Maureen Ritchey

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.

Neural correlates of emotional processing in depression: Changes with cognitive behavioral therapy and predictors of treatment response

Major depressive disorder (MDD) is characterized by the presence of disturbances in emotional processing. However, the neural correlates of these alterations, and how they may be affected by therapeutic interventions, remain unclear. The present study addressed these issues in a preliminary investigation using functional magnetic resonance imaging (fMRI) to examine neural responses to positive, negative, and neutral pictures in unmedicated MDD patients (N = 22) versus controls (N = 14). After this initial scan, MDD patients were treated with cognitive behavioral therapy (CBT) and scanned again after treatment. Within regions that showed pre-treatment differences between patients and controls, we tested the association between pre-treatment activity and subsequent treatment response as well as activity changes from pre- to post-treatment. This study yielded three main findings. First, prior to treatment and relative to controls, patients exhibited overall reduced activity in the ventromedial prefrontal cortex (PFC), diminished discrimination between emotional and neutral items in the amygdala, caudate, and hippocampus, and enhanced responses to negative versus positive stimuli in the left anterior temporal lobe (ATL) and right dorsolateral PFC. Second, CBT-related symptom improvement in MDD patients was predicted by increased activity at baseline in ventromedial PFC as well as the valence effects in the ATL and dorsolateral PFC. Third, from pre- to post-treatment, MDD patients exhibited overall increases in ventromedial PFC activation, enhanced arousal responses in the amygdala, caudate, and hippocampus, and a reversal of valence effects in the ATL. The study was limited by the relatively small sample that was able to complete both scan sessions, as well as an inability to determine the influence of comorbid disorders within the current sample. Nevertheless, components of the neural networks corresponding to emotion processing disturbances in MDD appear to resolve following treatment and are predictive of treatment response, possibly reflecting improvements in emotion regulation processes in response to CBT.

fMRI studies of successful emotional memory encoding: a quantitative meta-analysis

Over the past decade, fMRI techniques have been increasingly used to interrogate the neural correlates of successful emotional memory encoding. These investigations have typically aimed to either characterize the contributions of the amygdala and medial temporal lobe (MTL) memory system, replicating results in animals, or delineate the neural correlates of specific behavioral phenomena. It has remained difficult, however, to synthesize these findings into a systems neuroscience account of how networks across the whole-brain support the enhancing effects of emotion on memory encoding. To this end, the present study employed a meta-analytic approach using activation likelihood estimates to assess the anatomical specificity and reliability of event-related fMRI activations related to successful memory encoding for emotional versus neutral information. The meta-analysis revealed consistent clusters within bilateral amygdala, anterior hippocampus, anterior and posterior parahippocampal gyrus, the ventral visual stream, left lateral prefrontal cortex and right ventral parietal cortex. The results within the amygdala and MTL support a wealth of findings from the animal literature linking these regions to arousal-mediated memory effects. The consistency of findings in cortical targets, including the visual, prefrontal, and parietal cortices, underscores the importance of generating hypotheses regarding their participation in emotional memory formation. In particular, we propose that the amygdala interacts with these structures to promote enhancements in perceptual processing, semantic elaboration, and attention, which serve to benefit subsequent memory for emotional material. These findings may motivate future research on emotional modulation of widespread neural systems and the implications of this modulation for cognition.

Role of Amygdala Connectivity in the Persistence of Emotional Memories Over Time: An Event-Related fMRI Investigation

According to the consolidation hypothesis, enhanced memory for emotional information reflects the modulatory effect of the amygdala on the medial temporal lobe (MTL) memory system during consolidation. Although there is evidence that amygdala-MTL connectivity enhances memory for emotional stimuli, it remains unclear whether this enhancement increases over time, as consolidation processes unfold. To investigate this, we used functional magnetic resonance imaging to measure encoding activity predicting memory for emotionally negative and neutral pictures after short (20-min) versus long (1-week) delays. Memory measures distinguished between vivid remembering (recollection) and feelings of knowing (familiarity). Consistent with the consolidation hypothesis, the persistence of recollection over time (long divided by short) was greater for emotional than neutral pictures. Activity in the amygdala predicted subsequent memory to a greater extent for emotional than neutral pictures. Although this advantage did not vary with delay, the contribution of amygdala-MTL connectivity to subsequent memory for emotional items increased over time. Moreover, both this increase in connectivity and amygdala activity itself were correlated with individual differences in recollection persistence for emotional but not neutral pictures. These results suggest that the amygdala and its connectivity with the MTL are critical to sustaining emotional memories over time, consistent with the consolidation hypothesis.

Dissociable effects of conscious emotion regulation strategies on explicit and implicit memory.

The authors manipulated emotion regulation strategies at encoding and administered explicit and implicit memory tests. In Experiment 1, participants used reappraisal to enhance and decrease the personal relevance of unpleasant and neutral pictures. In Experiment 2, decrease cues were replaced with suppress cues that directed participants to inhibit emotion-expressive behavior. Across experiments, using reappraisal to enhance the personal relevance of pictures improved free recall. By contrast, attempting to suppress emotional displays tended to impair recall, especially compared to the enhance condition. Using reappraisal to decrease the personal relevance of pictures had different effects depending on picture type. Paired with unpleasant pictures, the decrease cue tended to improve recall. Paired with neutral stimuli, the decrease cue tended to impair recall. Emotion regulation did not affect perceptual priming. Results highlight dissociable effects of emotion regulation on explicit and implicit memory, as well as dissociations between regulation strategies with respect to explicit memory.

Neural Similarity Between Encoding and Retrieval is Related to Memory Via Hippocampal Interactions

A fundamental principle in memory research is that memory is a function of the similarity between encoding and retrieval operations. Consistent with this principle, many neurobiological models of declarative memory assume that memory traces are stored in cortical regions, and the hippocampus facilitates the reactivation of these traces during retrieval. The present investigation tested the novel prediction that encoding-retrieval similarity can be observed and related to memory at the level of individual items. Multivariate representational similarity analysis was applied to functional magnetic resonance imaging data collected during encoding and retrieval of emotional and neutral scenes. Memory success tracked fluctuations in encoding-retrieval similarity across frontal and posterior cortices. Importantly, memory effects in posterior regions reflected increased similarity between item-specific representations during successful recognition. Mediation analyses revealed that the hippocampus mediated the link between cortical similarity and memory success, providing crucial evidence for hippocampal-cortical interactions during retrieval. Finally, because emotional arousal is known to modulate both perceptual and memory processes, similarity effects were compared for emotional and neutral scenes. Emotional arousal was associated with enhanced similarity between encoding and retrieval patterns. These findings speak to the promise of pattern similarity measures for evaluating memory representations and hippocampal-cortical interactions.

The slow forgetting of emotional episodic memories: an emotional binding account

Emotional events are remembered better than neutral events, and this emotion advantage becomes particularly pronounced over time. The time-dependent effects of emotion impact upon recollection rather than on familiarity-based recognition, and they influence the recollection of item-specific details rather than contextual details. Moreover, the amygdala, but not the hippocampus, is crucial for producing these effects. Time-dependent effects of emotion have been attributed to an emotional consolidation process whereby the amygdala gradually facilitates the storage of emotional memories by other medial temporal lobe regions. However, we propose that these effects can be better understood by an emotional binding account whereby the amygdala mediates the recollection of item-emotion bindings that are forgotten more slowly than item-context bindings supported by the hippocampus.

Level of processing modulates the neural correlates of emotional memory formation

Emotion is known to influence multiple aspects of memory formation, including the initial encoding of the memory trace and its consolidation over time. However, the neural mechanisms whereby emotion impacts memory encoding remain largely unexplored. The present study used a levels-of-processing manipulation to characterize the impact of emotion on encoding with and without the influence of elaborative processes. Participants viewed emotionally negative, neutral, and positive scenes under two conditions: a shallow condition focused on the perceptual features of the scenes and a deep condition that queried their semantic meaning. Recognition memory was tested 2 days later. Results showed that emotional memory enhancements were greatest in the shallow condition. fMRI analyses revealed that the right amygdala predicted subsequent emotional memory in the shallow more than deep condition, whereas the right ventrolateral PFC demonstrated the reverse pattern. Furthermore, the association of these regions with the hippocampus was modulated by valence: the amygdala–hippocampal link was strongest for negative stimuli, whereas the prefrontal–hippocampal link was strongest for positive stimuli. Taken together, these results suggest two distinct activation patterns underlying emotional memory formation: an amygdala component that promotes memory during shallow encoding, especially for negative information, and a prefrontal component that provides extra benefits during deep encoding, especially for positive information.

Reinstatement of individual past events revealed by the similarity of distributed activation patterns during encoding and retrieval

Neurobiological memory models assume memory traces are stored in neocortex, with pointers in the hippocampus, and are then reactivated during retrieval, yielding the experience of remembering. Whereas most prior neuroimaging studies on reactivation have focused on the reactivation of sets or categories of items, the current study sought to identify cortical patterns pertaining to memory for individual scenes. During encoding, participants viewed pictures of scenes paired with matching labels (e.g., “barn,” “tunnel”), and, during retrieval, they recalled the scenes in response to the labels and rated the quality of their visual memories. Using representational similarity analyses, we interrogated the similarity between activation patterns during encoding and retrieval both at the item level (individual scenes) and the set level (all scenes). The study yielded four main findings. First, in occipitotemporal cortex, memory success increased with encoding-retrieval similarity (ERS) at the item level but not at the set level, indicating the reactivation of individual scenes. Second, in ventrolateral pFC, memory increased with ERS for both item and set levels, indicating the recapitulation of memory processes that benefit encoding and retrieval of all scenes. Third, in retrosplenial/posterior cingulate cortex, ERS was sensitive to individual scene information irrespective of memory success, suggesting automatic activation of scene contexts. Finally, consistent with neurobiological models, hippocampal activity during encoding predicted the subsequent reactivation of individual items. These findings show the promise of studying memory with greater specificity by isolating individual mnemonic representations and determining their relationship to factors like the detail with which past events are remembered.

Post-learning Hippocampal Dynamics Promote Preferential Retention of Rewarding Events

Reward motivation is known to modulate memory encoding, and this effect depends on interactions between the substantia nigra/ventral tegmental area complex (SN/VTA) and the hippocampus. It is unknown, however, whether these interactions influence offline neural activity in the human brain that is thought to promote memory consolidation. Here we used fMRI to test the effect of reward motivation on post-learning neural dynamics and subsequent memory for objects that were learned in high- and low-reward motivation contexts. We found that post-learning increases in resting-state functional connectivity between the SN/VTA and hippocampus predicted preferential retention of objects that were learned in high-reward contexts. In addition, multivariate pattern classification revealed that hippocampal representations of high-reward contexts were preferentially reactivated during post-learning rest, and the number of hippocampal reactivations was predictive of preferential retention of items learned in high-reward contexts. These findings indicate that reward motivation alters offline post-learning dynamics between the SN/VTA and hippocampus, providing novel evidence for a potential mechanism by which reward could influence memory consolidation.