Predicting the integration of overlapping memories by decoding mnemonic processing states during learning

• Published in: NeuroImage (Orlando, Fla.) Vol. 124; no. Pt A; pp. 323 - 335
• Main Authors: Richter, Franziska R., Chanales, Avi J.H., Kuhl, Brice A.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.01.2016; Elsevier Limited
• Subjects: Adult; Behavior; Brain - physiology; Brain Mapping; Episodic memory; Female; Hippocampus; Hippocampus - physiology; Humans; Individuality; Integration; Learning - physiology; Magnetic Resonance Imaging; Male; Medial prefrontal cortex; Memory - physiology; Mental Recall - physiology; MVPA; Prefrontal Cortex - physiology; Reinstatement; Young Adult; Medial prefrontal cortex; Integration; Episodic memory; Reinstatement; MVPA; Hippocampus
• ISSN: 1053-8119; 1095-9572; 1095-9572
• DOI: 10.1016/j.neuroimage.2015.08.051

The hippocampal memory system is thought to alternate between two opposing processing states: encoding and retrieval. When present experience overlaps with past experience, this creates a potential tradeoff between encoding the present and retrieving the past. This tradeoff may be resolved by memory integration—that is, by forming a mnemonic representation that links present experience with overlapping past experience. Here, we used fMRI decoding analyses to predict when – and establish how – past and present experiences become integrated in memory. In an initial experiment, we alternately instructed subjects to adopt encoding, retrieval or integration states during overlapping learning. We then trained across-subject pattern classifiers to ‘read out’ the instructed processing states from fMRI activity patterns. We show that an integration state was clearly dissociable from encoding or retrieval states. Moreover, trial-by-trial fluctuations in decoded evidence for an integration state during learning reliably predicted behavioral expressions of successful memory integration. Strikingly, the decoding algorithm also successfully predicted specific instances of spontaneous memory integration in an entirely independent sample of subjects for whom processing state instructions were not administered. Finally, we show that medial prefrontal cortex and hippocampus differentially contribute to encoding, retrieval, and integration states: whereas hippocampus signals the tradeoff between encoding vs. retrieval states, medial prefrontal cortex actively represents past experience in relation to new learning. •Memory retrieval, encoding, and integration elicit distinct fMRI activity patterns.•By decoding memory states during learning, subsequent behavior can be predicted.•Decoded evidence for an integration state selectively predicts across-event memory.•Reactivation of older memories is related to, but dissociable from, integration.•Medial prefrontal cortex and hippocampus differentially signal memory states.