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Significant Sleep facilitates both long-term episodic memory consolidation and short-term working memory functioning. However, the mechanism by which the sleeping brain performs both complex feats and which sleep features are associated with these processes remain unclear. Using a pharmacological approach, we demonstrate that long-term and working memory are served by distinct offline neural mechanisms and that these mechanisms are mutually antagonistic. We propose a sleep switch model in which the brain toggles between the two memory processes via a complex interaction at the synaptic, systems, and mechanistic level with implications for research on cognitive disturbances observed in neurodegenerative disorders such as Alzheimer’s and Parkinson's disease, both of which involve the decline of sleep., We provide evidence that human sleep is a competitive arena in which cognitive domains vie for limited resources. Using pharmacology and effective connectivity analysis, we demonstrate that long-term memory and working memory are served by distinct offline neural mechanisms that are mutually antagonistic. Specifically, we administered zolpidem to increase central sigma activity and demonstrated targeted suppression of autonomic vagal activity. With effective connectivity, we determined the central activity has greater causal influence over autonomic activity, and the magnitude of this influence during sleep produced a behavioral trade-off between offline long-term and working memory processing. These findings suggest a sleep switch mechanism that toggles between central sigma-dependent long-term memory and autonomic vagal-dependent working memory processing.

Significance How bodily arousal states influence decision-making has been a central question in psychology, but the neural mechanisms are unclear. We recorded heart rate (HR), a measure of bodily arousal, while simultaneously monitoring neural activity in orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) of macaques making reward-guided decisions. In intact macaques, higher HR was associated with shorter reaction times. Concurrently, the activity of a set of neurons in OFC and dACC selectively encoded HR. Following amygdala lesions, HR generally increased, and now the relationship between HR and reaction times was altered. At the neural level, the balance of encoding in dACC shifted toward signaling HR, suggesting a specific mechanism through which bodily arousal influences decision-making., Decision-making and representations of arousal are intimately linked. Behavioral investigations have classically shown that either too little or too much bodily arousal is detrimental to decision-making, indicating that there is an inverted “U” relationship between bodily arousal and performance. How these processes interact at the level of single neurons as well as the neural circuits involved are unclear. Here we recorded neural activity from orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) of macaque monkeys while they made reward-guided decisions. Heart rate (HR) was also recorded and used as a proxy for bodily arousal. Recordings were made both before and after subjects received excitotoxic lesions of the bilateral amygdala. In intact monkeys, higher HR facilitated reaction times (RTs). Concurrently, a set of neurons in OFC and dACC selectively encoded trial-by-trial variations in HR independent of reward value. After amygdala lesions, HR increased, and the relationship between HR and RTs was altered. Concurrent with this change, there was an increase in the proportion of dACC neurons encoding HR. Applying a population-coding analysis, we show that after bilateral amygdala lesions, the balance of encoding in dACC is skewed away from signaling either reward value or choice direction toward HR coding around the time that choices are made. Taken together, the present results provide insight into how bodily arousal and decision-making are signaled in frontal cortex.

Significance The widespread use of population-average cortical parcellations has provided important insights into broad properties of human brain organization. However, the size, location, and spatial arrangement of regions comprising functional brain networks can vary substantially across individuals. Here, we demonstrate considerable heritability in both the size and spatial organization of individual-specific network topography across cortex. Genetic factors had a regionally variable influence on brain organization, such that heritability in network size, but not topography, was greater in unimodal relative to heteromodal cortices. These data suggest individual-specific network parcellations may provide an avenue to understand the genetic basis of variation in human cognition and behavior., Human cortex is patterned by a complex and interdigitated web of large-scale functional networks. Recent methodological breakthroughs reveal variation in the size, shape, and spatial topography of cortical networks across individuals. While spatial network organization emerges across development, is stable over time, and is predictive of behavior, it is not yet clear to what extent genetic factors underlie interindividual differences in network topography. Here, leveraging a nonlinear multidimensional estimation of heritability, we provide evidence that individual variability in the size and topographic organization of cortical networks are under genetic control. Using twin and family data from the Human Connectome Project (n = 1,023), we find increased variability and reduced heritability in the size of heteromodal association networks (h2: M = 0.34, SD = 0.070), relative to unimodal sensory/motor cortex (h2: M = 0.40, SD = 0.097). We then demonstrate that the spatial layout of cortical networks is influenced by genetics, using our multidimensional estimation of heritability (h2-multi; M = 0.14, SD = 0.015). However, topographic heritability did not differ between heteromodal and unimodal networks. Genetic factors had a regionally variable influence on brain organization, such that the heritability of network topography was greatest in prefrontal, precuneus, and posterior parietal cortex. Taken together, these data are consistent with relaxed genetic control of association cortices relative to primary sensory/motor regions and have implications for understanding population-level variability in brain functioning, guiding both individualized prediction and the interpretation of analyses that integrate genetics and neuroimaging.

Significance A birth-to-adulthood study tested the effects of maternal–newborn contact and synchronous caregiving on the social processing brain in human adults. For two decades, we followed preterm and full-term neonates, who received or lacked initial maternal bodily contact, repeatedly observing mother–child social synchrony. We measured the brain basis of affect-specific empathy in young adulthood to pinpoint regions sensitive to others’ distinct emotions. Maternal–newborn contact enhanced social synchrony across development, which, in turn, predicted amygdalar and insular sensitivity to emotion-specific empathy. Findings demonstrate the long-term effects of maternal caregiving in humans, similar to their role in other mammals, particularly in tuning core regions implicated in salience detection, simulation, and interoception that sustain empathy and human attachment., Mammalian young are born with immature brain and rely on the mother’s body and caregiving behavior for maturation of neurobiological systems that sustain adult sociality. While research in animal models indicated the long-term effects of maternal contact and caregiving on the adult brain, little is known about the effects of maternal–newborn contact and parenting behavior on social brain functioning in human adults. We followed human neonates, including premature infants who initially lacked or received maternal–newborn skin-to-skin contact and full-term controls, from birth to adulthood, repeatedly observing mother–child social synchrony at key developmental nodes. We tested the brain basis of affect-specific empathy in young adulthood and utilized multivariate techniques to distinguish brain regions sensitive to others’ distinct emotions from those globally activated by the empathy task. The amygdala, insula, temporal pole (TP), and ventromedial prefrontal cortex (VMPFC) showed high sensitivity to others’ distinct emotions. Provision of maternal–newborn contact enhanced social synchrony across development from infancy and up until adulthood. The experience of synchrony, in turn, predicted the brain’s sensitivity to emotion-specific empathy in the amygdala and insula, core structures of the social brain. Social synchrony linked with greater empathic understanding in adolescence, which was longitudinally associated with higher neural sensitivity to emotion-specific empathy in TP and VMPFC. Findings demonstrate the centrality of synchronous caregiving, by which infants practice the detection and sharing of others’ affective states, for tuning the human social brain, particularly in regions implicated in salience detection, interoception, and mentalization that underpin affect sharing and human attachment.

Significance A tennis player planning the next stroke has to consider various pieces of information: the type of stroke, the trajectory of the incoming ball, and where to hit the ball. Here, by decoding electroencephalography signals while participants executed simple, rule-based actions, we found that such different, actionrelevant aspects are integrated within a unified, conjunctive representation rather than being processed in a piecemeal manner. Furthermore, the strength of conjunctive representations is a highly robust predictor of how quickly actions are executed. Human-level theories and recent single-cell evidence from animal models suggest that conjunctive representations are a necessary condition for successful action selection. Our results provide direct evidence in humans that is consistent with this hypothesis., People can use abstract rules to flexibly configure and select actions for specific situations, yet how exactly rules shape actions toward specific sensory and/or motor requirements remains unclear. Both research from animal models and human-level theories of action control point to the role of highly integrated, conjunctive representations, sometimes referred to as event files. These representations are thought to combine rules with other, goal-relevant sensory and motor features in a nonlinear manner and represent a necessary condition for action selection. However, so far, no methods exist to track such representations in humans during action selection with adequate temporal resolution. Here, we applied time-resolved representational similarity analysis to the spectral-temporal profiles of electroencephalography signals while participants performed a cued, rule-based action selection task. In two experiments, we found that conjunctive representations were active throughout the entire selection period and were functionally dissociable from the representation of constituent features. Specifically, the strength of conjunctions was a highly robust predictor of trial-by-trial variability in response times and was selectively related to an important behavioral indicator of conjunctive representations, the so-called partial-overlap priming pattern. These results provide direct evidence for conjunctive representations as critical precursors of action selection in humans.

Significance People distort probability in decision under risk and many other tasks. These distortions can be large, leading us to make markedly suboptimal decisions. There is no agreement on why we distort probability. Distortion changes systematically with task, hinting that distortions are dynamic compensations for some intrinsic “bound” on working memory. We first develop a model of the bound and compensation process and then report an experiment showing that the model accounts for individual human performance in decision under risk and relative frequency judgments. Last, we show that the particular compensation in each experimental condition serves to maximize the mutual information between objective decision variables and their internal representations. We distort probability to compensate for our own perceptual and cognitive limitations., In decision making under risk (DMR) participants’ choices are based on probability values systematically different from those that are objectively correct. Similar systematic distortions are found in tasks involving relative frequency judgments (JRF). These distortions limit performance in a wide variety of tasks and an evident question is, Why do we systematically fail in our use of probability and relative frequency information? We propose a bounded log-odds model (BLO) of probability and relative frequency distortion based on three assumptions: 1) log-odds: probability and relative frequency are mapped to an internal log-odds scale, 2) boundedness: the range of representations of probability and relative frequency are bounded and the bounds change dynamically with task, and 3) variance compensation: the mapping compensates in part for uncertainty in probability and relative frequency values. We compared human performance in both DMR and JRF tasks to the predictions of the BLO model as well as 11 alternative models, each missing one or more of the underlying BLO assumptions (factorial model comparison). The BLO model and its assumptions proved to be superior to any of the alternatives. In a separate analysis, we found that BLO accounts for individual participants’ data better than any previous model in the DMR literature. We also found that, subject to the boundedness limitation, participants’ choice of distortion approximately maximized the mutual information between objective task-relevant values and internal values, a form of bounded rationality.

Significance To see clearly, humans have to constantly move their eyes and bring objects of interest to the center of gaze. Vision scientists have tried to understand this selection process, modelling the “typical observer.” Here, we tested individual differences in the tendency to fixate different types of objects embedded in natural scenes. Fixation tendencies for faces, text, food, touched, and moving objects varied up to two- or threefold. These differences were present from the first eye movement after image onset and highly consistent across images and time. They predicted related perceptual skills and replicated across observer samples. This suggests individual gaze behavior is organized along semantic dimensions of biological significance, shaping the subjective way in which we see the world., What determines where we look? Theories of attentional guidance hold that image features and task demands govern fixation behavior, while differences between observers are interpreted as a “noise-ceiling” that strictly limits predictability of fixations. However, recent twin studies suggest a genetic basis of gaze-trace similarity for a given stimulus. This leads to the question of how individuals differ in their gaze behavior and what may explain these differences. Here, we investigated the fixations of >100 human adults freely viewing a large set of complex scenes containing thousands of semantically annotated objects. We found systematic individual differences in fixation frequencies along six semantic stimulus dimensions. These differences were large (>twofold) and highly stable across images and time. Surprisingly, they also held for first fixations directed toward each image, commonly interpreted as “bottom-up” visual salience. Their perceptual relevance was documented by a correlation between individual face salience and face recognition skills. The set of reliable individual salience dimensions and their covariance pattern replicated across samples from three different countries, suggesting they reflect fundamental biological mechanisms of attention. Our findings show stable individual differences in salience along a set of fundamental semantic dimensions and that these differences have meaningful perceptual implications. Visual salience reflects features of the observer as well as the image.

Significance Seeing in the three-dimensional world—stereopsis—is an innate human ability, but it varies substantially among individuals. The neurobiological basis of this variability is not understood. We combined diffusion and quantitative MRI imaging with a psychophysical measurements, and found that variability in stereoacuity is associated with microstructural differences in the right vertical occipital fasciculus, a white matter tract connecting dorsal and ventral visual cortex. This result suggests that the microstructure of the pathways that support information transmission across dorsal and ventral visual areas plays an important role human stereopsis., Stereopsis is a fundamental visual function that has been studied extensively. However, it is not clear why depth discrimination (stereoacuity) varies more significantly among people than other modalities. Previous studies have reported the involvement of both dorsal and ventral visual areas in stereopsis, implying that not only neural computations in cortical areas but also the anatomical properties of white matter tracts connecting those areas can impact stereopsis. Here, we studied how human stereoacuity relates to white matter properties by combining psychophysics, diffusion MRI (dMRI), and quantitative MRI (qMRI). We performed a psychophysical experiment to measure stereoacuity and, in the same participants, we analyzed the microstructural properties of visual white matter tracts on the basis of two independent measurements, dMRI (fractional anisotropy, FA) and qMRI (macromolecular tissue volume; MTV). Microstructural properties along the right vertical occipital fasciculus (VOF), a major tract connecting dorsal and ventral visual areas, were highly correlated with measures of stereoacuity. This result was consistent for both FA and MTV, suggesting that the behavioral–structural relationship reflects differences in neural tissue density, rather than differences in the morphological configuration of fibers. fMRI confirmed that binocular disparity stimuli activated the dorsal and ventral visual regions near VOF endpoints. No other occipital tracts explained the variance in stereoacuity. In addition, the VOF properties were not associated with differences in performance on a different psychophysical task (contrast detection). These series of experiments suggest that stereoscopic depth discrimination performance is, at least in part, constrained by dorso-ventral communication through the VOF.