Abstract
The hippocampus is an essential hub for episodic memory processing. However, how human hippocampal single neurons code multi-element associations remains unknown. Some argue that each hippocampal neuron codes for an invariant element within an episode. Instead, others have proposed that hippocampal neurons bind together all elements present in a discrete episodic memory. Here, we provide evidence for the latter. We show that individual neurons, which we term Episode Specific Neurons (ESNs), code discrete episodic memories using either a rate code or a temporal firing code. We find evidence for these neurons exclusively in the hippocampus. Importantly, these ESNs do not reflect the coding of a particular element in the episode (i.e., concept or time). Instead, they code for the conjunction of the different elements that make up the episode.
One-Sentence Summary Individual neurons in the hippocampus code for discrete episodic memories.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
1. We have continuously collected new data and reviewed electrode localizations, resulting in 216 instead of 86 hippocampal neurons for the second experiment. This substantially increases the statistical power of the second experiment. 2. We show that our core results are robust against variations in how exactly the reinstatement measure is calculated (such as normalizing the product of the standardized encoding and retrieval firing rate by their absolute difference [i.e., (ExR)/|E-R|], or by summing up the standardized firing rates [E+R]). 3. We have clarified that we find evidence for a conjunctive memory code in the hippocampus but that this does not exclude Concept Neurons from playing a relevant role in episodic memory processing. 4. We still find a significant number of Episode Specific Neurons (ESNs) when drastically lowering the threshold of what constitutes a Concept Neuron, which further supports the conclusion that ESNs are highly unlikely to be Concept Neurons. 5. We show that the parahippocampal cortex does not have a significant number of ESNs. 6. Finally, we show evidence for neurons which show episode specific reinstatement of a temporal code (as opposed to a rate code). We term these neurons temporal ESNs (tESNs). We also like to clarify that we have discovered a minor error in our previous calculation of event trigger timings and inter spike intervals, which we have now corrected. Importantly, this error had no bearings on the main findings. However, the analysis where we find neurons that reinstate at least one trial with two face associates and at least one trial with two place associate images is no longer feasible as too few trials reinstate two or more trials. In the past, this analysis has only led to confusion and the visual tuning task fulfils the role of ruling out Concept Neurons much more effectively. We, therefore, decided to remove this analysis from the paper.