The Hippocampus Remains Activated over the Long Term for the Retrieval of Truly Episodic Memories

Abstract

The role of the hippocampus in declarative memory consolidation is a matter of intense debate. We investigated the neural substrates of memory retrieval for recent and remote information using functional magnetic resonance imaging (fMRI). 18 young, healthy participants learned a series of pictures. Then, during two fMRI recognition sessions, 3 days and 3 months later, they had to determine whether they recognized or not each picture using the “Remember/Know” procedure. Presentation of the same learned images at both delays allowed us to track the evolution of memories and distinguish consistently episodic memories from those that were initially episodic and then became familiar or semantic over time and were retrieved without any contextual detail. Hippocampal activation decreased over time for initially episodic, later semantic memories, but remained stable for consistently episodic ones, at least in its posterior part. For both types of memories, neocortical activations were observed at both delays, notably in the ventromedial prefrontal and anterior cingulate cortices. These activations may reflect a gradual reorganization of memory traces within neural networks. Our data indicate maintenance and strengthening of hippocampal and cortico-cortical connections in the consolidation and retrieval of episodic memories over time, in line with the Multiple Trace theory (Nadel and Moscovitch, 1997). At variance, memories becoming semantic over time consolidate through strengthening of cortico-cortical connections and progressive disengagement of the hippocampus.

Consolidation Promotes the Emergence of Representational Overlap in the Hippocampus and Medial Prefrontal Cortex

“…With respect to univariate activation, some work highlights that hippocampal activation during retrieval decreases with the age of the memory (Takashima et al, 2006, 2009; Watanabe et al, 2012). At the same time, other work demonstrates that hippocampal activation is related to remote retrieval for memories that retain distinct episodic elements (Viard et al, 2007; Harand et al, 2012; Sterpenich et al, 2009). Furthermore, neural patterns in the hippocampus have been shown to carry information about distinct episodes for both recent and remote autobiographical memories (Bonnici et al, 2012, 2013), suggesting that the hippocampus may continue to represent episodic features of memories as they are transformed over time, consistent with multiple trace theory (Nadel et al, 2000).…”

Memory Consolidation

“…In this design, participants learn similar materials at multiple different time points before scanning. A number of recent neuroimaging studies have used this approach (Takashima et al 2006(Takashima et al , 2009Yamashita et al 2009;Furman et al 2012;Harand et al 2012). For example, in one study (Takashima et al 2009), participants memorized two sets of face-location associations; one was studied 24 h before testing (remote memories) and the other studied 15 min before testing (recent memories).…”

Memory Retrieval in Mice and Men

“…One of the major debates in this regard (see also discussion of rodent studies above) pertains to whether only retrieval of recent memories is dependent on the hippocampus (e.g., Squire et al 2001;Squire and Bayley 2007;Bartsch et al 2011), or whether it is required for retrieval of vivid memories, regardless of memory age (Moscovitch et al 2005(Moscovitch et al , 2006Rosenbaum et al 2008;Dudai 2012;Bonnici et al 2013). Evidence from human neuroimaging studies suggests that both vividness and memory age affect different aspects of the hippocampal activity and its connectivity with the cortical retrieval network (e.g., Gilboa et al 2004;Piolino et al 2009;Viard et al 2010;Furman et al 2012;Harand et al 2012;Söderlund et al 2012). Two recent multivoxel pattern analysis studies directly probed how passage of time affects the representation in both hippocampal and cortical regions by decoding specific recent/ remote autobiographical memories (Bonnici et al 2012(Bonnici et al , 2013.…”