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1.  Altered visual-spatial attention to task-irrelevant information is associated with falls risk in older adults 
Neuropsychologia  2013;51(14):3025-3032.
Executive cognitive functions play a critical role in falls risk – a pressing health care issue in seniors. In particular, intact attentional processing is integral for safe mobility and navigation. However, the specific contribution of impaired visual-spatial attention in falls remains unclear. In this study, we examined the association between visual-spatial attention to task-irrelevant stimuli and falls risk in community-dwelling older adults. Participants completed a visual target discrimination task at fixation while task-irrelevant probes were presented in both visual fields. We assessed attention to left and right peripheral probes using event-related potentials (ERPs). Falls risk was determined using the valid and reliable Physiological Profile Assessment (PPA). We found a significantly positive association between reduced attentional facilitation, as measured by the N1 ERP component, and falls risk. This relationship was specific to probes presented in the left visual field and measured at ipsilateral electrode sites. Our results suggest that fallers exhibit reduced attention to the left side of visual space and provide evidence that impaired right hemispheric function and/or structure may contribute to falls.
PMCID: PMC4318690  PMID: 24436970 CAMSID: cams4313
Visual-spatial attention; Aging; Older adults; Falls risk; Event-related potentials (ERPs); Neuroimaging
2.  Sex differences in brain-behavior relationships between verbal episodic memory and resting regional cerebral blood flow 
Neuropsychologia  2000;38(4):451-461.
Women have better verbal memory, and higher rates of resting regional cerebral blood flow (rCBF). This study examined whether there are also sex differences in the relationship between verbal episodic memory and resting rCBF. Twenty eight healthy right-handed volunteers (14 male, 14 female) underwent a neuropsychological evaluation and a Positron Emission Tomography (PET) 15O-water study. Immediate and delayed recall was measured on the logical memory subtest of the Wechsler Memory Scale — Revised (WMS-R), and on the California Verbal Learning Test (CVLT). Resting rCBF (ml/100 g/min) was calculated for four frontal, four temporal, and four limbic regions of interest (ROIs). Women had better immediate recall on both WMS-R and CVLT tasks. Sex differences in rCBF were found for temporal lobe regions. Women had greater bilateral blood flow in a mid-temporal brain region. There were also sex differences in rCBF correlations with performance. Women produced positive correlations with rCBF laterality in the temporal pole. Greater relative CBF in the left temporal pole was associated with better WMS-R immediate and delayed recall in women only. These results suggest that trait differences in temporal pole brain-behavior relationships may relate to sex differences in verbal episodic memory.
PMCID: PMC4334366  PMID: 10683395
Sex differences; episodic memory; cerebral blood flow; positron emission tomography; functional neuroimaging
3.  What might have been? The role of the ventromedial prefrontal cortex and lateral orbitofrontal cortex in counterfactual emotions and choice 
Neuropsychologia  2013;54:77-86.
Counterfactual feelings of regret occur when people make comparisons between an actual outcome and a better outcome that would have occurred under a different choice. We investigated the choices of individuals with damage to the ventral medial prefrontal cortex (VMPFC) and the lateral orbital frontal cortex (LOFC) to see whether their emotional responses were sensitive to regret. Participants made choices between gambles, each with monetary outcomes. After every choice, subjects learned the consequences of both gambles and rated their emotional response to the outcome. Normal subjects and lesion control subjects tended to make better choices and reported post-decision emotions that were sensitive to regret comparisons. VMPFC patients tended to make worse choices, and, contrary to our predictions, they reported emotions that were sensitive to regret comparisons. In contrast, LOFC patients made better choices, but reported emotional reactions that were insensitive to regret comparisons. We suggest the VMPFC is involved in the association between choices and anticipated emotions that guide future choices, while the LOFC is involved in experienced emotions that follow choices, emotions that may signal the need for behavioral change.
PMCID: PMC4319649  PMID: 24333168
VMPFC; OFC; regret; decision making; emotion; counterfactual comparison
4.  Autism spectrum disorder, but not amygdala lesions, impairs social attention in visual search 
Neuropsychologia  2014;63:259-274.
People with autism spectrum disorders (ASD) have pervasive impairments in social interactions, a diagnostic component that may have its roots in atypical social motivation and attention. One of the brain structures implicated in the social abnormalities seen in ASD is the amygdala. To further characterize the impairment of people with ASD in social attention, and to explore the possible role of the amygdala, we employed a series of visual search tasks with both social (faces and people with different postures, emotions, ages, and genders) and non-social stimuli (e.g., electronics, food, and utensils). We first conducted trial-wise analyses of fixation properties and elucidated visual search mechanisms. We found that an attentional mechanism of initial orientation could explain the detection advantage of non-social targets. We then zoomed into fixation-wise analyses. We defined target-relevant effects as the difference in the percentage of fixations that fell on target-congruent vs. target-incongruent items in the array. In Experiment 1, we tested 8 high-functioning adults with ASD, 3 adults with focal bilateral amygdala lesions, and 19 controls. Controls rapidly oriented to target-congruent items and showed a strong and sustained preference for fixating them. Strikingly, people with ASD oriented significantly less and more slowly to target-congruent items, an attentional deficit especially with social targets. By contrast, patients with amygdala lesions performed indistinguishably from controls. In Experiment 2, we recruited a different sample of 13 people with ASD and 8 healthy controls, and tested them on the same search arrays but with all array items equalized for low-level saliency. The results replicated those of Experiment 1. In Experiment 3, we recruited 13 people with ASD, 8 healthy controls, 3 amygdala lesion patients and another group of 11 controls and tested them on a simpler array. Here our group effect for ASD strongly diminished and all four subject groups showed similar target-relevant effects. These findings argue for an attentional deficit in ASD that is disproportionate for social stimuli, cannot be explained by low-level visual properties of the stimuli, and is more severe with high-load top-down task demands. Furthermore, this deficit appears to be independent of the amygdala, and not evident from general social bias independent of the target-directed search.
PMCID: PMC4317264  PMID: 25218953
Visual search; Autism; Amygdala; Saliency; Social
5.  [No title available] 
PMCID: PMC3932664  PMID: 24389506
6.  Dopamine receptor D4 (DRD4) gene modulates the influence of informational masking on speech recognition 
Neuropsychologia  2014;0:121-131.
Listeners vary substantially in their ability to recognize speech in noisy environments. Here we examined the role of genetic variation on individual differences in speech recognition in various noise backgrounds. Background noise typically varies in the levels of energetic masking (EM) and informational masking (IM) imposed on target speech. Relative to EM, release from IM is hypothesized to place greater demand on executive function to selectively attend to target speech while ignoring competing noises. Recent evidence suggests that the long allele variant in exon III of the DRD4 gene, primarily expressed in the prefrontal cortex, may be associated with enhanced selective attention to goal-relevant high-priority information even in the face of interference. We investigated the extent to which this polymorphism is associated with speech recognition in IM and EM conditions. In an unscreened adult sample (Experiment 1) and a larger screened replication sample (Experiment 2), we demonstrate that individuals with the DRD4 long variant show better recognition performance in noise conditions involving significant IM, but not in EM conditions. In Experiment 2, we also obtained neuropsychological measures to assess the underlying mechanisms. Mediation analyses revealed that this listening condition-specific advantage was mediated by enhanced executive attention/working memory capacity in individuals with the long allele variant. These findings suggest that DRD4 may contribute specifically to individual differences in speech recognition ability in noise conditions that place demands on executive function.
PMCID: PMC4297728  PMID: 25497692
Speech perception; Individual difference; Informational masking; Executive attention/working memory capacity; DRD4
7.  Activity reductions in perirhinal cortex predict conceptual priming and familiarity-based recognition 
Neuropsychologia  2013;52:19-26.
Although it is well established that regions in the medial temporal lobes are critical for explicit memory, recent work has suggested that one medial temporal lobe subregion – the perirhinal cortex (PRC) – may also support conceptual priming, a form of implicit memory. Here, we sought to investigate whether activity reductions in PRC, previously linked to familiarity-based recognition, might also support conceptual implicit memory retrieval. Using a free association priming task, the current study tested the prediction that PRC indexes conceptual priming independent of contributions from perceptual and response repetition. Participants first completed an incidental semantic encoding task outside of the MRI scanner. Next, they were scanned during performance of a free association priming task, followed by a recognition memory test. Results indicated successful conceptual priming was associated with decreased PRC activity, and that an overlapping region within the PRC also exhibited activity reductions that covaried with familiarity during the recognition memory test. Our results demonstrate that the PRC contributes to both conceptual priming and familiarity-based recognition, which may reflect a common role of this region in implicit and explicit memory retrieval.
PMCID: PMC3923843  PMID: 24157537
perirhinal cortex; hippocampus; implicit memory; conceptual priming; recognition memory; familiarity; recollection
8.  White matter hyperintensities are associated with visual search behavior independent of generalized slowing in aging 
Neuropsychologia  2013;52:93-101.
A fundamental controversy is whether cognitive decline with advancing age can be entirely explained by decreased processing speed, or whether specific neural changes can elicit cognitive decline, independent of slowing. These hypotheses are anchored by studies of healthy older individuals where age is presumed the sole influence. Unfortunately, advancing age is also associated with asymptomatic brain white matter injury. We hypothesized that differences in white matter injury extent, manifest by MRI white matter hyperintensities (WMH), mediate differences in visual attentional control in healthy aging, beyond processing speed differences. We tested young and cognitively healthy older adults on search tasks indexing speed and attentional control. Increasing age was associated with generally slowed performance. WMH was also associated with slowed search times independent of processing speed differences. Consistent with evidence attributing reduced network connectivity to WMH, these results conclusively demonstrate that clinically silent white matter injury contributes to slower search performance indicative of compromised cognitive control, independent of generalized slowing of processing speed.
PMCID: PMC3924853  PMID: 24183716
Cognitive control; Visual attention; Aging; Cerebrovascular disease; Cognitive neuroscience; Neuroimaging
9.  Longitudinal Processing Speed Impairments in Males with Autism and the Effects of White Matter Microstructure 
Neuropsychologia  2013;53:137-145.
The present study used an accelerated longitudinal design to examine group differences and age-related changes in processing speed in 81 individuals with Autism Spectrum Disorder (ASD) compared to 56 age-matched individuals with typical development (ages 6–39 years). Processing speed was assessed using the Wechsler Intelligence Scale for Children-3rd edition (WISC-III) and the Wechsler Adult Intelligence Scale-3rd edition (WAIS-III). Follow-up analyses examined processing speed subtest performance and relations between processing speed and white matter microstructure (as measured with diffusion tensor imaging [DTI] in a subset of these participants). After controlling for full scale IQ, the present results show that processing speed index standard scores were on average 12 points lower in the group with ASD compared to the group with typical development. There were, however, no significant group differences in standard score age-related changes within this age range. For subtest raw scores, the group with ASD demonstrated robustly slower processing speeds in the adult versions of the IQ test (i.e., WAIS-III) but not in the child versions (WISC-III), even though age-related changes were similar in both the ASD and typically developing groups. This pattern of results may reflect difficulties that become increasingly evident in ASD on more complex measures of processing speed. Finally, DTI measures of whole-brain white matter microstructure suggested that fractional anisotropy (but not mean diffusivity, radial diffusivity, or axial diffusivity) made significant but small-sized contributions to processing speed standard scores across our entire sample. Taken together, the present findings suggest that robust decreases in processing speed may be present in ASD, more pronounced in adulthood, and partially attributable to white matter microstructural integrity.
PMCID: PMC3946881  PMID: 24269298
autism; processing speed; diffusion tensor imaging; white matter; executive function
10.  A novel approach to an old problem: analysis of systematic errors in two models of recognition memory 
Neuropsychologia  2013;52:51-56.
For more than a decade, the high threshold dual process (HTDP) model has served as a guide for studying the functional neuroanatomy of recognition memory. The HTDP model's utility has been that it provides quantitative estimates of recollection and familiarity, two processes thought to support recognition ability. Important support for the model has been the observation that it fits experimental data well. The continuous dual process (CDP) model also fits experimental data well. However, this model does not provide quantitative estimates of recollection and familiarity, making it less immediately useful for illuminating the functional neuroanatomy of recognition memory. These two models are incompatible and cannot both be correct, and an alternative method of model comparison is needed. We tested for systematic errors in each model's ability to fit recognition memory data from four independent data sets from three different laboratories. Across participants and across data sets, the HTDP model (but not the CDP model) exhibited systematic error. In addition, the pattern of errors exhibited by the HTDP model was predicted by the CDP model. The findings were the same at both the group and individual levels of analysis. We conclude that the CDP model provides a better account of recognition memory than the HTDP model.
PMCID: PMC4079078  PMID: 24184486
11.  The local, global, and neural aspects of visuospatial processing in autism spectrum disorders 
Neuropsychologia  2013;51(14):2995-3003.
Behavioral studies have documented a relative advantage in some aspects of visuospatial cognition in autism although it is not consistently found in higher functioning individuals with autism. The purpose of this functional neuroimaging study was to examine the neural activity in high functioning individuals with autism while they performed a block design task that systematically varied with regard to whether a global pattern was present. Participants were 14 adults with high-functioning autism and 14 age and IQ matched typical controls. The task was to identify a missing block in target figures which had either an obvious global shape or was an arbitrary array of blocks. Behavioral results showed intact, but not superior, performance in our participants with autism. A key group difference was that the participants with autism showed reliably greater activation in occipital and parietal regions in both tasks suggesting an increased reliance of the autism group on posterior brain areas to mediate visuospatial tasks. Thus, increased reliance on relatively posterior brain regions in itself may not guarantee superior performance as seen in the present study.
PMCID: PMC3900283  PMID: 24184351
Autism; fMRI; global-local processing; block design task
12.  A neurocomputational account of cognitive deficits in Parkinson’s disease 
Neuropsychologia  2012;50(9):2290-2302.
Parkinson’s disease (PD) is caused by the accelerated death of dopamine (DA) producing neurons. Numerous studies documenting cognitive deficits of PD patients have revealed impairments in a variety of tasks related to memory, learning, visuospatial skills, and attention. While there have been several studies documenting cognitive deficits of PD patients, very few computational models have been proposed. In this article, we use the COVIS model of category learning to simulate DA depletion and show that the model suffers from cognitive symptoms similar to those of human participants affected by PD. Specifically, DA depletion in COVIS produced deficits in rule-based categorization, non-linear information-integration categorization, probabilistic classification, rule maintenance, and rule switching. These were observed by simulating results from younger controls, older controls, PD patients, and severe PD patients in five well-known tasks. Differential performance among the different age groups and clinical populations was modeled simply by changing the amount of DA available in the model. This suggests that COVIS may not only be an adequate model of the simulated tasks and phenomena but also more generally of the role of DA in these tasks and phenomena.
PMCID: PMC4220550  PMID: 22683450
Parkinson’s disease; Computational modeling; COVIS; Perceptual categorization; Probabilistic classification; Wisconsin Card Sorting Test (WCST)
13.  More attention when speaking: does it help or does it hurt? 
Neuropsychologia  2013;51(13):2770-2780.
Paying selective attention to a word in a multi-word utterance results in a decreased probability of error on that word (benefit), but an increased probability of error on the other words (cost). We ask whether excitation of the prefrontal cortex helps or hurts this cost. One hypothesis (the resource hypothesis) predicts a decrease in the cost due to the deployment of more attentional resources, while another (the focus hypothesis) predicts even greater costs due to further fine-tuning of selective attention. Our results are more consistent with the focus hypothesis: prefrontal stimulation caused a reliable increase in the benefit and a marginal increase in the cost of selective attention. To ensure that the effects are due to changes to the prefrontal cortex, we provide two checks: We show that the pattern of results is quite different if, instead, the primary motor cortex is stimulated. We also show that the stimulation-related benefits in the verbal task correlate with the stimulation-related benefits in an N-back task, which is known to tap into a prefrontal function. Our results shed light on how selective attention affects language production, and more generally, on how selective attention affects production of a sequence over time.
PMCID: PMC4124528  PMID: 24012690
Language production; cognitive control; executive functions; selective attention; transcranial direct cortical stimulation (tDCS)
14.  Lifelong Bilingualism Contributes to Cognitive Reserve against White Matter Integrity Declines in Aging 
Neuropsychologia  2013;51(13):10.1016/j.neuropsychologia.2013.09.037.
Recent evidence suggests that lifelong bilingualism may contribute to cognitive reserve (CR) in normal aging. However, there is currently no neuroimaging evidence to suggest that lifelong bilinguals can retain normal cognitive functioning in the face of age-related neurodegeneration. Here we explored this issue by comparing white matter (WM) integrity and gray matter (GM) volumetric patterns of older adult lifelong bilinguals (N = 20) and monolinguals (N = 20). The groups were matched on a range of relevant cognitive test scores and on the established CR variables of education, socioeconomic status and intelligence. Participants underwent high-resolution structural imaging for assessment of GM volume and diffusion tensor imaging (DTI) for assessment of WM integrity. Results indicated significantly lower microstructural integrity in the bilingual group in several WM tracts. In particular, compared to their monolingual peers, the bilingual group showed lower fractional anisotropy and/or higher radial diffusivity in the inferior longitudinal fasciculus/inferior fronto-occipital fasciculus bilaterally, the fornix, and multiple portions of the corpus callosum. There were no group differences in GM volume. Our results suggest that lifelong bilingualism contributes to CR against WM integrity declines in aging.
PMCID: PMC3856701  PMID: 24103400
cognitive reserve; brain reserve; bilingualism; DTI; aging
15.  The nature of anterograde and retrograde memory impairment after damage to the medial temporal lobe 
Neuropsychologia  2013;51(13):10.1016/j.neuropsychologia.2013.09.015.
The study of anterograde and retrograde amnesia (AA and RA) in the laboratory and the clinic has provided important information about the structure and organization of memory. The severity of AA is usually correlated with the severity of RA. Nevertheless, variations in the expression of AA and RA have been reported, which presumably reflect variation in the locus and extent of brain damage. The relationship between AA and RA has rarely been described quantitatively in groups of patients where detailed anatomical information is available. We have quantified the severity of AA and RA for factual information in 11 memory-impaired patients with bilateral medial temporal lobe lesions, including 5 for whom detailed post-mortem neurohistological information was available. The findings describe an orderly relationship between AA and RA, such that patients with more severe AA also had more extensive RA. In addition, RA was measurable only after AA reached a substantial level of severity. This relationship between AA and RA in patients with identified medial temporal lobe lesions appears to describe a general principle, which applies to a range of etiologies, including traumatic amnesia, where the locus and extent of brain damage is less well understood. Whenever patients deviate substantially from the relationship described here, one should be alert to the likelihood that significant damage has occurred outside or in addition to the structures in the medial temporal lobe.
PMCID: PMC3837701  PMID: 24041667
anterograde amnesia; retrograde amnesia; memory; medial temporal lobe
16.  The Functional Architecture for Face-processing Expertise: FMRI Evidence of the Developmental Trajectory of the Core and the Extended Face Systems 
Neuropsychologia  2013;51(13):10.1016/j.neuropsychologia.2013.08.005.
Expertise in processing faces is a cornerstone of human social interaction. However, the developmental course of many key brain regions supporting face preferential processing in the human brain remains undefined. Here, we present findings from an FMRI study using a simple viewing paradigm of faces and objects in a continuous age sample covering the age range from 6 years through adulthood. These findings are the first to use such a sample paired with whole-brain FMRI analyses to investigate development within the core and extended face networks across the developmental spectrum from middle childhood to adulthood. We found evidence, albeit modest, for a developmental trend in the volume of the right fusiform face area (rFFA) but no developmental change in the intensity of activation. From a spatial perspective, the middle portion of the right fusiform gyrus most commonly found in adult studies of face processing was increasingly likely to be included in the FFA as age increased to adulthood. Outside of the FFA, the most striking finding was that children hyperactivated nearly every aspect of the extended face system relative to adults, including the amygdala, anterior temporal pole, insula, inferior frontal gyrus, anterior cingulate gyrus, and parietal cortex. Overall, the findings suggest that development is best characterized by increasing modulation of face-sensitive regions throughout the brain to engage only those systems necessary for task requirements.
PMCID: PMC3825803  PMID: 23948645
Functional MRI; Brain Development; Fusiform Face Area: Face Processing Expertise; Core and Extended Face Networks
17.  Early visual ERP sensitivity to the species and animacy of faces 
Neuropsychologia  2013;51(13):10.1016/j.neuropsychologia.2013.09.014.
Assessing the agency of potential actors in the visual world is a critically important aspect of social cognition. Adult observers are generally capable of distinguishing real faces from artificial faces (even allowing for recent advances in graphics technology and motion capture); even small deviations from real facial appearance can lead to profound effects on face recognition. Presently, we examined how early components ofvisual event-related potentials (ERPs) are affected by the “life” in human faces and animal faces. We presented participants with real and artificial faces of humans and dogs, and analyzed the response properties of the P100 and the N170 as a function of stimulus appearance and task (species categorization vs. animacy categorization). The P100 exhibited sensitivity to face species and animacy. We found that the N170's differential responses to human faces vs. dog faces depended on the task participants’ performed. Also, the effect of species was only evident for real faces of humans and dogs, failing to obtain with artificial faces. These results suggest that face animacy does modulate early components of visual ERPs – the N170 is not merely a crude face detector, but reflects the tuning of the visual system to natural face appearance.
PMCID: PMC3865704  PMID: 24041668
Face perception; event-related potentials; social cognition
18.  Age-related differences in agenda-driven monitoring of format and task information 
Neuropsychologia  2013;51(12):2427-2441.
Age-related source memory deficits may arise, in part, from changes in the agenda-driven processes that control what features of events are relevant during remembering. Using fMRI, we compared young and older adults on tests assessing source memory for format (picture, word) or encoding task (self-, other-referential), as well as on old-new recognition. Behaviorally, relative to old-new recognition, older adults showed disproportionate and equivalent deficits on both source tests compared to young adults. At encoding, both age groups showed expected activation associated with format in posterior visual processing areas, and with task in medial prefrontal cortex. At test, the groups showed similar selective, agenda-related activity in these representational areas. There were, however, marked age differences in the activity of control regions in lateral and medial prefrontal cortex and lateral parietal cortex. Results of correlation analyses were consistent with the idea that young adults had greater trial-by-trial agenda-driven modulation of activity (i.e., greater selectivity) than did older adults in representational regions. Thus, under selective remembering conditions where older adults showed clear differential regional activity in representational areas depending on type of test, they also showed evidence of disrupted frontal and parietal function and reduced item-by-item modulation of test-appropriate features. This pattern of results is consistent with an age-related deficit in the engagement of selective reflective attention.
PMCID: PMC3664244  PMID: 23357375
source memory; aging; reflective attention; agenda-driven processing
19.  A task to assess behavioral pattern separation (BPS) in humans: Data from healthy aging and mild cognitive impairment 
Neuropsychologia  2013;51(12):2442-2449.
Changes in memory performance are one of the hallmark symptoms of mild cognitive impairment and are affected by healthy aging as well. Pattern separation, which refers to the process of orthogonalizing overlapping inputs into distinct memory representations, may be a sensitive marker of these memory changes. Here, we describe a paradigm, the Behavioral Pattern Separation Task – Object Version (BPS-O task), which reveals age-related changes in pattern separation performance. Specifically, we report an age-related decline in pattern separation in healthy adults, ranging from ages 20–89. When we classify those individuals ages 60 and older into two groups, Aged Unimpaired (AU) and Aged Impaired (AI) based on their delayed word recall performance, we observe impairments in pattern separation performance in the Impaired group, but no overall impairment in recognition performance. In contrast, those individuals diagnosed with mild cognitive impairment demonstrate worse performance than age-matched controls in both pattern separation and recognition memory performance. Therefore, the BPS-O task provides a sensitive measure for observing changes in memory performance across the lifespan and may be useful for the early detection of memory impairments that may provide an early signal of later development to mild cognitive impairment.
PMCID: PMC3675184  PMID: 23313292
healthy aging; pattern separation; dentate gyrus (DG); MCI
20.  Moderate Levels of Activation Lead to Forgetting In the Think/No-Think Paradigm 
Neuropsychologia  2013;51(12):2371-2388.
Using the think/no-think paradigm (Anderson & Green, 2001), researchers have found that suppressing retrieval of a memory (in the presence of a strong retrieval cue) can make it harder to retrieve that memory on a subsequent test. This effect has been replicated numerous times, but the size of the effect is highly variable. Also, it is unclear from a neural mechanistic standpoint why preventing recall of a memory now should impair your ability to recall that memory later. Here, we address both of these puzzles using the idea, derived from computational modeling and studies of synaptic plasticity, that the function relating memory activation to learning is U-shaped, such that moderate levels of memory activation lead to weakening of the memory and higher levels of activation lead to strengthening. According to this view, forgetting effects in the think/no-think paradigm occur when the suppressed item activates moderately during the suppression attempt, leading to weakening; the effect is variable because sometimes the suppressed item activates strongly (leading to strengthening) and sometimes it does not activate at all (in which case no learning takes place). To test this hypothesis, we ran a think/no-think experiment where participants learned word-picture pairs; we used pattern classifiers, applied to fMRI data, to measure how strongly the picture associates were activating when participants were trying not to retrieve these associates, and we used a novel Bayesian curve-fitting procedure to relate this covert neural measure of retrieval to performance on a later memory test. In keeping with our hypothesis, the curve-fitting procedure revealed a nonmonotonic relationship between memory activation (as measured by the classifier) and subsequent memory, whereby moderate levels of activation of the to-be-suppressed item led to diminished performance on the final memory test, and higher levels of activation led to enhanced performance on the final test.
PMCID: PMC3702674  PMID: 23499722
fMRI; memory; inhibition; plasticity
21.  Medial Temporal Lobe Contributions to Cued Retrieval of Items and Contexts 
Neuropsychologia  2013;51(12):2322-2332.
Several models have proposed that different regions of the medial temporal lobes contribute to different aspects of episodic memory. For instance, according to one view, the perirhinal cortex represents specific items, parahippocampal cortex represents information regarding the context in which these items were encountered, and the hippocampus represents item-context bindings. Here, we used event-related functional magnetic resonance imaging (fMRI) to test a specific prediction of this model – namely, that successful retrieval of items from context cues will elicit perirhinal recruitment and that successful retrieval of contexts from item cues will elicit parahippocampal cortex recruitment. Retrieval of the bound representation in either case was expected to elicit hippocampal engagement. To test these predictions, we had participants study several item-context pairs (i.e., pictures of objects and scenes, respectively), and then had them attempt to recall items from associated context cues and contexts from associated item cues during a scanned retrieval session. Results based on both univariate and multivariate analyses confirmed a role for hippocampus in content-general relational memory retrieval, and a role for parahippocampal cortex in successful retrieval of contexts from item cues. However, we also found that activity differences in perirhinal cortex were correlated with successful cued recall for both items and contexts. These findings provide partial support for the above predictions and are discussed with respect to several models of medial temporal lobe function.
PMCID: PMC3737273  PMID: 23466350
Episodic Memory; Retrieval; Medial Temporal Lobe; Perirhinal Cortex; Parahippocampal Cortex; Hippocampus
22.  Human Hippocampal Increases in Low-Frequency Power during Associative Prediction Violations 
Neuropsychologia  2013;51(12):2344-2351.
Environmental cues often trigger memories of past events (associative retrieval), and these memories are a form of prediction about imminent experience. Learning is driven by the detection of prediction violations, when the past and present diverge. Using intracranial electroencephalography (iEEG), we show that associative prediction violations elicit increased low-frequency power (in the slow-theta range) in human hippocampus, that this low-frequency power increase is modulated by whether conditions allow predictions to be generated, that the increase rapidly onsets after the moment of violation, and that changes in low-frequency power are not present in adjacent perirhinal cortex. These data suggest that associative mismatch is computed within hippocampus when cues trigger predictions that are violated by imminent experience.
PMCID: PMC3805697  PMID: 23571081
hippocampus; associative memory; prediction violation; intracranial EEG; novelty; mismatch
23.  Distinct medial temporal contributions to different forms of recognition in amnestic mild cognitive impairment and Alzheimer's disease 
Neuropsychologia  2013;51(12):2450-2461.
The simplest expression of episodic memory is the experience of familiarity, the isolated recognition that something has been encountered previously. Brain structures of the medial temporal lobe (MTL) make essential contributions to episodic memory, but the distinct contributions from each MTL structure to familiarity are debatable. Here we used specialized tests to assess recognition impairments and their relationship to MTL integrity in people with amnestic mild cognitive impairment (aMCI, n=19), people with probable Alzheimer's disease (AD; n=10), and age-matched individuals without any neurological disorder (n=20). Recognition of previously presented silhouette objects was tested in two formats—forced-choice recognition with four concurrent choices (one target and three foils) and yes/no recognition with individually presented targets and foils. Every foil was extremely similar to a corresponding target, such that forced-choice recognition could be based on differential familiarity among the choices, whereas yes/no recognition necessitated additional memory and decision factors. Only yes/no recognition was impaired in the aMCI group, whereas both forced-choice and yes/no recognition were impaired in the AD group. Magnetic resonance imaging showed differential brain atrophy, as MTL volume was reduced in the AD group but not in the aMCI group. Pulsed arterial spin-labeled scans demonstrated that MTL blood flow was abnormally increased in aMCI, which could indicate physiological dysfunction prior to the emergence of significant atrophy. Regression analyses with data from all patients revealed that regional patterns of MTL integrity were differentially related to forced-choice and yes/no recognition. Smaller perirhinal cortex volume was associated with lower forced-choice recognition accuracy, but not with lower yes/no recognition accuracy. Instead, smaller hippocampal volumes were associated with lower yes/no recognition accuracy. In sum, familiarity memory can be specifically assessed using the forced-choice recognition test, it declines later than other MTL-dependent memory functions as AD progresses, and it has distinct anatomical substrates.
PMCID: PMC3805744  PMID: 23831717
familiarity; episodic memory; recognition memory; amnestic mild cognitive impairment; Alzheimer's disease
24.  An fMRI investigation of the cognitive reappraisal of negative memories 
Neuropsychologia  2013;51(12):2389-2400.
Episodic memory retrieval can be influenced by individuals’ current goals, including those that are emotional in nature. Participants underwent an fMRI scan while reappraising, or changing the way they thought about aversive images they had previously encoded, to down-regulate (i.e., decrease), up-regulate (i.e., increase), or maintain the emotional intensity associated with their recall. A conjunction analysis between down- and up-regulation during the entire 12-sec recall period revealed that both commonly activated reappraisal-related regions, particularly in the lateral and medial prefrontal cortex (PFC). However, when we analyzed a reappraisal instruction phase prior to recall and then divided the recall phase into the time when individuals were first searching for their memories and later elaborating on their details, we found that down- and up-regulation engaged greater neural activity at different time points. Up-regulation engaged greater PFC activity than down-regulation or maintenance during the reappraisal instruction phase. In contrast, down-regulation engaged greater lateral PFC activity as images were being searched for and retrieved. Maintaining the emotional intensity associated with the aversive images engaged similar regions to a greater extent than either reappraisal condition as participants elaborated on the details of the images they were holding in mind. Our findings suggest that down- and up-regulation engage similar neural regions during memory retrieval, but differ in the timing of this engagement.
PMCID: PMC3723712  PMID: 23500898
episodic memory; retrieval; emotion; emotion regulation; cognitive reappraisal
25.  Remembering what could have happened: Neural correlates of episodic counterfactual thinking 
Neuropsychologia  2013;51(12):2401-2414.
Recent evidence suggests that our capacities to remember the past and to imagine what might happen in the future largely depend on the same core brain network that includes the middle temporal lobe, the posterior cingulate/retrosplenial cortex, the inferior parietal lobe, the medial prefrontal cortex, and the lateral temporal cortex. However, the extent to which regions of this core brain network are also responsible for our capacity to think about what could have happened in our past, yet did not occur (i.e., episodic counterfactual thinking), is still unknown. The present study examined this issue. Using a variation of the experimental recombination paradigm (Addis et al., 2009), participants were asked both to remember personal past events and to envision alternative outcomes to such events while undergoing functional magnetic resonance imaging. Three sets of analyses were performed on the imaging data in order to investigate two related issues. First, a mean-centered spatiotemporal partial least square (PLS) analysis identified a pattern of brain activity across regions of the core network that was common to episodic memory and episodic counterfactual thinking. Second, a non-rotated PLS analysis identified two different patterns of brain activity for likely and unlikely episodic counterfactual thoughts, with the former showing significant overlap with the set of regions engaged during episodic recollection. Finally, a parametric modulation was conducted to explore the differential engagement of brain regions during counterfactual thinking, revealing that areas such as the parahippocampal gyrus and the right hippocampus were modulated by the subjective likelihood of counterfactual simulations. These results suggest that episodic counterfactual thinking engages regions that form the core brain network, and also that the subjective likelihood of our counterfactual thoughts modulates the engagement of different areas within this set of regions.
PMCID: PMC3919504  PMID: 23376052
Episodic memory; Counterfactual thinking; Imagination; Mental time travel; fMRI; Partial least squares

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