The medial temporal lobe and recognition memory

Abstract

The ability to recognize a previously experienced stimulus is supported by two processes: recollection of the stimulus in the context of other information associated with the experience, and a sense of familiarity with the features of the stimulus. Although familiarity and recollection are functionally distinct, there is considerable debate about how these kinds of memory are supported by regions in the medial temporal lobes (MTL). Here, we review evidence for the distinction between recollection and familiarity and then consider the evidence regarding the neural mechanisms of these processes. Evidence from neuropsychological, neuroimaging, and neurophysiological studies of humans, monkeys, and rats indicates that different subregions of the MTL make distinct contributions to recollection and familiarity. The data suggest that the hippocampus is critical for recollection but not familiarity. The parahippocampal cortex also contributes to recollection, possibly via the representation and retrieval of contextual (especially spatial) information, whereas perirhinal cortex contributes to and is necessary for familiarity-based recognition. The findings are consistent with an anatomically guided hypothesis about the functional organization of the MTL and suggest mechanisms by which the anatomical components of the MTL interact to support the phenomenology of recollection and familiarity.

Figure 1

Receiver operating characteristic (ROC) analyses of recognition memory. Left panels plot probability of hits versus false alarms (FA). Right panels plot the same data normalized (z-Hit and zFA). Chance performance is represented by the diagonal in each panel. (a) ROCs for strongly encoded items (studied twice) and weakly encoded items (studied once) from Egan (1958, experiment 1). (b) ROCs for items studied under deep encoding conditions (i.e., rate the pleasantness of the word) and shallow encoding conditions (i.e., count the number of syllables in the word) (from Yonelinas et al. 1996). (c) ROCs in which subjects studied verbal items spoken once or twice by a male or female speaker. At test they were visually presented with the words and were to indicate how confident they were that the item had been presented earlier and whether it was presented by the male or female source (from Yonelinas 1997, experiment 3).

Figure 2

ERPs from Rugg et al. (2002) illustrating a mid-frontal ERP modulation (left panel ) associated with familiarity and a parietally distributed (right panel ) related to recollection. In this study, the familiarity effect was evident for deeply and shallowly encoding items, whereas the recollection effect was most pronounced for the deeply encoding items.

Figure 3

Functional organization of the MTL system. Neocortical input regarding the object features (“what”) converges in the perirhinal cortex (PRC) and lateral entorhinal area (LEA), whereas details about the location (“where”) of objects converge in the parahippocampal cortex (PHC) and medial entorhinal area (MEA). These streams converge in the hippocampus, which represents items in the context in which they were experienced. Reverse projections follow the same pathways back to the parahippocampal and neocortical regions. Back projections to the PHC-MEA may support recall or context, whereas back projections to the PHC-LEA may support recall of item associations.

Figure 4

Measures of recollection and familiarity in amnesic patients with expected hippocampal damage (Yonelinas et al. 2002) and in rats with selective hippocampal lesions (Fortin et al. 2004). (a) ROCs for the amnesic patients are lower and more symmetrical than those of the controls. (b) ROC measures of recollection (R) and familiarity (F) indicate that recollection, but not familiarity, is reduced in the amnesics (H) compared with controls (C). (c) R and F estimates derived from a separate remember/know experiment also indicate that recollection was disrupted in the amnesic patients whereas familiarity was unaffected. (d ) R and F estimates derived using structural equation modeling (SEM) in a larger group of amnesic patients showed that increases in hypoxic severity led to a decrease in recollection but left familiarity unaffected. (e) ROCs for rats with hippocampal lesions are lower and more symmetrical than are those of control animals. ( f ) ROC measures indicated that familiarity is unaffected by hippocampal lesions.

Figure 5

Double dissociations between hippocampal and anterior parahippocampal activity. (a) Data from Ranganath et al. (2003). Participants were scanned during encoding of words shown in red or green and subsequently were asked to rate their confidence regarding whether each word was shown in the scanner and to decide whether the word was shown in red or green during the study phase. Activity in the left anterior parahippocampal gyrus (PHG; left) during encoding was correlated with subsequent confidence ratings, suggesting a role in familiarity-based recognition. Encoding activity in the right hippocampus was correlated with accuracy on the relational-recognition test, suggesting a role in recollection. (b) Comparison of the magnitudes of subsequent familiarity (left) and recollection (right) effects in the left anterior PHG and right hippocampal regions. The comparison revealed a reliable double dissociation between the two regions. (c) Data from Montaldi et al. (2006). Participants studied scenes and were scanned during recognition testing. For each item that was judged old, participants were to indicate if it was recollected (R) or to rate its familiarity on a 1–3 scale (F1–F3). Activation is separately plotted for correctly rejected new items (CR) and for old items that elicited new (M), F1–F3, and R responses. Activation in bilateral anterior parahippocampal regions (left) monotonically decreased with increasing confidence and did not differ between highly familiar items (F3) and items that were recollected. In contrast, activation in bilateral hippocampal regions (right) was increased specifically for recollected items, as compared with nonrecollected items, and was insensitive to gradations in familiarity strength.

Figure 6

Performance of normal monkeys (N) and monkeys with lesions of the hippocampus (H), perirhinal cortex (PRC), or parahippocampal cortex (PHC) on two recognition memory tasks. (a) In the delayed nonmatch to sample task, animals must remember a sample object over a delay period, then select against it (nonmatch) in the choice phase. Normal monkeys show robust recognition over long memory delays, as do animals with hippocampal or PHC damage. PRC lesions result in rapid decay of memory. (b)In the visual paired comparison task, animals remember a once-viewed scene and later prefer to view a novel scene. Normal monkeys also show robust recognition over long delays in this task, but memory in animals with H, PHC, or PRC lesions rapidly decays (data from Nemanic et al. 2004).