Voluntary Explicit versus Involuntary Conceptual Memory Are Associated with Dissociable fMRI Responses in Hippocampus, Amygdala, and Parietal Cortex for Emotional and Neutral Word Pairs Cristina Ramponi 1 , Philip J. Barnard 1 , Ferath Kherif 2,3 , and Richard N. Henson 1 Abstract ■ Although functional neuroimaging studies have supported the distinction between explicit and implicit forms of memory, few have matched explicit and implicit tests closely, and most of these tested perceptual rather than conceptual implicit mem- ory. We compared event-related fMRI responses during an inten- tional test, in which a group of participants used a cue word to recall its associate from a prior study phase, with those in an in- cidental test, in which a different group of participants used the same cue to produce the first associate that came to mind. Both semantic relative to phonemic processing at study, and emo- tional relative to neutral word pairs, increased target completions in the intentional test, but not in the incidental test, suggesting that behavioral performance in the incidental test was not con- taminated by voluntary explicit retrieval. We isolated the neural correlates of successful retrieval by contrasting fMRI responses to studied versus unstudied cues for which the equivalent “tar- get” associate was produced. By comparing the difference in this repetition-related contrast across the intentional and incidental tests, we could identify the correlates of voluntary explicit re- trieval. This contrast revealed increased bilateral hippocampal responses in the intentional test, but decreased hippocampal responses in the incidental test. A similar pattern in the bilateral amygdale was further modulated by the emotionality of the word pairs, although surprisingly only in the incidental test. Parietal re- gions, however, showed increased repetition-related responses in both tests. These results suggest that the neural correlates of successful voluntary explicit memory differ in directionality, even if not in location, from the neural correlates of successful involuntary implicit (or explicit) memory, even when the inciden- tal test taps conceptual processes. ■ INTRODUCTION Human memory is multifaceted, and considerable effort has been expended in uncovering the psychological pro- cesses and brain structures that support these different facets. Two expressions of memory that have often been con- trasted are explicit and implicit memory (Graf & Schacter, 1985). Explicit memories are memories that are consciously retrieved, usually implying volition in retrieval and often bringing to mind a specific episode, whereas implicit mem- ories can influence our behavior in the absence of conscious associations with the past. Although originally intended as phenomenological labels, the terms explicit and implicit memory have also been assumed to map onto distinct neural systems (Schacter & Tulving, 1994; Schacter, 1987). Func- tional neuroimaging studies have since been used to inves- tigate this claim, although often by examining each type of memory in isolation. In order to identify more precisely the brain structures that are specific to voluntary explicit memory (and those structures that are shared), it is neces- sary to study explicit and implicit memory in conjunction (Voss & Paller, 2008). In particular, it is essential to com- pare memory tests that are matched in all respects (such as the type of memoranda, type of retrieval cue, etc.), except for their relative reliance on voluntary explicit memory. One paradigm that has proved useful in this respect is the cued-recall/free-completion paradigm. In the “word- stem” version of this paradigm, participants are exposed to a list of words (the “study phase”), and then perform one of two tests: (1) in the intentional test, they are given the first few letters of a word (“word-stem”), and asked to recall a word from the study phase that completes that stem; (2) in the incidental test, they are given the same type of cue (a word-stem) but complete it with the first word that comes to mind (i.e., no reference is made to the previous study phase). 1 Because everything is matched except the instructions to participants, this pair of tests satisfies the “retrieval intentionality” criterion (Schacter, Bowers, & Booker, 1989). Behavioral dissociations between these two tests have been found as a function of other variables, such as the match versus mismatch in the visual/ 1 MRC Cognition & Brain Sciences Unit, Cambridge, UK, 2 Univer- sity College London, UK, 3 Université de Lausanne, Switzerland © 2011 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 23:8, pp. 1935–1951