This past year we have continued to focus on a major part of long-term memory, termed semantic memory, that is composed of general information, such as facts, ideas, and the meaning of objects and words. We are particularly interested in characterizing the neural substrate mediating object and word meaning and its role in object perception. We are also interested in understanding how abstract knowledge, such as information about social interactions, is represented. Our studies have shown that information about salient properties of an object - such as what it looks like, how it moves, how it is used, and our affective reaction to it - are stored in our perceptual, action, and emotion systems. As a result, objects belonging to different categories such as animate entities (people, animals) and manmade manipulable objects (tools, utensils) are represented in partially distinct neural circuits. These distributed circuits also underpin our ability to understand more abstract events such as social and mechanical interactions. One of the most robust and oft-replicated findings in cognitive neuroscience is that different regions of ventral temporal cortex respond preferentially to different categories of concrete objects. However, the determinants of this category-related organization remain to be fully established. We, and others, have recently proposed that a major contributing factor to this organization is privileged connectivity from each of these ventral temporal regions to other brain regions that store property information associated with that category. To test this hypothesis, we used fMRI to define category-related brain regions of interest (ROIs) in a large group of subjects. We then used these ROIs in resting-state functional connectivity MRI analyses to explore functional connectivity among these regions. Our results demonstrate that distinct category-preferential regions of ventral temporal cortex show differentially stronger functional connectivity with other regions that have congruent category preference. These findings support the claim that privileged connectivity with other cortical regions provides a powerful constraint on the category-related organization of this region of the brain. In addition to our knowledge of what objects look like, how they move, and how we use them, we often also have strong emotional reactions to them. In collaboration with our colleagues at Duke University, we have engaged in a series of studies on the neural systems associated with acquisition of object-associated fear. Previous studies have documented changes in neural activity in the amygdala and sensory cortices when subjects learn to associate fear with a simple stimulus like a shape or color. However, real-world fears typically involve complex stimuli represented at the category level. As a result, an aversive experience with a particular object may lead one to infer that related instances, or exemplars, of that object category also pose a threat, despite variations in physical form (e.g., generalizing the fear associated with a specific dog, to all dogs). Using fMRI, we examined the effect of category-level representations of threat on human brain activity using the categories of animals and tools as conditioned stimuli. We found that activity in the amygdala and other category-responsive brain regions was modulated by the reinforcement contingency, leading to widespread fear of different exemplars from the reinforced category. Learning to fear animate objects was additionally characterized by enhanced functional coupling between the amygdala and fusiform gyrus. These findings provide novel evidence that aversive learning can modulate category-level representations of object concepts, thereby enabling individuals to express fear to a range of related stimuli. In marked contrast to a negative emotion like fear, other objects are typically associated with pleasurable experiences. A prime example is food. Food advertisements often promote choices that are driven by inferences about the pleasures of eating a particular food. Given the individual and public health consequences of obesity, it is critical to address unanswered questions about the specific neural systems underlying these pleasurable inferences. To address this issue, we used fMRI to measure neural activity when subjects made item-by-item ratings of how pleasant it would be to eat particular food depicted in a photograph. We found that activity in the orbitofrontal cortex was directly modulated by the subject's pleasantness ratings. In addition, we found that a subcortical brain region, the ventral pallidum, was also strongly modulated by the pleasantness ratings. This finding was particularly important because it demonstrated for the first time that a brain region known to be associated with reward in rodents, plays a central role in the moment-to-moment inferences of pleasure that influence our food-related preferences and decisions. Finally, we have used both task-related fMRI and analyses of resting-state functional connectivity to evaluate the origins of individual differences in cognitive strategy during decision-making. In a typical real-world situation that requires a decision, individual differences in strategy often emerge. To explore the neural underpinnings of these strategy differences we adapted a well-studied decision making paradigm, motion direction discrimination, which required subjects to simply decide whether circles on the screen were moving to the left or right. We tested whether strategies emerged from moment-to-moment reconfiguration of functional brain networks involved in decision making with task-evoked fMRI and whether intrinsic properties of functional brain networks, measured at rest with functional connectivity MRI, were associated with strategy use. We found that subjects reliably selected one of two strategies across two days of task performance, either continuously accumulating evidence or waiting for task difficulty to decrease. Importantly, these individual differences in decision strategy were predicted both by the degree of task-evoked activation of decision-related brain regions and by the strength of correlated spontaneous brain activity measured prior to taking part in the motion discrimination task. These results suggest that individual differences in a cognitive strategy can be predicted by individual differences in intrinsic patterns of neural connectivity.

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25
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2015
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U.S. National Institute of Mental Health
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Power, Jonathan D; Plitt, Mark; Gotts, Stephen J et al. (2018) Ridding fMRI data of motion-related influences: Removal of signals with distinct spatial and physical bases in multiecho data. Proc Natl Acad Sci U S A 115:E2105-E2114
Stevens, W Dale; Kravitz, Dwight J; Peng, Cynthia S et al. (2017) Privileged Functional Connectivity between the Visual Word Form Area and the Language System. J Neurosci 37:5288-5297
Power, Jonathan D; Laumann, Timothy O; Plitt, Mark et al. (2017) On Global fMRI Signals and Simulations. Trends Cogn Sci 21:911-913
Avery, Jason A; Gotts, Stephen J; Kerr, Kara L et al. (2017) Convergent gustatory and viscerosensory processing in the human dorsal mid-insula. Hum Brain Mapp 38:2150-2164
Power, Jonathan D; Plitt, Mark; Laumann, Timothy O et al. (2017) Sources and implications of whole-brain fMRI signals in humans. Neuroimage 146:609-625
Mellem, Monika S; Wohltjen, Sophie; Gotts, Stephen J et al. (2017) Intrinsic frequency biases and profiles across human cortex. J Neurophysiol 118:2853-2864
Vattikuti, Shashaank; Thangaraj, Phyllis; Xie, Hua W et al. (2016) Canonical Cortical Circuit Model Explains Rivalry, Intermittent Rivalry, and Rivalry Memory. PLoS Comput Biol 12:e1004903
Martin, Alex (2016) GRAPES-Grounding representations in action, perception, and emotion systems: How object properties and categories are represented in the human brain. Psychon Bull Rev 23:979-90
Mellem, Monika S; Jasmin, Kyle M; Peng, Cynthia et al. (2016) Sentence processing in anterior superior temporal cortex shows a social-emotional bias. Neuropsychologia 89:217-224
Meoded, Avner; Morrissette, Arthur E; Katipally, Rohan et al. (2015) Cerebro-cerebellar connectivity is increased in primary lateral sclerosis. Neuroimage Clin 7:288-96

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