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1.  Parietal Functional Connectivity in Numerical Cognition 
Cerebral Cortex (New York, NY)  2012;23(9):2127-2135.
The parietal cortex is central to numerical cognition. The right parietal region is primarily involved in basic quantity processing, while the left parietal region is additionally involved in precise number processing and numerical operations. Little is known about how the 2 regions interact during numerical cognition. We hypothesized that functional connectivity between the right and left parietal cortex is critical for numerical processing that engages both basic number representation and learned numerical operations. To test this hypothesis, we estimated neural activity using functional magnetic resonance imaging in participants performing numerical and arithmetic processing on dot arrays. We first found task-based functional connectivity between a right parietal seed and the left sensorimotor cortex in all task conditions. As we hypothesized, we found enhanced functional connectivity between this right parietal seed and both the left parietal cortex and neighboring right parietal cortex, particularly during subtraction. The degree of functional connectivity also correlated with behavioral performance across individual participants, while activity within each region did not. These results highlight the role of parietal functional connectivity in numerical processing. They suggest that arithmetic processing depends on crosstalk between and within the parietal cortex and that this crosstalk contributes to one's numerical competence.
doi:10.1093/cercor/bhs193
PMCID: PMC3729197  PMID: 22784605
arithmetic processing; functional connectivity; intraparietal sulcus; numerical cognition
2.  Amygdala response to smoking-cessation messages mediates the effects of serotonin transporter gene variation on quitting 
Neuroimage  2012;60(1):766-773.
The amygdala is critically involved in detecting emotionally salient stimuli and in enhancing memory for emotional information. Growing evidence also suggests that the amygdala plays a crucial role in addiction, perhaps by strengthening associations between emotionally-charged drug cues and drug-seeking behavior. In the current study, by integrating functional MRI (fMRI), genetics, and outcome data from a large group of smokers who completed a smoking-cessation intervention and attempted to quit, we show that the amygdala also plays a role in quitting. Specifically, we demonstrate that the amygdala response to smoking-cessation messages in smokers trying to quit is a predictor of their post-intervention quitting outcome. We further show that the amygdala response is modulated by genetic variation in the serotonin transporter and mediates the impact of this genetic variation on quitting. These results point to a gene-brain-behavior pathway relevant to smoking cessation, and add to our understanding of the role of the amygdala in nicotine addiction.
doi:10.1016/j.neuroimage.2011.12.064
PMCID: PMC3288964  PMID: 22245645
Amygdala; smoking cessation; serotonin transporter gene; fMRI; imaging genetics
3.  Correlation and heritability in neuroimaging datasets: A spatial decomposition approach with application to an fMRI study of twins 
NeuroImage  2011;59(2):1132-1142.
Advances in modern neuroimaging in combination with behavioral genetics have allowed neuroscientists to investigate how genetic and environmental factors shape human brain structure and function. Estimating the heritability of brain structure and function via twin studies has become one of the major approaches in studying the genetics of the brain. In a classical twin study, heritability is estimated by computing genetic and phenotypic variation based on the similarity of monozygotic and dizygotic twins. However, heritability has traditionally been measured for univariate, scalar traits, and it is challenging to assess the heritability of a spatial process, such as a pattern of neural activity. In this work, we develop a statistical method to estimate phenotypic variance and covariance at each location in a spatial process, which in turn can be used to estimate the heritability of a spatial dataset. The method is based on a dimensionally-reduced model of spatial variation in paired images, in which adjusted least squares estimates can be used to estimate the key model parameters. The advantage of the proposed method compared to conventional methods such as a voxelwise or mean-ROI approaches is demonstrated in both a simulation study and a real data study assessing genetic influence on patterns of brain activity in the visual and motor cortices in response to a simple visuomotor task.
doi:10.1016/j.neuroimage.2011.06.066
PMCID: PMC3219840  PMID: 21763433
Heritability; Intraclass Correlation; Twin Study; Spatial Analysis; Genetics
4.  Task Difficulty Modulates the Impact of Emotional Stimuli on Neural Response in Cognitive-Control Regions 
Both heightened reactivity to emotional stimuli and impaired cognitive control are key aspects of depression, anxiety, and addiction. But the impact of emotion on cognitive-control processes, and the factors that modulate this impact, are still not well understood. We examined the effects of threat and reward distracters on the neural correlates of cognitive control using functional MRI (fMRI) and the Multi-Source Interference Task (MSIT). Behaviorally, subjects were slower and less accurate on the more demanding incongruent trials compared to the easier congruent trials. In addition, both threat and reward distracters significantly impaired the speed of responding on incongruent trials relative to the no-distracter condition. At the neural level, we used the incongruent – congruent contrast to functionally define four cognitive-control regions of interest (ROIs): anterior cingulate cortex (ACC), left and right inferior frontal gyrus (IFG)/insula, and right dorsolateral prefrontal cortex (DLPFC). A repeated-measures analysis of variance on the extracted contrast values in these ROIs indicated a significant interaction of stimulus salience and task difficulty on the neural response in cognitive-control regions. Specifically, threat distracters significantly decreased the response in cognitive-control regions on incongruent trials, whereas they significantly increased that response on congruent trials, relative to the no-distracter condition. Exploratory analyses of the amygdala response showed a similar interaction of stimulus salience and task difficulty: threat distracters significantly decreased the amygdala response only on incongruent trials. Overall, our results suggest that the impact of emotional distracters on the neural response in cognitive-control regions as well as in the amygdala is modulated by task difficulty, and add to our understanding of the factors that determine whether emotion enhances or impairs cognition.
doi:10.3389/fpsyg.2012.00345
PMCID: PMC3464044  PMID: 23060828
emotion; cognitive control; executive function; emotion-cognition interactions; fMRI; ACC; DLPFC; IFG
5.  Neural Broadening or Neural Attenuation? Investigating Age-Related Dedifferentiation in the Face Network in a Large Lifespan Sample 
Previous studies have found that cortical responses to different stimuli become less distinctive as people get older. This age-related dedifferentiation may reflect the broadening of the tuning curves of category-selective neurons (broadening hypothesis) or it may be due to decreased activation of category-selective neurons (attenuation hypothesis). In this study, we evaluated these hypotheses in the context of the face-selective neural network. Over 300 participants, ranging in age from 20 to 89 years, viewed images of faces, houses, and control stimuli in a functional magnetic resonance imaging session. Regions within the core face network and extended face network were identified in individual subjects. Activation in many of these regions became significantly less face-selective with age, confirming previous reports of age-related dedifferentiation. Consistent with the broadening hypothesis, this dedifferentiation in the fusiform face area (FFA) was driven by increased activation to houses. In contrast, dedifferentiation in the extended face network was driven by decreased activation to faces, consistent with the attenuation hypothesis. These results suggest that age-related dedifferentiation reflects distinct processes in different brain areas. More specifically, dedifferentiation in FFA activity may be due to broadening of the tuning curves for face-selective neurons, while dedifferentiation in the extended face network reflects reduced face- or emotion-selective activity.
doi:10.1523/JNEUROSCI.4494-11.2012
PMCID: PMC3361757  PMID: 22323727
6.  Neural Dissociation of Number from Letter Recognition and Its Relationship to Parietal Numerical Processing 
The visual recognition of letters dissociates from the recognition of numbers at both the behavioral and neural level. In this article, using fMRI, we investigate whether the visual recognition of numbers dissociates from letters, thereby establishing a double dissociation. In Experiment 1, participants viewed strings of consonants and Arabic numerals. We found that letters activated the left midfusiform and inferior temporal gyri more than numbers, replicating previous studies, whereas numbers activated a right lateral occipital area more than letters at the group level. Because the distinction between letters and numbers is culturally defined and relatively arbitrary, this double dissociation provides some of the strongest evidence to date that a neural dissociation can emerge as a result of experience. We then investigated a potential source of the observed neural dissociation. Specifically, we tested the hypothesis that lateralization of visual number recognition depends on lateralization of higher-order numerical processing. In Experiment 2, the same participants performed addition, subtraction, and counting on arrays of nonsymbolic stimuli varying in numerosity, which produced neural activity in and around the intraparietal sulcus, a region associated with higher-order numerical processing. We found that individual differences in the lateralization of number activity in visual cortex could be explained by individual differences in the lateralization of numerical processing in parietal cortex, suggesting a functional relationship between the two regions. Together, these results demonstrate a neural double dissociation between letter and number recognition and suggest that higher-level numerical processing in parietal cortex may influence the neural organization of number processing in visual cortex.
doi:10.1162/jocn_a_00085
PMCID: PMC3357212  PMID: 21736455
7.  Both left and right posterior parietal activations contribute to compensatory processes in normal aging 
Neuropsychologia  2011;50(1):55-66.
Older adults often exhibit greater brain activation in prefrontal cortex compared to younger adults, and there is some evidence that this increased activation compensates for age-related neural degradation that would otherwise adversely affect cognitive performance. Less is known about aging and compensatory recruitment in the parietal cortex. In this event-related functional magnetic resonance imaging study, we presented healthy young and old participants with two Stroop-like tasks (number magnitude and physical size). In young, the number magnitude task activated right parietal cortex and the physical size task activated left parietal cortex. In older adults, we observed contralateral parietal recruitment that depended on the task: in the number magnitude task older participants recruited left posterior parietal cortex (in addition to the right parietal activity observed in young) while in the physical size task they recruited right (in addition to left) posterior parietal cortex. In both cases, the additional parietal activity was associated with better performance suggesting that it played a compensatory role. Older adults also recruited left prefrontal cortex during both tasks and this common activation was also associated with better performance. The results provide evidence for task-specific compensatory recruitment in parietal cortex as well as task-independent compensatory recruitment in prefrontal cortex in normal aging.
doi:10.1016/j.neuropsychologia.2011.10.022
PMCID: PMC3355662  PMID: 22063904
Age-related compensation; Event-related fMRI; Interference resolution; Posterior parietal cortex; Prefrontal cortex
8.  Age differences in neural distinctiveness revealed by multi-voxel pattern analysis 
NeuroImage  2010;56(2):736-743.
Current theories of cognitive aging argue that neural representations become less distinctive in old age, a phenomenon known as dedifferentiation. The present study used multi-voxel pattern analysis (MVPA) to measure age differences in the distinctiveness of distributed patterns of neural activation evoked by different categories of visual images. We found that neural activation patterns within the ventral visual cortex were less distinctive among older adults. Further, we report that age differences in neural distinctiveness extend beyond the ventral visual cortex: older adults also showed decreased distinctiveness in early visual cortex, inferior parietal cortex, and medial and lateral prefrontal cortex. Neural distinctiveness scores in early and late visual areas were highly correlated, suggesting shared mechanisms of age-related decline. Finally, we investigated whether older adults can compensate for altered processing in visual cortex by encoding stimulus information across larger numbers of voxels within the visual cortex or in regions outside visual cortex. We found no evidence that older adults can increase the distinctiveness of distributed activation patterns, either within or beyond the visual cortex. Our results have important implications for theories of cognitive aging and highlight the value of MVPA to the study of neural coding in the aging brain.
doi:10.1016/j.neuroimage.2010.04.267
PMCID: PMC2962693  PMID: 20451629
aging; fMRI; MVPA; dedifferentiation; compensation; ventral visual cortex
9.  Influence of Threat and Serotonin Transporter Genotype on Interference Effects 
Emotion-cognition interactions are critical in goal-directed behavior and may be disrupted in psychopathology. Growing evidence also suggests that emotion-cognition interactions are modulated by genetic variation, including genetic variation in the serotonin system. The goal of the current study was to examine the impact of threat-related distracters and serotonin transporter promoter polymorphism (5-HTTLPR/rs25531) on cognitive task performance in healthy females. Using a novel threat-distracter version of the Multi-Source Interference Task specifically designed to probe emotion-cognition interactions, we demonstrate a robust and temporally dynamic modulation of cognitive interference effects by threat-related distracters relative to other distracter types and relative to no-distracter condition. We further show that threat-related distracters have dissociable and opposite effects on cognitive task performance in easy and difficult task conditions, operationalized as the level of response interference that has to be surmounted to produce a correct response. Finally, we present evidence that the 5-HTTLPR/rs25531 genotype in females modulates susceptibility to cognitive interference in a global fashion, across all distracter conditions, and irrespective of the emotional salience of distracters, rather than specifically in the presence of threat-related distracters. Taken together, these results add to our understanding of the processes through which threat-related distracters affect cognitive processing, and have implications for our understanding of disorders in which threat signals have a detrimental effect on cognition, including depression and anxiety disorders.
doi:10.3389/fpsyg.2012.00139
PMCID: PMC3349301  PMID: 22590463
cognition; emotion; interference resolution; threat; serotonin transporter gene; 5-HTTLPR; MSIT
10.  Investigating Unique Environmental Contributions to the Neural Representation of Written Words: A Monozygotic Twin Study 
PLoS ONE  2012;7(2):e31512.
The visual word form area (VWFA) is a region of left inferior occipitotemporal cortex that is critically involved in visual word recognition. Previous studies have investigated whether and how experience shapes the functional characteristics of VWFA by comparing neural response magnitude in response to words and nonwords. Conflicting results have been obtained, however, perhaps because response magnitude can be influenced by other factors such as attention. In this study, we measured neural activity in monozygotic twins, using functional magnetic resonance imaging. This allowed us to quantify differences in unique environmental contributions to neural activation evoked by words, pseudowords, consonant strings, and false fonts in the VWFA and striate cortex. The results demonstrate significantly greater effects of unique environment in the word and pseudoword conditions compared to the consonant string and false font conditions both in VWFA and in left striate cortex. These findings provide direct evidence for environmental contributions to the neural architecture for reading, and suggest that learning phonology and/or orthographic patterns plays the biggest role in shaping that architecture.
doi:10.1371/journal.pone.0031512
PMCID: PMC3275550  PMID: 22347490
11.  Age-Related Neural Dedifferentiation in the Motor System 
PLoS ONE  2011;6(12):e29411.
Recent neuroimaging studies using multi-voxel pattern analysis (MVPA) show that distributed patterns of brain activation elicited by different visual stimuli are less distinctive in older adults than in young adults. However, less is known about the effects of aging on the neural representation of movement. The present study used MVPA to compare the distinctiveness of motor representations in young and older adults. We also investigated the contributions of brain structure to age differences in the distinctiveness of motor representations. We found that neural distinctiveness was reduced in older adults throughout the motor control network. Although aging was also associated with decreased gray matter volume in these regions, age differences in motor distinctiveness remained significant after controlling for gray matter volume. Our results suggest that age-related neural dedifferentiation is not restricted to sensory perception and is instead a more general feature of the aging brain.
doi:10.1371/journal.pone.0029411
PMCID: PMC3245287  PMID: 22216274
12.  A symbolic/subsymbolic interface protocol for cognitive modeling 
Researchers studying complex cognition have grown increasingly interested in mapping symbolic cognitive architectures onto subsymbolic brain models. Such a mapping seems essential for understanding cognition under all but the most extreme viewpoints (namely, that cognition consists exclusively of digitally implemented rules; or instead, involves no rules whatsoever). Making this mapping reduces to specifying an interface between symbolic and subsymbolic descriptions of brain activity. To that end, we propose parameterization techniques for building cognitive models as programmable, structured, recurrent neural networks. Feedback strength in these models determines whether their components implement classically subsymbolic neural network functions (e.g., pattern recognition), or instead, logical rules and digital memory. These techniques support the implementation of limited production systems. Though inherently sequential and symbolic, these neural production systems can exploit principles of parallel, analog processing from decision-making models in psychology and neuroscience to explain the effects of brain damage on problem solving behavior.
doi:10.1093/jigpal/jzp046
PMCID: PMC2919065  PMID: 20711520
problem solving; production system; neural network; diffusion; decision making; symbolic; subsymbolic
13.  Self-related neural response to tailored smoking-cessation messages predicts quitting 
Nature neuroscience  2011;14(4):426-427.
Although tailored health interventions can be more effective in eliciting positive behavior change then generic interventions, the underlying neural mechanisms are not yet understood. Ninety-one smokers participated in a functional magnetic resonance imaging (fMRI) session and a tailored smoking-cessation program. We found that increases in activations in self-related processing regions, particularly dorsomedial prefrontal cortex, to tailored messages predicted quitting during a 4-month follow-up.
doi:10.1038/nn.2761
PMCID: PMC3109081  PMID: 21358641
14.  Evaluating Functional Localizers: The Case of the FFA 
NeuroImage  2009;50(1):56-71.
Functional localizers are routinely used in neuroimaging studies to test hypotheses about the function of specific brain areas. The specific tasks and stimuli used to localize particular regions vary widely from study to study even when the same cortical region is targeted. Thus, it is important to ask whether task and stimulus changes lead to differences in localization or whether localization procedures are largely immune to differences in tasks and contrasting stimuli. We present two experiments and a literature review that explore whether face localizer tasks yield differential localization in the fusiform gyrus as a function of task and contrasting stimuli. We tested standard localization tasks---passive viewing, 1-back, and 2-back memory tests---and did not find differences in localization based on task. We did, however, find differences in the extent, strength and patterns/reliabilities of the activation in the fusiform gyrus based on comparison stimuli (faces vs. houses compared to faces vs. scrambled stimuli).
doi:10.1016/j.neuroimage.2009.12.024
PMCID: PMC2825676  PMID: 20025980
15.  Neural specificity predicts fluid processing ability in older adults 
We investigated whether individual differences in neural specificity—the distinctiveness of different neural representations—could explain individual differences in cognitive performance in older adults. Neural specificity was estimated based on how accurately multivariate pattern analysis identified neural activation patterns associated with specific experimental conditions. Neural specificity calculated from a same-different task on two categories of visual stimuli (faces and houses) significantly predicted performance on a range of fluid processing behavioral tasks (dot-comparison, digit-symbol, Trails-A, Trails-B, verbal-fluency) in older adults, whereas it did not correlate with a measure of crystallized knowledge (Shipley-vocabulary). In addition, the neural specificity measure accounted for thirty percent of the variance in a composite measure of fluid processing ability. These results are consistent with the hypothesis that loss of neural specificity, or dedifferentiation, contributes to reduced fluid processing ability in old age.
doi:10.1523/JNEUROSCI.0853-10.2010
PMCID: PMC2913723  PMID: 20610760
16.  Neural Responses to Elements of a Web-Based Smoking Cessation Program 
An increasing number of smokers are obtaining information from the web to help them quit smoking. In this study, we examined how smokers process different types of messages similar to those from a web-based smoking cessation program: personalization/feedback (“Jane, you are a 23-year old female smoker”), motivational (“If you quit smoking, you could save $1200 a year”), and instructional (“When you feel angry, talk to someone instead of smoking”) messages. Using functional magnetic resonance imaging, smokers were exposed to the messages. On a later session, participants completed an online tailored smoking cessation program and started on a 10-week course of nicotine patch. Results show that participants indeed process the messages differently, activating brain regions associated with self-related processing (personalization/feedback), anticipated reward processing (motivational messages) and rules processing (instructional messages). This research is relevant for advancing web-based tailored interventions for substance use.
PMCID: PMC2892852  PMID: 19592758
Addiction; substance abuse; smoking; internet; neuroimaging
17.  Attention enhances the neural processing of relevant features and suppresses the processing of irrelevant features in humans: An fMRI study of the Stroop task 
We present a functional MRI experiment investigating the neural basis of feature-based attention in humans using the Stroop task. Cortical areas specifically involved in color processing and word reading were first identified in individual participants using independent tests. These areas were then probed during the Stroop task (in which participants must selectively attend to the font color of a word while ignoring the word itself). We found that activation in functionally-defined color areas increased during the task relative to a neutral color-naming task while activation in functionally-defined word areas decreased. These results are consistent with a biased competition model of feature-based attention in which the processing of attended features is enhanced and the processing of ignored features is suppressed.
doi:10.1523/JNEUROSCI.1026-08.2008
PMCID: PMC2659668  PMID: 19091969
attention; Stroop task; feature-based; functional MRI; enhancement; suppression
18.  Age Differences in Default Mode Activity on Easy and Difficult Spatial Judgment Tasks 
The default network is a system of brain areas that are engaged when the mind is not involved in goal-directed activity. Most previous studies of age-related changes in default mode processing have used verbal tasks. We studied non-verbal spatial tasks that vary in difficulty. We presented old and young participants with two spatial judgment tasks: an easy categorical judgment and a more demanding coordinate judgment. We report that (a) Older adults show markedly less default network modulation than young on the demanding spatial task, but there is age equivalence on the easy task; (b) This Age × Task interaction is restricted to the default network: Brain areas that are deactivated by the tasks, but that are outside the default network, show no interaction; (c) Young adults exhibit significantly stronger functional connectivity among posterior regions of the default network compared with older adults, whereas older adults exhibit stronger connectivity between medial prefrontal cortex and other sites; and (d) The relationship of default activity to reaction time performance on the spatial tasks is mediated by age: in old adults, those who deactivate the default network most also perform best, whereas the opposite is true in younger adults. These results extend the findings of age-related changes in default mode processing and connectivity to visuo-spatial tasks and demonstrate that the results are specific to the default network.
doi:10.3389/neuro.09.075.2009
PMCID: PMC2814559  PMID: 20126437
default mode; deactivation; aging brain; spatial judgment; parietal cortex; connectivity; fMRI
19.  Cerebral aging: integration of brain and behavioral models of cognitive function 
There are substantial declines in behavioral measures of cognitive function with age, including decreased function of executive processes and long-term memory. There is also evidence that, with age, there is a decrease in brain volume, particularly in the frontal cortex. When young and older adults perform cognitive tasks that depend heavily on frontal function, neuroimaging evidence indicates that older adults recruit additional brain regions in order to perform the tasks. This additional neural recruitment is termed “dedifferentiation,” and can take multiple forms. This recruitment of additional neural tissue with age to perform cognitive tasks was not reflected in the behavioral literature, and suggests that there is more plasticity in the ability to organize brain function than was previously suspected. We review both behavioral and neuroscience perspectives on cognitive aging, and then connect the findings in the two areas. From this integration, we suggest important unresolved questions and directions for future research.
PMCID: PMC3181659  PMID: 22034448
aging; cognition; compensation; dedifferentiation; executive function; memory; neuroimaging; plasticity; prefrontal cortex; slowing

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