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

Abstract

We used a continuous recognition procedure that included multiple presentations of test items, along with high-resolution functional magnetic resonance imaging (fMRI), to investigate the relationship between item novelty and recognition-related activity in the medial temporal lobe (MTL). In several regions of hippocampus and parahippocampal cortex, activity elicited by new items exceeded that for old items, whereas no MTL regions exhibited greater activity for old items. Critically, anatomically-distinct regions of MTL were engaged by item novelty in two different ways, as evidenced by statistically-dissociable profiles of activity. In bilateral medial hippocampus and left posterior parahippocampal cortex, activity followed a categorical profile in which it was greater for new than old items but did not differ further with additional presentations of old items. By contrast, effects in adjacent regions of right lateral hippocampus and left parahippocampal cortex were graded, whereby activity declined linearly with respect to each successive item presentation. These findings suggest that the relationship between hippocampal (and parahippocampal) activity and continuous psychological dimensions, such as item novelty, cannot be captured by a unitary function. Keywords novelty; familiarity; hippocampus; fMRI; high-resolution Consistent with human and animal lesion data implicating MTL in recognition memory (for reviews, see Brown & Aggleton, 2001;Eichenbaum et al., 2007;Squire et al., 2007), fMRI and intracranial (local field potential and single-neuron) recording studies have demonstrated that hippocampal activity is modulated by the study status of recognition test items (e.g., Grunwald et al., 1998;Heit et al., 1988; for a review of fMRI findings, see Henson, 2005). Among event-related fMRI studies employing separate study and test phases, it has occasionally been reported that correctly-recognized (old) items elicit greater hippocampal activity than correctly-rejected (new) items (e.g., Donaldson et al., 2001;Stark & Squire, 2001). 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 ...

Prefrontal direct current stimulation modulates resting EEG and event-related potentials in healthy subjects: A standardized low resolution tomography (sLORETA) study

“…Past studies have found direct neuronal activity between the medial prefrontal cortex and the hippocampus in rodents during spatial working memory tasks (Jones and Wilson, 2005;Siapas et al, 2005) and there is evidence for a fronto-parietal network (Laufs, 2008;van den Heuvel et al, 2009). One major effect of the parahippocampal activation might be the updating of the working memory processes, as this region is wellknown for its role in episodic memory (Johnson et al, 2008;Kumari et al, 2003;Ramsoy et al, 2009). Reciprocal connections between the dorsolateral prefrontal cortex (including the ACC) and the parahippocampal region are known (Goldman-Rakic et al, 1984).…”

Environmental novelty is associated with a selective increase in Fos expression in the output elements of the hippocampal formation and the perirhinal cortex

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Pre-experimental Familiarization Increases Hippocampal Activity for Both Targets and Lures in Recognition Memory: An fMRI Study

“…The memory strength account of hippocampal activity has been challenged recently by the results of fMRI studies using the continuous recognition procedure (e.g., Suzuki et al, 2011;Johnson, Muftuler, & Rugg, 2008). According to these authors, if hippocampal activity reflects strong memories rather than recollection of contextual details associated with an item, then it should demonstrate a positive correlation with item repetition during continuous recognition.…”

“…A number of authors have noted the likelihood of concurrent encoding of new and repeated items during continuous recognition (e.g., Johnson et al, 2008;Yassa & Stark, 2008;Brozinsky, Yonelinas, Kroll, & Ranganath, 2005). Johnson et al (2008) interpreted the reductions in hippocampal activity observed with successive item presentation in their study as reflecting "new item encoding" that "likely played a minimal (if any) role in supporting recognition judgments." To make judgments about serial order in continuous recognition (e.g., Suzuki et al, 2011), participants need to encode temporal information, a requirement that is absent during typical retrieval tasks in item recognition memory.…”