The human hippocampus contributes to both the recollection and familiarity components of recognition memory

Abstract

Despite a substantial body of work comprising theoretical modeling, the effects of medial temporal lobe lesions, and electrophysiological signal analysis, the role of the hippocampus in recognition memory remains controversial. In particular, it is not known whether the hippocampus exclusively supports recollection or both recollection and familiarity-the two latent cognitive processes theorized to underlie recognition memory. We studied recognition memory in a large group of patients undergoing intracranial electroencephalographic (iEEG) monitoring for epilepsy. By measuring high-frequency activity (HFA)-a signal associated with precise spatiotemporal properties-we show that hippocampal activity during recognition predicted recognition memory performance and tracked both recollection and familiarity. Through the lens of dual-process models, these results indicate that the hippocampus supports both the recollection and familiarity processes.hippocampus | recognition memory | recollection | familiarity | high-frequency activity R ecognition is one's ability to judge an item as previously encountered. Whereas it is well known that the hippocampus plays a crucial role in human recall memory, the role of the hippocampus in recognition memory remains surprisingly controversial (1-4). A number of studies have reported that bilateral hippocampal injury in humans causes impaired recall, whereas recognition remains intact (5). Others document the preservation of recognition in the setting of hippocampal lesioning in nonhuman primates (6) and rodents (7). On the other hand, a substantial literature describes combined recall and recognition deficits in a similarly injured group of patients (8) and animals (9, 10).Recognition is thought to rely on two processes: familiarity, wherein upon seeing a person's face, the rememberer has only a vague sense he has met the person before, and recollection, wherein the subject sees the person's face and vividly remembers details of the encounter (11,12). What role the hippocampus plays in supporting these processes remains the subject of considerable debate. Many memory researchers have proposed the discrepancy in the lesion data above derives from the fact that the hippocampus, which is well known to play a role in associative and relational memory (13), exclusively subserves recollection, whereas familiarity is supported by the extrahippocampal medial temporal lobe (MTL) (14). By this account, humans and animals are able to compensate for the loss of the hippocampus, and thus recollection, by relying on familiarity (15-18). A contrasting view holds that the hippocampus instead contributes to both recollection and familiarity, thus explaining why hippocampal damage is associated with severe impairment of both processes and consequently the overall recognition performance (4,8,19,20). Whether neural circuitry underlying familiarity and recollection lie within the hippocampus has also been extensively studied using functional MRI (fMRI) (21). Still, that many fMRI experiments show that ...

Recognition memory: Cellular evidence of a massive contribution of the LEC to familiarity and a lack of involvement of the hippocampal subfields CA1 and CA3

“…Furthermore, this time in agreement with both the dual and one process models of recognition memory, strong correlates for recollection judgements were found in the hippocampus (Fortin et al, ; Merkow, Burke, & Kahana, ; Reed and Squire, ; Sauvage et al, ; Vilberg and Rugg, ; Wixted and Squire, ). Especially, we report for the first time evidence for a stronger role for CA3 than CA1 in recollection.…”

“…Importantly, however, our findings extend these results by evaluating whether the reported lack of engagement of the hippocampus could have been a by-product of averaging CA1 and CA3's contribution to familiarity, which could have masked the engagement of one or the other area, as it has been reported to be the case recently for the retrieval of very remote memory (Lux, Atucha, Kitsukawa, & Sauvage, 2016). Furthermore, this time in agreement with both the dual and one process models of recognition memory, strong correlates for recollection judgements were found in the hippocampus (Fortin et al, 2004;Merkow, Burke, & Kahana, 2015;Reed and Squire, 1997;Sauvage et al, 2008;Vilberg and Rugg, 2012;Wixted and Squire, 2011). Especially, we report for the first time evidence for a stronger role for CA3 than CA1 in recollection.…”

A four-component model of age-related memory change.

“…First, because participants completed multiple sessions, each of which included over 300 recognition probes, the study is sufficiently powered to detect modest age differences. Second, whereas in most recognition tasks the lag between studying an item and being tested on that item (in terms of both the amount of time and the number of intervening items) is relatively short, in PEERS the lag is on the order of dozens of items and minutes, which will tend to increase difficulty and minimize any ceiling effects that could mask age differences (For other examples of the use of post-recall recognition see Lohnas & Kahana, 2013; Merkow, Burke, & Kahana, Submitted). …”

Differential generation of saccade, fixation and image onset event-related potentials in the human mesial temporal lobe

“…A variety of invasive and non-invasive electrophysiological recording techniques have been used to correlate MTL responses to underlying memory processes (Brewer et al, 1998;Jackson and Schacter, 2004;Long et al, 2014;McCormick et al, 2015;Merkow et al, 2015;Sederberg et al, 2006). Intracranial electroencephalography (iEEG), unlike other recording modalities, provides access to neural activity with high spatial and temporal resolution allowing investigation of electrophysiological activity in deep structures associated with memory processes, at 'fast' time scales (Johnson and Knight, 2015).…”