Charan Ranganath

Dissociable correlates of recollection and familiarity within the medial temporal lobes

Regions in the medial temporal lobes (MTL) have long been implicated in the formation of new memories for events, however, it is unclear whether different MTL subregions support different memory processes. Here, we used event-related functional magnetic resonance imaging (fMRI) to examine the degree to which two recognition memory processes-recollection and familiarity-were supported by different MTL subregions. Results showed that encoding activity in the rhinal cortex selectively predicted familiarity-based recognition, whereas, activity in the hippocampus and posterior parahippocampal cortex selectively predicted recollection. Collectively, these results support the view that different subregions within the MTL memory system implement unique encoding processes that differentially support familiarity and recollection.

Two cortical systems for memory-guided behaviour

Although the perirhinal cortex (PRC), parahippocampal cortex (PHC) and retrosplenial cortex (RSC) have an essential role in memory, the precise functions of these areas are poorly understood. Here, we review the anatomical and functional characteristics of these areas based on studies in humans, monkeys and rats. Our Review suggests that the PRC and PHC–RSC are core components of two separate large-scale cortical networks that are dissociable by neuroanatomy, susceptibility to disease and function. These networks not only support different types of memory but also appear to support different aspects of cognition.

Prefrontal Cortex and Long-Term Memory Encoding: An Integrative Review of Findings from Neuropsychology and Neuroimaging

Recent findings have led to a growing appreciation of the role of the lateral prefrontal cortex (PFC) in episodic long-term memory (LTM). Here, the authors will review results from neuropsychological and neuroimaging studies of humans and present a framework to explain how different regions of the PFC contribute to successful LTM formation. Central to this framework is the idea that different regions within the PFC implement different control processes that augment memory by enhancing or attenuating memory for certain aspects of a particular item or event. Evidence reviewed here suggests that ventrolateral regions of the PFC contribute to the ability to select goal-relevant item information, and that this processing strengthens the representation of goal-relevant features of items during LTM encoding. Dorsolateral regions of the PFC may contribute to the ability to organize multiple pieces of information in working memory, thereby enhancing memory for associations among items in LTM. Thus, dorsolateral and ventrolateral regions of the PFC may implement different control processes that support LTM formation in a complementary fashion. NEUROSCIENTIST 13(3):280—291, 2007.

Medial Temporal Lobe Activity Associated with Active Maintenance of Novel Information

Using event-related functional magnetic resonance imaging, we investigated the role of medial temporal regions during active maintenance of information over short delays or working memory. In experiment 1, we observed sustained bilateral hippocampal activation during maintenance of novel faces across a short delay period but not during face encoding or recognition. In contrast, we observed transient right parahippocampal activation during encoding and recognition but not during maintenance. We replicated these findings in experiment 2 and further determined that anterior hippocampal activation was greater during maintenance of novel than familiar faces. Our results reveal the importance of medial temporal lobe regions for the active maintenance of novel information in the absence of perceptual stimulation.

Reward expectation modulates feedback-related negativity and EEG spectra

The ability to evaluate outcomes of previous decisions is critical to adaptive decision-making. The feedback-related negativity (FRN) is an event-related potential (ERP) modulation that distinguishes losses from wins, but little is known about the effects of outcome probability on these ERP responses. Further, little is known about the frequency characteristics of feedback processing, for example, event-related oscillations and phase synchronizations. Here, we report an EEG experiment designed to address these issues. Subjects engaged in a probabilistic reinforcement learning task in which we manipulated, across blocks, the probability of winning and losing to each of two possible decision options. Behaviorally, all subjects quickly adapted their decision-making to maximize rewards. ERP analyses revealed that the probability of reward modulated neural responses to wins, but not to losses. This was seen both across blocks as well as within blocks, as learning progressed. Frequency decomposition via complex wavelets revealed that EEG responses to losses, compared to wins, were associated with enhanced power and phase coherence in the theta frequency band. As in the ERP analyses, power and phase coherence values following wins but not losses were modulated by reward probability. Some findings between ERP and frequency analyses diverged, suggesting that these analytic approaches provide complementary insights into neural processing. These findings suggest that the neural mechanisms of feedback processing may differ between wins and losses.

Prefrontal activity associated with working memory and episodic long-term memory

Many recent neuroimaging studies have highlighted the role of prefrontal regions in the sustained maintenance and manipulation of information over short delays, or working memory (WM). In addition, neuroimaging findings have highlighted the role of prefrontal regions in the formation and retrieval of memories for events, or episodic long-term memory (LTM), but it remains unclear whether these regions are distinct from those that support WM. We used event-related functional magnetic resonance imaging (fMRI) to identify patterns of prefrontal activity associated with encoding and recognition during WM and LTM tasks performed by the same subjects. Results showed that the same bilateral ventrolateral prefrontal regions (at or near Brodmanns Areas [BA] 6, 44, 45, and 47) and dorsolateral prefrontal regions (BA 9/46) were engaged during encoding and recognition within the context of WM and LTM tasks. In addition, a region situated in the left anterior middle frontal gyrus (BA 10/46) was engaged during the recognition phases of the WM and LTM tasks. These results support the view that the same prefrontal regions implement reflective processes that support both WM and LTM.

Inferior Temporal, Prefrontal, and Hippocampal Contributions to Visual Working Memory Maintenance and Associative Memory Retrieval

Higher order cognition depends on the ability to recall information from memory and hold it in mind to guide future behavior. To specify the neural mechanisms underlying these processes, we used event-related functional magnetic resonance imaging to compare brain activity during the performance of a visual associative memory task and a visual working memory task. Activity within category-selective subregions of inferior temporal cortex reflected the type of information that was actively maintained during both the associative memory and working memory tasks. In addition, activity in the anterior prefrontal cortex and hippocampus was specifically enhanced during associative memory retrieval. These data are consistent with the view that the active maintenance of visual information is supported by activation of object representations in inferior temporal cortex, but that goal-directed associative memory retrieval additionally depends on top-down signals from the anterior prefrontal cortex and medial temporal lobes.

Doubts about double dissociations between short- and long-term memory

Historically, psychologists and neuroscientists have distinguished between processes supporting memory for events across retention delays of several seconds (short-term memory, STM), and those supporting memory for events across longer retention delays of minutes or more (long-term memory, LTM). Dissociations reported in some neuropsychological studies have contributed to a popular view that there must be neurally distinct memory stores that differentially support STM and LTM. In this article, we review evidence from recent studies regarding dissociations between STM and LTM. We suggest that the evidence reveals problems with claims of selective STM or LTM impairments, which in turn questions whether theories of memory need to propose neurally distinct stores for short- and long-term retention. We consider alternative ways to explain the neural mechanisms of memory across different retention intervals.

A Unified Framework for the Functional Organization of the Medial Temporal Lobes and the Phenomenology of Episodic Memory

There is currently an intense debate about the nature of recognition memory and about the roles of medial temporal lobe subregions in recognition memory processes. At a larger level, this debate has been about whether it is appropriate to propose unified theories to explain memory at neural, functional, and phenomenological levels of analysis. Here, I review findings from physiology, functional imaging, and lesion studies in humans, monkeys, and rodents relevant to the roles of medial temporal lobe subregions in recognition memory, as well as in short‐term memory and perception. The results from these studies are consistent with the idea that there is functional heterogeneity in the medial temporal lobes, although the differences among medial temporal lobe subregions do not precisely correspond to different types of memory tasks, cognitive processes, or states of awareness. Instead, the evidence is consistent with the idea that medial temporal lobe subregions differ in terms of the kind of information they process and represent, and that these regions collectively support episodic memory by binding item and context information.

Dorsolateral Prefrontal Cortex Promotes Long-Term Memory Formation through Its Role in Working Memory Organization

Results from neuroimaging studies have shown that the dorsolateral prefrontal cortex (DLPFC) implements processes critical for organizing items in working memory (WM). Based on its role in WM, we hypothesized that the DLPFC should contribute to long-term memory (LTM) formation by strengthening associations among items that are organized in WM. We conducted an event-related functional magnetic resonance imaging (fMRI) study to test this hypothesis by investigating prefrontal activity during performance of two different WM tasks: on “rehearse” trials, participants actively maintained triplets of words during a brief delay, whereas on “reorder” trials, participants actively organized each triplet during the delay. After scanning, subjects performed an LTM test on words presented during both WM conditions. Behavioral results showed that WM processing in the reorder condition enhanced LTM by strengthening inter-item associations. fMRI results showed that DLPFC activity specifically during reorder trials was predictive of subsequent LTM. In contrast, activity in the posterior ventrolateral prefrontal cortex was predictive of LTM for words studied on both reorder and rehearse trials. These results support the view that the DLPFC contributes to LTM formation through its role in organization of information in WM.