Ian G. Dobbins

Executive control during episodic retrieval: Multiple prefrontal processes subserve source memory

During recognition, one may sense items as familiar (item memory) and additionally recollect specific contextual details of the earlier encounters (source memory). Cognitive theory suggests that, unlike item memory, source memory requires controlled cue specification and monitoring processes. Functional imaging suggests that such processes may depend on left prefrontal cortex (PFC). However, the nature and possible anatomical segregation of these processes remains unknown. Using functional magnetic resonance imaging, we isolated distinct response patterns in left PFC during source memory consistent with semantic analysis/cue specification (anterior ventrolateral), recollective monitoring (posterior dorsolateral and frontopolar), and phonological maintenance/rehearsal (posterior ventrolateral). Importantly, cue specification and recollective monitoring responses were not seen during item memory and were unaffected by retrieval success, demonstrating that the mere attempt to recollect episodic detail engages multiple control processes with different left PFC substrates.

Recollection and familiarity deficits in amnesia: convergence of remember-know, process dissociation, and receiver operating characteristic data.

Previous studies using the process dissociation and the remember-know procedures led to conflicting conclusions regarding the effects of anterograde amnesia on recollection and familiarity. We argue that these apparent contradictions arose because different models were used to interpret the results and because differences in false-alarm rates between groups biased the estimates provided by those models. A reanalysis of those studies with a dual-process signal-detection model that incorporates response bias revealed that amnesia led to a pronounced reduction in recollection and smaller but consistent reduction in familiarity. To test the assumptions of the model and to further assess recognition deficits in amnesics, we examined receiver operating characteristics (ROCs) in amnesics and controls. The ROCs of the controls were curved and asymmetrical, whereas those of the amnesics were curved and symmetrical. The results supported the predictions of the model and indicated that amnesia was associated with deficits in both recollection and familiarity.

Memory orientation and success: separable neurocognitive components underlying episodic recognition

Episodic recognition can be based on recollection of contextual details, on a sense of recent encounter, or some combination of the two. According to several cognitive models, selectively attending to these distinct aspects of memory may require different retrieval orientations and result in different neural responses depending upon whether or not retrieval is successful. Using event-related fMRI, we examined retrieval orientation by having subjects discriminate between two test words in one of two manners. During source recollection, they selected the member of the pair previously associated with a particular encoding task. In contrast, recency judgment required selection of the most recently encountered item of the pair, regardless of how it had been encoded. Furthermore, successful and unsuccessful trials within each retrieval task were contrasted to determine whether retrieval success effects occurred in overlapping or dissimilar neural populations compared to those associated with each retrieval orientation. The results revealed distinct lateral prefrontal and parietal activations that distinguished attempted source recollection from judgments of relative recency; these orientation effects were largely independent of retrieval success. In contrast, medial temporal lobe structures (hippocampus and parahippocampal gyrus) were differentially more active during successful recollection of encoding context, showing similar reduced responses during failed source recollection and judgments of recency. These results indicate that different memory orientations recruit distinct prefrontal and parietal networks and that the recovery of episodic context is associated with the hippocampus and surrounding medial temporal cortices.

Specificity of priming: a cognitive neuroscience perspective

Priming is a nonconscious form of memory that involves a change in a persons ability to identify, produce or classify an item as a result of a previous encounter with that item or a related item. One important question relates to the specificity of priming — the extent to which priming reflects the influence of abstract representations or the retention of specific features of a previous episode. Cognitive neuroscience analyses provide evidence for three types of specificity: stimulus, associative and response. We consider empirical, methodological and conceptual issues that relate to each type of specificity, and suggest a theoretical perspective to help in guiding future research.

Recognition memory for faces: When familiarity supports associative recognition judgments

Recognition memory for single items can be dissociated from recognition memory for the associations between items. For example, recognition tests for single words produce curvilinear receiver operating characteristics (ROCs), but associative recognition tests for word pairs produce linear ROCs. These dissociations are consistent with dual-process theories of recognition and suggest that associative recognition relies on recollection but that item recognition relies on a combination of recollection and assessments of familiarity. In the present study, we examined associative recognition ROCs for facial stimuli by manipulating the central and external features, in order to determine whether linear ROCs would be observed for stimuli other than arbitrary word pairs. When the faces were presented upright, familiarity estimates were significantly above zero, and the associative ROCs were curvilinear, suggesting that familiarity contributed to associative judgments. However, presenting the faces upside down effectively eliminated the contribution of familiarity to associative recognition, and the ROCs were linear. The results suggest that familiarity can support associative recognition judgments, if the associated components are encoded as a coherent gestalt, as in upright faces.

The inferior parietal lobule and recognition memory: Expectancy violation or successful retrieval?

Functional neuroimaging studies of episodic recognition demonstrate an increased lateral parietal response for studied versus new materials, often termed a retrieval success effect. Using a novel memory analog of attentional cueing, we manipulated the correspondence between anticipated and actual recognition evidence by presenting valid or invalid anticipatory cues (e.g., “likely old”) before recognition judgments. Although a superior parietal region demonstrated the retrieval success pattern, a larger inferior parietal lobule (IPL) region tracked the validity of the memory cueing (invalid cueing > valid cueing) and no retrieval success-sensitive lateral parietal region was insensitive to cueing. The invalid cueing response occurred even for correctly identified new items unlikely to trigger substantive episodic retrieval. Within the IPL, although supramarginal and angular gyrus (SMG; AG) regions both demonstrated invalid cueing amplitude elevations, each region differentially coupled with distinct cortical networks when unexpectedly old items were encountered; a connectivity pattern also observed at rest in the same subjects. These findings jointly suggest that the lateral parietal response during recognition does not signify the recovery of episodic content, but is a marker of the violation of memory expectations. A second independent dataset confirmed this interpretation by demonstrating that SMG activation tracked the decision biases of observers, not their accuracy, with increased activation for nondominant recognition judgments. The expectancy violation interpretation of the lateral parietal recognition response is consistent with the literature on visual search and oddball paradigms and suggests that damage to these regions should impair memory-linked orienting behavior and not retrieval per se.

fMRI Evidence for Separable and Lateralized Prefrontal Memory Monitoring Processes

Source memory research suggests that attempting to remember specific contextual aspects surrounding prior stimulus encounters results in greater left prefrontal cortex (PFC) activity than simple item-based old/new recognition judgments. Here, we tested a complementary hypothesis that predicts increases in the right PFC with tasks requiring close monitoring of item familiarity. More specifically, we compared a judgment of frequency (JOF) task to an item memory task, in which the former required estimating the number of previous picture encounters and the latter required discriminating old from new exemplars of previously seen items. In comparison to standard old/new recognition, both source memory and the JOF task examined here require more precise mnemonic judgments. However, in contrast to source memory, cognitive models suggest the JOF task relies heavily upon item familiarity, not specific contextual recollections. Event-related fMRI demonstrated greater recruitment of right, not left, dorso-lateral and frontopolar PFC regions during the JOF compared to item memory task. These data suggest a role for right PFC in the close monitoring of the familiarity of objects, which becomes critical when contextual recollection is ineffective in satisfying a memory demand.

The effects of priming on frontal-temporal communication

Repeated exposure to a stimulus facilitates its processing. This is reflected in faster and more accurate identification, reduced perceptual identification thresholds, and more efficient classifications for repeated compared with novel items. Here, we test a hypothesis that this experience-based behavioral facilitation is a result of enhanced communication between distinct cortical regions, which reduces local processing demands. A magnetoencephalographic investigation revealed that repeated object classification led to decreased neural responses in the prefrontal cortex and temporal cortex. Critically, this decrease in absolute activity was accompanied by greater neural synchrony (a measure of functional connectivity) between these regions with repetition. Additionally, the onset of the enhanced interregional synchrony predicted the degree of behavioral facilitation. These findings suggest that object repetition results in enhanced interactions between brain regions, which facilitates performance and reduces processing demands on the regions involved.

Cue- versus Probe-dependent Prefrontal Cortex Activity during Contextual Remembering

Functional neuroimaging comparisons of context and item memory frequently implicate the left prefrontal cortex (PFC) during the recovery of contextually specific memories. However, because cues and probes are often presented simultaneously, this activity could reflect operations involved in planning retrieval or instead reflect later operations dependent upon the memory probes themselves, such as evaluation of probe-evoked recollections. More importantly, planning-related activity, wherein subjects reinstate details outlining the nature of desired remembrances, should occur in response to contextual memory cues even before retrieval probes are available. Using event-related functional magnetic resonance imaging, we tested this by dissociating cue- from probe-related activity during context memory for pictures. Cues forewarning contextual memory demands yielded more activity than those forewarning item memory in the left lateral precentral gyrus, midline superior frontal gyrus, and right frontopolar cortex. Thus, these anticipatory, cue-based activations indicated whether upcoming probe decisions would require contextually specific memories or not. In contrast, the left dorsolateral/midventrolateral and anterior ventrolateral PFC areas did not show differential activity until the probes were actually presented, demonstrating greater activity for context than for item memory probes. Direct comparison of proximal left PFC regions demonstrated qualitatively different response profiles across cue versus probe periods for lateral precentral versus dorsolateral regions. These results potentially isolate contextual memory-planning-related processes from subsequent processes such as the evaluation of recollections, which are necessarily dependent on individual probe features. They also demonstrate that contextual remembering recruits multiple, functionally distinct PFC processes.

Functional Significance of Striatal Responses during Episodic Decisions: Recovery or Goal Attainment?

Memory retrieval is typically a goal-directed behavior, and as such, potentially influenced by reinforcement and motivation processes. Although striatal activation is often evident during memory retrieval, its functional significance remains unclear because typical memory paradigms do not control the motivational significance of memory decisions. We used event-related functional magnetic resonance imaging (fMRI) to investigate striatal activation during recognition with and without performance-linked monetary incentives. During initial performance in the absence of incentives, dorsal striatal activation for “Old” memory conclusions nonetheless exceeded that for “New” conclusions regardless of the accuracy of these conclusions. In contrast, subsequent scans paired incentives with either “Old” or “New” conclusions and demonstrated greater activation for whichever judgment was potentially rewarded, both with and without performance feedback. The data demonstrate that striatal activation during recognition judgments does not signal monetary reward receipt, cognitive feedback, or successful episodic retrieval. Instead, it is heavily dependent upon satisfaction of the subjective goals of the observer.