CA1 reinstatement and novelty response independently support recognition memory

Abstract

One of the central tensions in memory research is whether consistency or differentiation across events is beneficial for remembering. While theoretical models posit that the hippocampal subfield CA1 subserves both types of computations, it remains unclear how it can simultaneously express both in service of recognition memory. Here, we contrasted the two prominent functions of CA1: reinstatement (consistency) and novelty processing (differentiation) to address this gap. To this end, we analysed the Natural Scenes Dataset featuring eight participants who completed a continuous recognition memory task spanning 41 separate days with 213,000 trials in total. We calculated reinstatement and novelty indices for each image and then examined the degree to which these reflected successful memory encoding. We found that CA1 showed evidence for encoding-related reinstatement as well as for novelty processing even after controlling for each other. Reinstatement was specific to retrieving the initial representation during the first retrieval attempt and did not extend to other forms of reinstatement. Exploratory analyses additionally identified reinstatement in CA3, which exhibited different response profiles compared to CA1. Our work thus highlights that computations of consistency as well as differentiation can be orthogonal signals contributing independently to memory success and can simultaneously co-exist within the same region of the hippocampus. Significance statement One of the central tensions in memory research is whether consistency, measured by reinstatement or differentiation, measured by activation difference across repeated events benefits remembering. While both have been associated with the hippocampal subfield CA1, it remains unclear how they can simultaneously support recognition memory. Here, we leveraged 7T precision fMRI in a densely-sampled continuous recognition task and demonstrated that reinstatement of the first representation and the novelty response co-exist in CA1. Critically, both independently predict subsequent memory success, suggesting computations of consistency and differentiation are orthogonal signals. We additionally identified subfield CA3 in which reinstatement, but not novelty, is predictive of memory, further highlighting the unique role of CA1 as a convergent hub of multiple hippocampal functions.