Putting names to faces:

Abstract

The ability to form associations between previously unrelated items of information, such as names and faces, is an essential aspect of episodic memory function. The neural substrate that determines success vs. failure in learning these associations remains to be elucidated. Using event-related functional MRI during the encoding of novel face-name associations, we found that successfully remembered face-name pairs showed significantly greater activation in the anterior hippocampal formation bilaterally and left inferior prefrontal cortex, compared to pairs that were forgotten. Functional connectivity analyses revealed significant correlated activity between the right and left hippocampus and neocortical regions during successful, but not attempted, encoding. These findings suggest that anterior regions of the hippocampal formation, in particular, are crucial for successful associative encoding and that the degree of coordination between hippocampal and neocortical activity may predict the likelihood of subsequent memory.

Introduction

The hippocampus and related structures in the medial temporal lobe are thought to be critical for episodic memory, but the precise function of the hippocampus in creating successful memories is not yet fully understood. Converging evidence from animal models of amnesia Squire and Zola-Morgan, 1991, Bunsey and Eichenbaum, 1995, Nakazawa et al., 2002, animal electrophysiological studies Wood et al., 1999, Suzuki and Eichenbaum, 2000, and amnestic patients Squire, 1992, Schacter and Church, 1995, Chalfonte et al., 1996, Ryan et al., 2000 suggests that one primary role of the hippocampal formation in episodic memory encoding is to form new associations between previously unrelated items of information Squire and Zola-Morgan, 1991, Eichenbaum et al., 1996. Recent functional imaging studies have provided additional support for this role of the hippocampal formation in associative memory processes Henke et al., 1997, Yonelinas et al., 2001, Zeineh et al., 2003. Many of these studies, as well as a meta-analysis by Schacter and Wagner (1999), have suggested that tasks that require relational or associative processing between stimuli are more likely to activate anterior regions of the hippocampal formation, as opposed to tasks that require processing of single stimuli, which tend to activate posterior hippocampal and parahippocampal regions Stern et al., 1996, Brewer et al., 1998, Wagner et al., 1998, Kirchhoff et al., 2000. The majority of associative memory studies published to date, however, have used block design paradigms, which did not allow for the separation of signal associated with individual stimuli, and thus could not adequately control for other contributing factors, such as whether the associations were successfully remembered.

Advances in functional neuroimaging paradigm design, specifically event-related fMRI designs (Dale and Buckner, 1997), have allowed the separation of specific stimuli based on whether the stimuli are subsequently remembered or forgotten. The “subsequent memory” fMRI studies published to date have primarily examined nonassociative encoding. These studies have reported that the degree of activation in parahippocampal and some posterior hippocampal regions, as well as prefrontal cortex, predicts the likelihood of subsequent memory for single stimuli, such as words or scenes Brewer et al., 1998, Wagner et al., 1998, Kirchhoff et al., 2000. It is unknown, however, whether activation in the same regions would also predict successful encoding of associations between unrelated items.

One particularly difficult associative encoding task encountered in daily life is learning the name associated with a new person one meets. Face-name association may be especially challenging because it requires the formation of a novel association between inherently unrelated items of information across the verbal and visual domains. We have previously reported that encoding novel face-name associations activates a set of brain regions, which include the hippocampus, fusiform, and prefrontal cortices (Sperling et al., 2001). We subsequently found that pharmacologically induced associative memory impairment selectively decreases activation in these same regions (Sperling et al., 2002). We undertook the current study, with an event-related face-name associative encoding paradigm with subsequent memory testing, to examine which brain regions are the most critical for successful encoding of novel face-name associations and whether the degree of coordination between regions predicts the likelihood of successful associative memory. We hypothesized that the hippocampal formation, specifically the anterior hippocampus, is critical for successful associative encoding, and that the degree of activation in the anterior hippocampus during encoding would predict success in subsequent associative memory performance.

It is unlikely that the hippocampus, or any other region, functions in isolation to form successful associations. If, in fact, the hippocampal formation is acting to “bind” together distributed representations of the information into a cohesive memory trace Squire and Zola-Morgan, 1991, Eichenbaum et al., 1996, it is likely that this process requires coordinated activity between the hippocampal formation and neocortical regions. Given the extensive afferent and efferent neocortical connections of the anterior hippocampal formation, this region seems ideally situated to integrate neural activity from widespread neocortical inputs. Thus, we hypothesized that successful encoding would demonstrate a high degree of correlation between activity in the hippocampal formation and neocortical regions involved in the process of forming face-name associations.