We measured brain activity with fMRI during an incidental learning task and later collected confidence judgments during a post-scan recognition memory test. There were two main findings. First, in regions within what has been termed the default network, as well as in other regions, activity negatively correlated with subsequent memory strength. Second, in the medial temporal lobe, activity in both the hippocampus and perirhinal cortex positively correlated with the subsequent memory strength of remembered items.
The finding that activity in prefrontal cortex, inferior parietal cortex, and the posterior midline (which include regions of the default network) decreased with increasing subsequent memory strength () is consistent with previous fMRI reports. Thus, in earlier studies, activity in these structures for items that were subsequently forgotten was greater than for items that were subsequently remembered with high confidence (Daselaar et al., 2004
; Otten and Rugg, 2001b
). We have extended these results by showing that activity was negatively associated with subsequent memory across five levels of memory strength. The default network was originally identified as consisting of areas that were more active during resting states than during cognitive tasks of interest (Gusnard et al., 2001
; Gusnard and Raichle, 2001
; Raichle et al., 2001
; Shulman et al., 1997
). Interestingly, activity within these regions, as well as other regions, was subsequently linked to momentary lapses in attention and mind wandering (Mason et al., 2007
; Weissman et al., 2006
). Our finding of a negative association between subsequent memory strength and activity in default network structures as well as other regions, is consistent with these ideas. Participants may have varied from trial to trial in how attentive they were to the words being presented, and this variation affected how successful they later were at recognizing the words.
The second finding was that activity in hippocampus, perirhinal cortex, and temporopolar cortex increased with the subsequent memory strength of remembered items (i.e., items with memory strengths of 4, 5, or 6) (). Interestingly, even though activity in these structures did increase during learning in relation to the memory strength of subsequently remembered items, this activity was no higher than activity associated with subsequently forgotten items (i.e., items with memory strengths of 1&2 and 3). Indeed, the activity across all five memory strengths tended toward a U-shaped function (Supplemental Figure 2
We suggest that the U-shaped pattern of activity in these structures reflects variation in attention to the study words at the time of word presentation. Thus, on trials where the study words were later least well remembered (i.e., study words later given ratings of 1&2), the high activity in the medial temporal lobe may indicate that participants gave strong attention to, and subsequently would have had good memory for, mental activity unrelated to the word task, and/or that participants were retrieving task-irrelevant information from memory. Correspondingly, on trials where the study words were later best remembered (i.e., study words later given a rating of 6), high activity in the medial temporal lobe indicates that participants gave strong attention to, and subsequently had good memory for, the study words themselves.
These ideas lead one to expect that in regions where fMRI activity decreased with increasing subsequent memory strength (1 – 6) (presumably because of task-irrelevant mental activity), fMRI activity would be more strongly correlated with activity in the medial temporal lobe for subsequently forgotten items (memory strengths 1&2, 3) than for subsequently remembered items (memory strengths 4, 5, 6). And conversely, in regions where fMRI activity increased with subsequent memory strength (1 – 6) (presumably because of task-relevant mental activity), fMRI activity would be more strongly correlated with activity in the medial temporal lobe for subsequently remembered items (memory strengths 4, 5, 6) than for subsequently forgotten items (memory strengths 1&2, 3). The results of a functional connectivity analysis, correlating activity in the medial temporal lobe with regions exhibiting a negative correlation between activity and memory strengths 1 – 6 and also with regions exhibiting a positive correlation between activity and memory strengths 1 – 6, were consistent with this idea (Supplemental Figure 3
It is important to emphasize that the U-shaped pattern of findings would be expected to depend on the extent to which a study task demands full attention. In the present study, the task was relatively undemanding and even tedious (a pleasant/unpleasant judgment was made for each of 360 words), and participants could have made their responses early during the 2.5-second period when each word was presented. The rest of the time was available for mind wandering. In studies where the learning task is more demanding, or more time consuming, participants would be less likely to engage in task-irrelevant activity. In such circumstances, the relation between neural activity and subsequent memory performance can be expected to be different than what was observed here, and activity in the default network and other regions where activity correlated negatively with memory strength, might not be apparent during learning (Kirwan et al., submitted
; Ranganath et al., 2004
Our findings raise a caution about the interpretation of comparisons between activity related to subsequently remembered and subsequently forgotten items. At first glance, our finding that activity for subsequently remembered items was similar to the activity for subsequently forgotten items might suggest that medial temporal lobe activity does not predict subsequent memory. Yet, predictive activity was revealed when the analysis focused specifically on the relative memory strength of subsequently remembered items. Some previous studies also did not report a difference in medial temporal lobe activity between subsequently remembered items and subsequently forgotten items (Baker et al., 2001
; Buckner et al., 2001
; Otten and Rugg, 2001a
). One possible explanation for such an outcome is that, for items that were subsequently forgotten, there was substantial mnemonic activity unrelated to the task and that an analysis restricted to the relative strength of subsequently remembered items might have revealed predictive activity in the medial temporal lobe.
Another issue raised by our findings concerns possible functional differentiation within the medial temporal lobe. One suggestion is that the hippocampus and perirhinal cortex differ in their contributions to recognition memory decisions. Specifically, the hippocampus has been suggested to support recollection-based decisions, and the perirhinal cortex has been suggested to support familiarity-based decisions (Brown and Aggleton, 2001
; Eichenbaum et al., 2007
). Some fMRI studies have been taken in support of this distinction (e.g., Davachi et al., 2003
; Davachi and Wagner, 2002
; Kensinger and Schacter, 2006
; Ranganath et al., 2004
; Uncapher et al., 2006
; Uncapher and Rugg, 2005
). Yet, it has also been pointed out that the distinction between recollection and familiarity has frequently been confounded with memory strength and that hippocampal activity and perirhinal activity may be sensitive to different levels of memory strength rather than qualitatively different memory processes (Squire et al., 2007
We tested whether subsequent memory strength would correlate with activity in the hippocampus and perirhinal cortex, and we found that activity in both these structures exhibited a similar linear relationship with the subsequent memory strength of remembered items. Our study did not distinguish explicitly between the effects of memory strength and the effects of recollection and familiarity, so it remains possible that the perirhinal and hippocampal activity reflects familiarity-based and recollection-based decisions, respectively. Nevertheless, given that the relationship between activity and memory strength was similar in hippocampus and perirhinal cortex, it seems parsimonious to interpret the finding in each structure in similar ways. Thus, if increasing activity in hippocampus is thought to predict increasing numbers of recollection-based decisions, then it seems reasonable to suggest that increasing activity in perirhinal cortex also predicts recollection-based decisions. Conversely, if increasing activity in perirhinal cortex is thought to predict increasing numbers of familiarity-based decisions, then it seems reasonable to suggest that increasing activity in hippocampus also predicts familiarity-based decisions. We suggest that activity in both hippocampus and perirhinal cortex during learning predicts the subsequent memory strength of remembered items, regardless whether memory is based on recollection or familiarity. In any case, we suggest that the possible importance of memory strength in fMRI studies of recognition memory deserves consideration.
It is worth indicating how our study differs from an earlier study that also correlated activity during learning with subsequent memory (Ranganath et al., 2004
). We used a single orienting question (is the word pleasant or unpleasant?) and later tested memory strength for the items. In contrast, Ranganath et al. used one of two orienting questions on each trial and later tested memory strength for the items as well as source memory about information related to the orienting question. This difference was probably important. Our relatively tedious and undemanding study task likely resulted in task-irrelevant activity during study, whereas the more demanding task used by Ranganath et al. (2004)
likely encouraged participants to remain on task. We found that activity in the hippocampus and perirhinal cortex varied positively with memory strengths 4 – 6 (and across all memory strengths 1 – 6, activity conformed to a U-shape, see Discussion
above), while Ranganath and colleagues found that activity in the perirhinal cortex varied positively with memory strengths 1 – 5.
It is also worth mentioning that reaction times during study varied positively with subsequent memory strength. It is important to note that this pattern was qualitatively different from the U-shaped relationship between activity and subsequent memory strength in the medial temporal lobe. Thus, our findings in the medial temporal lobe cannot be attributed to the effect of reaction times during study.
In summary, activity during learning in regions known to be active during momentary lapses of attention and mind wandering was negatively correlated with subsequent memory strength. This finding shows that activity during learning might sometimes reflect processes unrelated to the task of interest. Further, in both hippocampus and perirhinal cortex, activity was positively correlated with the subsequent memory strength of remembered items. This finding does not point to a sharp distinction between these structures with respect to recollection and familiarity. At the same time, the data do not count against the idea that the functions of these structures are distinct in other important ways (Squire et al., 2007
; Suzuki and Eichenbaum, 2000