kubie, 1987)
We extend environment specific coding to the human hippocampus using voxel-pattern based analyses
Using a searchlight classifier approach, which naively identified medial temporal lobe regions carrying city specific information, we found a cluster of voxels in CA3/DG and CA1 whose patterns decoded specific cities during retrieval
Summary
Place neurons (e.g. “place cells”) in the rodent hippocampus preferentially fire in a particular spatial location (O’Keefe and Dostrovsky, 1971), the combination of which provide a neural code for that spatial environment (O’Keefe and Nadel, 1978; Wilson and McNaughton, 1993; Muller and Kubie, 1987). The collection of active place cells in an environment is thought to serve as a “cognitive map,” providing a spatial framework for both navigation and memory more generally (O’Keefe and Nadel, 1978; Redish, 1999; Buzsaki and Moser, 2013). A form of reorganization of hippocampal “maps” for different environments, is theorized to be a fundamental mechanism to navigation and memory more generally. Invasive recordings from the hippocampus have demonstrated place-coding neurons in single environments (Ekstrom et al, 2003; Jacobs et al, 2013; Miller et al, 2013). The human hippocampal formation is important to episodic memory more broadly (Spiers et al, 2001), with place cells activating during item recall (Miller et al, 2013) and several studies demonstrating the
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