Human Hippocampal and Parahippocampal Activity during Visual Associative Recognition Memory for Spatial and Nonspatial Stimulus Configurations

Abstract

Evidence from animal studies points to the importance of the parahippocampal region (PHR) [including entorhinal, perirhinal, and parahippocampal (PHC) cortices] for recognition of visual stimuli. Recent findings in animals suggest that PHR may also be involved in visual associative recognition memory for configurations of stimuli. Thus far, however, such involvement has not been demonstrated in humans. In fact, it has been argued that associative recognition in humans is critically dependent on the hippocampal formation (HF). To better understand the division of function between HF and PHR during recognition memory in humans, we measured the activity of both areas in healthy young adults during an associative recognition memory task using functional magnetic resonance imaging. To more precisely characterize the nature of the associations that might be coded by the HF and PHR during recognition, subjects were required to learn and were later tested for associations based on either the spatial arrangements of two stimuli or the identity of two stimuli (a face and a tool). An area in the PHC was found to be more active for recognized old configurations than new configurations in both the spatial and identity conditions. The HF, on the other hand, was more active for recognition of new configurations than old configurations and also more active in the spatial than the identity condition. These data highlight the involvement of PHR in the long-term coding of associative relationships between stimuli and help to clarify the nature of its functional distinction from the HF.

Item familiarity and controlled associative retrieval in Alzheimer's disease: An fMRI study

“…The results of the PPI analyses revealed that, in healthy older participants (and not in AD+ patients), the inferior precuneus/PCC was functionally connected to the hippocampus, the inferior parietal cortex and the DLPFC specifically during successful controlled retrieval of the association. The hippocampus has been found to be engaged during retrieval of word pairs (Giovanello et al, 2004(Giovanello et al, , 2009Meltzer and Constable, 2005;Prince et al, 2005;Stark and Squire, 2001), face-name associations (Kirwan and Stark, 2004;Small et al, 2001), face-object associations (Ranganath et al, 2004a), face-spatial location associations (Duzel et al, 2003) and retrieval of an item with its learning context (Slotnick, 2010;Yonelinas et al, 2001). These findings support the idea that the hippocampus plays a role in the use of relational information in declarative memory (Preston et al, 2004).…”

Reduced Hippocampal Activation During Recall is Associated with Elevated FMR1 mRNA and Psychiatric Symptoms in Men with the Fragile X Premutation

“…FMRI recall task-Associative memory recall tasks done during functional MRI scanning have repeatedly been shown to result in robust activation of the hippocampal formation (e.g., Killgore 2000;Sperling et al 2001;Stark and Squire 2001;Yonelinas et al 2001;Duzel et al 2003;Sperling et al 2003;Giovanello et al 2004). These studies, and others, document both the role of the hippocampus in recall tasks and the ability of fMRI to measure the functioning of the hippocampus during such tasks.…”

Multiple repetitions reveal functionally and anatomically distinct patterns of hippocampal activity during continuous recognition memory

“…More frequently, enhanced hippocampal activity has been reported for recognition test items that are accompanied by either "remember" or accurate source memory judgments, relative to when items are designated with "know" responses or lack source information (e.g., Cansino et al, 2002;Eldridge et al, 2000;Johnson & Rugg, 2007;Wheeler & Buckner, 2004;Woodruff et al, 2005;Yonelinas et al, 2005 to imply that enhanced hippocampal activity is associated with the retrieval (recollection) of qualitative information about a study episode, rather than an acontextual sense of familiarity (Rugg & Yonelinas, 2003; but see Squire et al, 2007). Of significance, however, is that other fMRI studies of recognition memory have reported greater hippocampal activity for new compared to old items (e.g., Duzel et al, 2003;Rombouts et al, 2001;. Such findings have been interpreted as evidence that the hippocampus is sensitive to stimulus novelty, with elevated activity reflecting an allocation of processing resources toward the encoding of novel items (e.g., Duzel et al, 2003;Stark & Okado, 2003; also see Stern et al, 1996).…”

“…Of significance, however, is that other fMRI studies of recognition memory have reported greater hippocampal activity for new compared to old items (e.g., Duzel et al, 2003;Rombouts et al, 2001;. Such findings have been interpreted as evidence that the hippocampus is sensitive to stimulus novelty, with elevated activity reflecting an allocation of processing resources toward the encoding of novel items (e.g., Duzel et al, 2003;Stark & Okado, 2003; also see Stern et al, 1996). To further complicate matters, activity in the same hippocampal region can seemingly demonstrate enhancement to both recollected and new test items relative to items that are merely familiar, suggesting that recollection and encoding may be subserved by common or closely adjacent neuronal populations (Woodruff et al, 2005;Yonelinas et al, 2005).…”

“…Of significance, however, is that other fMRI studies of recognition memory have reported greater hippocampal activity for new compared to old items (e.g., Duzel et al, 2003;Rombouts et al, 2001;. Such findings have been interpreted as evidence that the hippocampus is sensitive to stimulus novelty, with elevated activity reflecting an allocation of processing resources toward the encoding of novel items (e.g., Duzel et al, 2003;Stark & Okado, 2003; also see Stern et al, 1996).…”