Recollection versus strength as the primary determinant of hippocampal engagement at retrieval

Abstract

We examined whether hippocampal activity in recognition relates to the strength of the memory or to recollective experience, a subject of considerable current debate. Participants studied word pairs and then made two successive recognition decisions on each item: first on the uncued target and then on the target presented with the studied cue word. We compared recollection and familiarity patterns of activation in fMRI for these decisions. Critically, our analyses attempted in two ways to equate perceived memory strength while varying the associative information available. First, activity for targets judged familiar before cueing was contrasted with activity for the same items in the second decision as a function of whether the targets converted to recollection or remained familiar when the context cues were provided. We found increased hippocampal activity following cueing only with recollective conversion. Second, we investigated whether hippocampal activity was modulated by the rated familiarity strength of cued items or whether it increased uniquely in recollection. Hippocampal activation was not modulated parametrically by familiarity strength and recollected items were associated with greater activity relative to highly familiar items. Together, our results support the notion that it is recollection of context, rather than memory strength, that underlies hippocampal engagement at retrieval.

Fig. 1.

Examples of test trials.

Fig. 2.

Pattern of hippocampal activation. (A) Lack of hippocampal engagement for items that remain familiar after cueing or for initial presentation (uncued) of cohorts of familiar items based on recognition decision following cueing (R vs. F). (B) Left hippocampal activation for items that become recollected following cueing. (C) Percent signal change in the peak hippocampal voxel from the contrast described in B as a function of item types [i.e., items that remain familiar (uFF, cFF), convert to recollection (uFR, cFR) or are judged as novel on uncued and cued trials (uNN, cNN)]. (D) Absence of hippocampal activity modulation with familiarity ratings on cued trials. (E) Bilateral hippocampal activity for recollected versus highly familiar cued items with exclusive masking for regions showing linear familiarity function (i.e., ratings 1 to 4). (F) Percent signal change in the peak hippocampal voxel from the contrast described in e as a function of recognition responses.