Zara M. Bergström

Neural Markers of Inhibition in Human Memory Retrieval

Retrieving particular information from memory facilitates the later retrieval of that information, but also impairs the later retrieval of related, interfering information. It has been theorized that this retrieval-induced forgetting reflects inhibition of interfering memory representations. We used event-related fMRI to investigate the functional neuroanatomy of this impaired retrieval, at the time the impairment is observed. Neural activity differences between impaired and facilitated information occurred in left ventrolateral prefrontal cortex (VLPFC, BA 45 and 47), precuneus (BA 7), and right inferior parietal lobule (IPL, BA 40). Activity in left anterior VLPFC (BA 47) and left posterior temporal cortex (BA 22), regions implicated in the controlled retrieval of weak semantic memory representations, predicted the degree of retrieval-induced forgetting. In contrast, activity in precuneus and right IPL predicted the degree of retrieval-induced facilitation. Our findings demonstrate that impairment of interfering memories and facilitation of practiced memories involve distinct neural processes, and suggest that the impairment reflects inhibition that weakens interfering memory representations.

ERP evidence for successful voluntary avoidance of conscious recollection

We investigated neurocognitive processes of voluntarily avoiding conscious recollection by asking participants to either attempt to recollect (the Think condition) or to avoid recollecting (the No-Think condition) a previously exposed paired associate. Event-related potentials (ERPs) during Think and No-Think trials were separated on the basis of previous learning success versus failure. This separation yielded temporal and topographic dissociations between early ERP effects of a Think versus No-Think strategy, which were maximal between 200 and 300 ms after stimulus presentation and independent of learning status, and a later learning-specific ERP effect maximal between 500 and 800 ms after stimulus presentation. In this later time-window, Learned Think items elicited a larger late left parietal positivity than did Not Learned Think, Learned No-Think, and Not Learned No-Think items; moreover, Learned No-Think and Not Learned Think items did not differ in late left parietal positivity. Because the late left parietal positivity indexes conscious recollection, the results provide firm evidence that conscious recollection of recollectable information can be voluntarily avoided on an item-specific basis and help to clarify previous neural evidence from the Think/No-Think procedure, which could not separate item-specific from strategic processes.

ERP and behavioural evidence for direct suppression of unwanted memories

There are some past experiences that we would prefer not to remember. Previous research has shown that repeatedly stopping retrieval of an unwanted memory increases the probability of later forgetting of that memory, and engages prefrontal control mechanisms to attenuate activity in the hippocampus. However, the mechanisms of preventing memory retrieval, and how these relate to the later forgetting, are yet to be fully understood. Here we present neural and behavioural evidence that two distinct strategies for retrieval stopping - direct memory suppression and self-distracting thought substitution - contribute to forgetting of unwanted memories in qualitatively different ways. Only direct memory suppression reduced centro-parietal positivity in the event-related potentials (ERP) between 300 and 600 ms post-stimulus, consistent with a reduction in the ERP correlate of recollection. Furthermore, only direct memory suppression produced later inhibitory forgetting that was predicted by an earlier negative ERP effect that may be associated with motor inhibition. In contrast, thought substitution produced later non-inhibitory forgetting and had no effect on the ERP correlate of recollection. Our findings demonstrate the first ERP and behavioural dissociation between inhibitory and non-inhibitory forgetting, and suggest that unwanted memories may be directly suppressed without selective retrieval of alternative memories.

Behavioral and ERP evidence of greater distractor processing in old age

The ability to minimize processing for irrelevant information is a central component of goal-directed behavior, which has been suggested to be compromised in old age. In this study, we investigate age differences in distractor rejection by presenting target names alongside to-be-ignored distractor faces. Older adults (mean age 70) showed greater behavioral slowing than young adults (mean age 24) when the distractor face was incompatible with the target name. That this increased interference in the older adults was indeed associated with more distractor processing, was shown by the face-related N170 component of the EEG, which had greater amplitude in older adults when faces were unattended, but not when they were attended. These findings suggest a reduced ability to prevent distractor processing in old age.

A Specific Brain Structural Basis for Individual Differences in Reality Monitoring

Much recent interest has centered on understanding the relationship between brain structure variability and individual differences in cognition, but there has been little progress in identifying specific neuroanatomical bases of such individual differences. One cognitive ability that exhibits considerable variability in the healthy population is reality monitoring; the cognitive processes used to introspectively judge whether a memory came from an internal or external source (e.g., whether an event was imagined or actually occurred). Neuroimaging research has implicated the medial anterior prefrontal cortex (PFC) in reality monitoring, and here we sought to determine whether morphological variability in a specific anteromedial PFC brain structure, the paracingulate sulcus (PCS), might underlie performance. Fifty-three healthy volunteers were selected on the basis of MRI scans and classified into four groups according to presence or absence of the PCS in their left or right hemisphere. The group with absence of the PCS in both hemispheres showed significantly reduced reality monitoring performance and ability to introspect metacognitively about their performance when compared with other participants. Consistent with the prediction that sulcal absence might mean greater volume in the surrounding frontal gyri, voxel-based morphometry revealed a significant negative correlation between anterior PFC gray matter and reality monitoring performance. The findings provide evidence that individual differences in introspective abilities like reality monitoring may be associated with specific structural variability in the PFC.

Continuous Theta Burst Stimulation of Angular Gyrus Reduces Subjective Recollection

The contribution of lateral parietal regions such as the angular gyrus to human episodic memory has been the subject of much debate following widespread observations of left parietal activity in healthy volunteers during functional neuroimaging studies of memory retrieval. Patients with lateral parietal lesions are not amnesic, but recent evidence indicates that their memory abilities may not be entirely preserved. Whereas recollection appears intact when objective measures such as source accuracy are used, patients often exhibit reduced subjective confidence in their accurate recollections. When asked to recall autobiographical memories, they may produce spontaneous narratives that lack richness and specificity, but can remember specific details when prompted. Two distinct theoretical accounts have been proposed to explain these results: that the patients have a deficit in the bottom-up capturing of attention by retrieval output, or that they have an impairment in the subjective experience of recollection. The present study aimed to differentiate between these accounts using continuous theta burst stimulation (cTBS) in healthy participants to disrupt function of specific left parietal subregions, including angular gyrus. Inconsistent with predictions of the attentional theory, angular gyrus cTBS did not result in greater impairment of free recall than cued recall. Supporting predictions of the subjective recollection account, temporary disruption of angular gyrus was associated with highly accurate source recollection accuracy but a selective reduction in participants’ rated source confidence. The findings are consistent with a role for angular gyrus in the integration of memory features into a conscious representation that enables the subjective experience of remembering.

Event-related potential evidence that automatic recollection can be voluntarily avoided

Voluntary control processes can be recruited to facilitate recollection in situations where a retrieval cue fails to automatically bring to mind a desired episodic memory. We investigated whether voluntary control processes can also stop recollection of unwanted memories that would otherwise have been automatically recollected. Participants were trained on cue–associate word-pairs, then repeatedly presented with the cue and asked to either recollect or avoid recollecting the associate, while having the event-related potential (ERP) correlate of conscious recollection measured. Halfway through the phase, some cues switched instructions so that participants had to start avoiding recall of associates they had previously repeatedly recalled, and vice versa. ERPs during recollection avoidance showed a significantly reduced positivity in the correlate of conscious recollection, and switching instructions reversed the ERP effect even for items that had been previously repeatedly recalled, suggesting that voluntary control processes can override highly practiced, automatic recollection. Avoiding recollection of particularly prepotent memories was associated with an additional, earlier ERP negativity that was separable from the later voluntary modulation of conscious recollection. The findings have implications for theories of memory retrieval by highlighting the involvement of voluntary attentional processes in controlling conscious recollection.

Suppressing Unwanted Autobiographical Memories Reduces Their Automatic Influences: Evidence From Electrophysiology and an Implicit Autobiographical Memory Test

The present study investigated the extent to which people can suppress unwanted autobiographical memories in a memory-detection context involving a mock crime. Participants encoded sensorimotor-rich memories by enacting a lab-based crime (stealing a ring) and received instructions to suppress memory of the crime in order to evade guilt detection in a brain-wave-based concealed-information test. Aftereffects of suppression on automatic memory processes were measured in an autobiographical Implicit Association Test. Results showed that suppression attenuated brain-wave activity (the P300) associated with crime-relevant memory retrieval, which rendered waveforms from innocent and guilty participants indistinguishable. However, the two groups could nevertheless be discriminated via the late-posterior-negative slow wave, which may reflect the need to monitor response conflict arising between voluntary suppression and automatic recognition processes. Finally, extending recent findings that suppression can impair implicit memory processes, we provide novel evidence that suppression reduces automatic cognitive biases often associated with actual autobiographical memories.

Multimodal imaging reveals the spatiotemporal dynamics of recollection.

Functional MRI research suggests that different frontal and parietal cortical regions support strategic processes that are engaged at different stages of recollection, from pre-retrieval processing of a cue to post-retrieval maintenance and evaluation of recollected information. Whereas some of these regions respond in a domain-general way, other regions are sensitive to the type of information being recollected. However, the low temporal resolution of fMRI cannot distinguish component processes at the time-scale at which recollection occurs. We therefore combined fMRI with the excellent temporal resolution of source localised EEG/MEG to investigate the spatiotemporal neural dynamics of recollection. fMRI and EEG/MEG data were collected from the same participants in two sessions while they retrieved different types of episodic information. This multimodal imaging approach revealed striking consistency between the regions identified with fMRI and EEG/MEG, providing novel evidence of how these brain areas interact over time to support source recollection. For domain-general recollection, results from both modalities converged in showing the strongest activations in medial parietal cortex, which according to EEG/MEG was reliable at a late retrieval stage. Domain-specific source recollection increased fMRI and EEG/MEG activation in the left lateral prefrontal cortex, which EEG/MEG indicated also to be recruited during a post-recollection stage. The findings suggest that although medial parietal and left lateral prefrontal regions mediate functionally different retrieval processes, they are both engaged at a late stage of episodic retrieval.

Intentional retrieval suppression can conceal guilty knowledge in ERP memory detection tests

Highlights • Brain activity markers of memory retrieval are used in tests of criminal guilt.• These tests assume neural markers of memory are outside voluntary control.• We tested whether participants could suppress memory-related brain activity.• Suppression was highly successful, significantly reducing guilt detection.• Our results indicate that a core assumption of memory detection tests is unjustified.