J. Benjamin Hutchinson

High-resolution fmri of content-sensitive subsequent memory responses in human medial temporal lobe

The essential role of the medial temporal lobe (MTL) in long-term memory for individual events is well established, yet important questions remain regarding the mnemonic functions of the component structures that constitute the region. Within the hippocampus, recent functional neuroimaging findings suggest that formation of new memories depends on the dentate gyrus and the CA3 field, whereas the contribution of the subiculum may be limited to retrieval. During encoding, it has been further hypothesized that structures within MTL cortex contribute to encoding in a content-sensitive manner, whereas hippocampal structures may contribute to encoding in a more domain-general manner. In the current experiment, high-resolution fMRI techniques were utilized to assess novelty and subsequent memory effects in MTL subregions for two classes of stimuli—faces and scenes. During scanning, participants performed an incidental encoding (target detection) task with novel and repeated faces and scenes. Subsequent recognition memory was indexed for the novel stimuli encountered during scanning. Analyses revealed voxels sensitive to both novel faces and novel scenes in all MTL regions. However, similar percentages of voxels were sensitive to novel faces and scenes in perirhinal cortex, entorhinal cortex, and a combined region comprising the dentate gyrus, CA2, and CA3, whereas parahippocampal cortex, CA1, and subiculum demonstrated greater sensitivity to novel scene stimuli. Paralleling these findings, subsequent memory effects in perirhinal cortex were observed for both faces and scenes, with the magnitude of encoding activation being related to later memory strength, as indexed by a graded response tracking recognition confidence, whereas subsequent memory effects were scene-selective in parahippocampal cortex. Within the hippocampus, encoding activation in the subiculum correlated with subsequent memory for both stimulus classes, with the magnitude of encoding activation varying in a graded manner with later memory strength. Collectively, these findings suggest a gradient of content sensitivity from posterior (parahippocampal) to anterior (perirhinal) MTL cortex, with MTL cortical regions differentially contributing to successful encoding based on event content. In contrast to recent suggestions, the present data further indicate that the subiculum may contribute to successful encoding irrespective of event content.

Functional Heterogeneity in Posterior Parietal Cortex Across Attention and Episodic Memory Retrieval

While attention is critical for event memory, debate has arisen regarding the extent to which posterior parietal cortex (PPC) activation during episodic retrieval reflects engagement of PPC-mediated mechanisms of attention. Here, we directly examined the relationship between attention and memory, within and across subjects, using functional magnetic resonance imaging attention-mapping and episodic retrieval paradigms. During retrieval, 4 functionally dissociable PPC regions were identified. Specifically, 2 PPC regions positively tracked retrieval outcomes: lateral intraparietal sulcus (latIPS) indexed graded item memory strength, whereas angular gyrus (AnG) tracked recollection. By contrast, 2 other PPC regions demonstrated nonmonotonic relationships with retrieval: superior parietal lobule (SPL) tracked retrieval reaction time, consistent with a graded engagement of top-down attention, whereas temporoparietal junction displayed a complex pattern of below-baseline retrieval activity, perhaps reflecting disengagement of bottom-up attention. Analyses of retrieval effects in PPC topographic spatial attention maps (IPS0-IPS5; SPL1) revealed that IPS5 and SPL1 exhibited a nonmonotonic relationship with retrieval outcomes resembling that in the SPL region, further suggesting that SPL activation during retrieval reflects top-down attention. While demands on PPC attention mechanisms vary during retrieval attempts, the present functional parcellation of PPC indicates that 2 additional mechanisms (mediated by latIPS and AnG) positively track retrieval outcomes.

Functional MRI-based lie detection: scientific and societal challenges

Functional MRI (fMRI)-based lie detection has been marketed as a tool for enhancing personnel selection, strengthening national security and protecting personal reputations, and at least three US courts have been asked to admit the results of lie detection scans as evidence during trials. How well does fMRI-based lie detection perform, and how should the courts, and society more generally, respond? Here, we address various questions — some of which are based on a meta-analysis of published studies — concerning the scientific state of the art in fMRI-based lie detection and its legal status, and discuss broader ethical and societal implications. We close with three general policy recommendations.

Increased Functional Connectivity between Dorsal Posterior Parietal and Ventral Occipitotemporal Cortex during Uncertain Memory Decisions

Retrieval of episodic memories is a multi-component act that relies on numerous operations ranging from processing the retrieval cue, evaluating retrieved information, and selecting the appropriate response given the demands of the task. Motivated by a rich functional neuroimaging literature, recent theorizing about various computations at retrieval has focused on the role of posterior parietal cortex (PPC). In a potentially promising line of research, recent neuroimaging findings suggest that different subregions of dorsal PPC respond distinctly to different aspects of retrieval decisions, suggesting that better understanding of their contributions might shed light on the component processes of retrieval. In an attempt to understand the basic operations performed by dorsal PPC, we used functional MRI and functional connectivity analyses to examine how activation in, and connectivity between, dorsal PPC and ventral temporal regions representing retrieval cues varies as a function of retrieval decision uncertainty. Specifically, participants made a five-point recognition confidence judgment for a series of old and new visually presented words. Consistent with prior studies, memory-related activity patterns dissociated across left dorsal PPC subregions, with activity in the lateral IPS tracking the degree to which participants perceived an item to be old, whereas activity in the SPL increased as a function of decision uncertainty. Importantly, whole-brain functional connectivity analyses further revealed that SPL activity was more strongly correlated with that in the visual word-form area during uncertain relative to certain decisions. These data suggest that the involvement of SPL during episodic retrieval reflects, at least in part, the processing of the retrieval cue, perhaps in service of attempts to increase the mnemonic evidence elicited by the cue.

Reduced hippocampal activity during encoding in cognitively normal adults carrying the APOE ɛ4 allele.

Apolipoprotein (APOE) ɛ4-related differences in memory performance have been detected before age 65. The hippocampus and the surrounding medial temporal lobe (MTL) structures are the first site affected by Alzheimers disease (AD) and the MTL is the seat of episodic memory, including visuo-spatial memory. While reports of APOE ɛ4-related differences in these brain structures are not consistent in either cross-sectional or longitudinal structural and functional magnetic resonance imaging (fMRI) studies, there is increasing evidence that brain activity at baseline (defined as activity during fixation or rest) may differ in APOE ɛ4 carriers compared to non-carriers. In this fMRI study, cognitively normal APOE ɛ4 carriers and non-carriers engaged in a perspective-dependent spatial learning task (Shelton & Gabrieli, 2002) previously shown to activate MTL structures in older participants (Borghesani et al., 2008). A low-level, visually engaging dot-control task was used for comparison, in addition to fixation. APOE ɛ4 carriers showed less activation than non-carriers in the hippocampus proper during encoding. Specifically, when spatial encoding was contrasted against the dot-control task, encoding-related activation was significantly lower in carriers than non-carriers. By contrast, no ɛ4-related differences in the hippocampus were found when spatial encoding was compared with fixation. Lower activation, however, was not global since encoding-related activation in early visual cortex (left lingual gyrus) was not different between APOE ɛ4 carriers and non-carriers. The present data document APOE ɛ4-related differences in the hippocampus proper during encoding and underscore the role of low-level control contrasts for complex encoding tasks. These results have implications for fMRI studies that investigate the default-mode network (DMN) in middle-aged to older APOE ɛ4 carriers to help evaluate AD risk in this otherwise cognitively normal population.

A Roadmap to Brain Mapping: Toward a Functional Map of Human Parietal Cortex

In this issue of Neuron, Nelson and colleagues report a novel parcellation of human lateral parietal cortex based on task-induced response profiles and resting-state functional connectivity. Their findings inform current debates about the contributions of parietal cortex to cognition, including the retrieval of episodic memories.

Electrocorticography reveals the temporal dynamics of posterior parietal cortical activity during recognition memory decisions

Significance Over the past decade, human posterior parietal cortex (PPC) has been unexpectedly implicated in remembering and memory-related decision making. Functional neuroimaging indicates that memory-related responses differ across PPC, and patients with PPC lesions show subtle to significant changes in memory behavior. These surprising observations have motivated novel theorizing, yet current understanding of PPC contributions to memory is limited by the absence of temporal information about activity in PPC subregions as retrieval decisions unfold. In this study, recordings from the human brain show for the first time that distinct temporal and functional profiles of activity are present in PPC subregions as participants make recognition memory decisions. These new findings inform theories of parietal functional contributions to memory, decision making, and attention. Theories of the neurobiology of episodic memory predominantly focus on the contributions of medial temporal lobe structures, based on extensive lesion, electrophysiological, and imaging evidence. Against this backdrop, functional neuroimaging data have unexpectedly implicated left posterior parietal cortex (PPC) in episodic retrieval, revealing distinct activation patterns in PPC subregions as humans make memory-related decisions. To date, theorizing about the functional contributions of PPC has been hampered by the absence of information about the temporal dynamics of PPC activity as retrieval unfolds. Here, we leveraged electrocorticography to examine the temporal profile of high gamma power (HGP) in dorsal PPC subregions as participants made old/new recognition memory decisions. A double dissociation in memory-related HGP was observed, with activity in left intraparietal sulcus (IPS) and left superior parietal lobule (SPL) differing in time and sign for recognized old items (Hits) and correctly rejected novel items (CRs). Specifically, HGP in left IPS increased for Hits 300–700 ms poststimulus onset, and decayed to baseline ∼200 ms preresponse. By contrast, HGP in left SPL increased for CRs early after stimulus onset (200−300 ms) and late in the memory decision (from 700 ms to response). These memory-related effects were unique to left PPC, as they were not observed in right PPC. Finally, memory-related HGP in left IPS and SPL was sufficiently reliable to enable brain-based decoding of the participant’s memory state at the single-trial level, using multivariate pattern classification. Collectively, these data provide insights into left PPC temporal dynamics as humans make recognition memory decisions.

When past is present: Substitutions of long-term memory for sensory evidence in perceptual judgments.

When perception is underdetermined by current sensory inputs, memories for related experiences in the past might fill in missing detail. To evaluate this possibility, we measured the likelihood of relying on long-term memory versus sensory evidence when judging the appearance of an object near the threshold of awareness. Specifically, we associated colors with shapes in long-term memory and then presented the shapes again later in unrelated colors and had observers judge the appearance of the new colors. We found that responses were well characterized as a bimodal mixture of original and current-color representations (vs. an integrated unimodal representation). That is, although irrelevant to judgments of the current color, observers occasionally anchored their responses on the original colors in memory. Moreover, the likelihood of such memory substitutions increased when sensory input was degraded. In fact, they occurred even in the absence of sensory input when observers falsely reported having seen something. Thus, although perceptual judgments intuitively seem to reflect the current state of the environment, they can also unknowingly be dictated by past experiences.

Biased competition during long-term memory formation

A key task for the brain is to determine which pieces of information are worth storing in memory. To build a more complete representation of the environment, memory systems may prioritize new information that has not already been stored. Here, we propose a mechanism that supports this preferential encoding of new information, whereby prior experience attenuates neural activity for old information that is competing for processing. We evaluated this hypothesis with fMRI by presenting a series of novel stimuli concurrently with repeated stimuli at different spatial locations in Experiment 1 and from different visual categories (i.e., faces and scenes) in Experiment 2. Subsequent memory for the novel stimuli could be predicted from the reduction in activity in ventral temporal cortex for the accompanying repeated stimuli. This relationship was eliminated in control conditions where the competition during encoding came from another novel stimulus. These findings reveal how prior experience adaptively guides learning toward new aspects of the environment.