Declarative memory is supported by distributed brain networks in which the medial-temporal lobes (MTLs) and pFC serve as important hubs. Identifying the unique and shared contributions of these regions to successful memory performance is an active area of research, and a growing literature suggests that these structures often work together to support declarative memory. Here, we present data from a context-dependent relational memory task in which participants learned that individuals belonged in a single room in each of two buildings. Room assignment was consistent with an underlying contextual rule structure in which male and female participants were assigned to opposite sides of a building and the side assignment switched between buildings. In two experiments, neural correlates of performance on this task were evaluated using multiple neuroimaging tools: diffusion tensor imaging (Experiment 1), magnetic resonance elastography (Experiment 1), and functional MRI (Experiment 2). Structural and functional data from each individual modality provided complementary and consistent evidence that the hippocampus and the adjacent white matter tract (i.e., fornix) supported relational memory, whereas the ventromedial pFC/OFC (vmPFC/OFC) and the white matter tract connecting vmPFC/OFC to MTL (i.e., uncinate fasciculus) supported memory-guided rule use. Together, these data suggest that MTL and pFC structures differentially contribute to and support contextually guided relational memory.

Memory can profoundly influence new learning, presumably because memory optimizes exploration of to-be-learned material. Although hippocampus and frontoparietal networks have been implicated in memory-guided exploration, their specific and interactive roles have not been identified. We examined eye movements during fMRI scanning to identify neural correlates of the influences of memory retrieval on exploration and learning. After retrieval of one object in a multiobject array, viewing was strategically directed away from the retrieved object toward nonretrieved objects, such that exploration was directed toward to-be-learned content. Retrieved objects later served as optimal reminder cues, indicating that exploration caused memory to become structured around the retrieved content. Hippocampal activity was associated with memory retrieval, whereas frontoparietal activity varied with strategic viewing patterns deployed after retrieval, thus providing spatiotemporal dissociation of memory retrieval from memory-guided learning strategies. Time-lagged fMRI connectivity analyses indicated that hippocampal activity predicted frontoparietal activity to a greater extent for a condition in which retrieval guided exploration occurred than for a passive control condition in which exploration was not influenced by retrieval. This demonstrates network-level interaction effects specific to influences of memory on strategic exploration. These findings show how memory guides behavior during learning and demonstrate distinct yet interactive hippocampal–frontoparietal roles in implementing strategic exploration behaviors that determine the fate of evolving memory representations.

Familiarity and recollection are qualitatively different explicit-memory phenomena evident during recognition testing. Investigations of the neurocognitive substrates of familiarity and recollection, however, have typically disregarded implicit-memory processes likely to be engaged during recognition tests. We reasoned that differential neural responses to old and new items in a recognition test may reflect either explicit or implicit memory. Putative neural correlates of familiarity in prior experiments, for example, may actually reflect contamination by implicit memory. In two experiments, we used obscure words that subjects could not formally define to tease apart electrophysiological correlates of familiarity and one form of implicit memory, conceptual priming. In Experiment 1, conceptual priming was observed for words only if they elicited meaningful associations. In Experiment 2, two distinct neural signals were observed in conjunction with familiarity-based recognition: late posterior potentials for words that both did and did not elicit meaningful associations and FN400 potentials only for the former. Given that symbolic meaning is a prerequisite for conceptual priming, the combined results specifically link late posterior potentials and FN400 potentials with familiarity and conceptual priming, respectively. These findings contradict previous interpretations of FN400 potentials as generic signals of familiarity and show that repeated stimuli in recognition tests can engender facilitated processing of conceptual information in addition to retrieval processing that leads to the awareness of memory retrieval. The different characteristics of the electrical markers of these two types of process further underscore the biological validity of the distinction between implicit memory and explicit memory.

Stenberg et al. argued that FN400 brain potentials index familiarity rather than conceptual priming. Their data from a test of name recognition showed that both familiarity and FN400s were influenced by frequency but not fame, whereas separate behavioral measures of priming were influenced by fame but not frequency. However, this apparent dissociation was gravely weakened by confounds in task demands and inadequate behavioral measures of priming. Although Stenberg et al. failed to provide evidence suitable for disentangling neural correlates of familiarity from those of conceptual priming, an analysis of their report can be used to highlight difficulties that remain to be surmounted to understand recognition and the neural events that signal distinct memory functions engaged during recognition.