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1.  Making predictions in a changing world—inference, uncertainty, and learning 
To function effectively, brains need to make predictions about their environment based on past experience, i.e., they need to learn about their environment. The algorithms by which learning occurs are of interest to neuroscientists, both in their own right (because they exist in the brain) and as a tool to model participants' incomplete knowledge of task parameters and hence, to better understand their behavior. This review focusses on a particular challenge for learning algorithms—how to match the rate at which they learn to the rate of change in the environment, so that they use as much observed data as possible whilst disregarding irrelevant, old observations. To do this algorithms must evaluate whether the environment is changing. We discuss the concepts of likelihood, priors and transition functions, and how these relate to change detection. We review expected and estimation uncertainty, and how these relate to change detection and learning rate. Finally, we consider the neural correlates of uncertainty and learning. We argue that the neural correlates of uncertainty bear a resemblance to neural systems that are active when agents actively explore their environments, suggesting that the mechanisms by which the rate of learning is set may be subject to top down control (in circumstances when agents actively seek new information) as well as bottom up control (by observations that imply change in the environment).
PMCID: PMC3682109  PMID: 23785310
change detection; uncertainty; exploratory behavior; modeling; bayes theorem; learning
2.  A Neural Circuit Covarying with Social Hierarchy in Macaques 
PLoS Biology  2014;12(9):e1001940.
A neural circuit that covaries with social hierarchy A neuroimaging study reveals that individual variation in brain circuits in structures below the cerebral cortex of macaques is associated with experience at different ends of the social hierarchy.
Despite widespread interest in social dominance, little is known of its neural correlates in primates. We hypothesized that social status in primates might be related to individual variation in subcortical brain regions implicated in other aspects of social and emotional behavior in other mammals. To examine this possibility we used magnetic resonance imaging (MRI), which affords the taking of quantitative measurements noninvasively, both of brain structure and of brain function, across many regions simultaneously. We carried out a series of tests of structural and functional MRI (fMRI) data in 25 group-living macaques. First, a deformation-based morphometric (DBM) approach was used to show that gray matter in the amygdala, brainstem in the vicinity of the raphe nucleus, and reticular formation, hypothalamus, and septum/striatum of the left hemisphere was correlated with social status. Second, similar correlations were found in the same areas in the other hemisphere. Third, similar correlations were found in a second data set acquired several months later from a subset of the same animals. Fourth, the strength of coupling between fMRI-measured activity in the same areas was correlated with social status. The network of subcortical areas, however, had no relationship with the sizes of individuals' social networks, suggesting the areas had a simple and direct relationship with social status. By contrast a second circuit in cortex, comprising the midsuperior temporal sulcus and anterior and dorsal prefrontal cortex, covaried with both individuals' social statuses and the social network sizes they experienced. This cortical circuit may be linked to the social cognitive processes that are taxed by life in more complex social networks and that must also be used if an animal is to achieve a high social status.
Author Summary
Social status is an important feature of group life in many primates. Position in the dominance hierarchy influences access to food and mates and is correlated with both general and mental health. Discovering how the brain is organized with respect to individual social status is an important first step for understanding the neural mechanisms that might drive social status and mediate its consequences. We performed a neuroimaging study in non-human primates and our findings suggest that brain organization reflects at least two aspects of dominance. First, we identified neural circuits in brain regions that appear to have a relatively simple and direct relationship with social status—one circuit in which gray matter volume tended to be greater in socially dominant individuals and another in which gray matter volume was greater in those with a more subordinate social position. We also showed that the degree of connectivity within each circuit was associated with experiences at each end of the social hierarchy. Second, given that social status in male macaques depends not only on successful engagement in agonistic behavior but also on success in forming social bonds that promote coalitions, we explored regions where gray matter relates to both social status and social network size. This second neural circuit may mediate the way in which dominance is dependent on social bond formation, which is in turn dependent on social cognition.
PMCID: PMC4151964  PMID: 25180883
3.  Distinct and Overlapping Functional Zones in the Cerebellum Defined by Resting State Functional Connectivity 
Cerebral Cortex (New York, NY)  2009;20(4):953-965.
The cerebellum processes information from functionally diverse regions of the cerebral cortex. Cerebellar input and output nuclei have connections with prefrontal, parietal, and sensory cortex as well as motor and premotor cortex. However, the topography of the connections between the cerebellar and cerebral cortices remains largely unmapped, as it is relatively unamenable to anatomical methods. We used resting-state functional magnetic resonance imaging to define subregions within the cerebellar cortex based on their functional connectivity with the cerebral cortex. We mapped resting-state functional connectivity voxel-wise across the cerebellar cortex, for cerebral–cortical masks covering prefrontal, motor, somatosensory, posterior parietal, visual, and auditory cortices. We found that the cerebellum can be divided into at least 2 zones: 1) a primary sensorimotor zone (Lobules V, VI, and VIII), which contains overlapping functional connectivity maps for domain-specific motor, somatosensory, visual, and auditory cortices; and 2) a supramodal zone (Lobules VIIa, Crus I, and II), which contains overlapping functional connectivity maps for prefrontal and posterior-parietal cortex. The cortical connectivity of the supramodal zone was driven by regions of frontal and parietal cortex which are not directly involved in sensory or motor processing, including dorsolateral prefrontal cortex and the frontal pole, and the inferior parietal lobule.
PMCID: PMC2837094  PMID: 19684249
cerebellum; fMRI; functional connectivity; networks; resting-state
4.  The Organization of Dorsal Frontal Cortex in Humans and Macaques 
The Journal of Neuroscience  2013;33(30):12255-12274.
The human dorsal frontal cortex has been associated with the most sophisticated aspects of cognition, including those that are thought to be especially refined in humans. Here we used diffusion-weighted magnetic resonance imaging (DW-MRI) and functional MRI (fMRI) in humans and macaques to infer and compare the organization of dorsal frontal cortex in the two species. Using DW-MRI tractography-based parcellation, we identified 10 dorsal frontal regions lying between the human inferior frontal sulcus and cingulate cortex. Patterns of functional coupling between each area and the rest of the brain were then estimated with fMRI and compared with functional coupling patterns in macaques. Areas in human medial frontal cortex, including areas associated with high-level social cognitive processes such as theory of mind, showed a surprising degree of similarity in their functional coupling patterns with the frontal pole, medial prefrontal, and dorsal prefrontal convexity in the macaque. We failed to find evidence for “new” regions in human medial frontal cortex. On the lateral surface, comparison of functional coupling patterns suggested correspondences in anatomical organization distinct from those that are widely assumed. A human region sometimes referred to as lateral frontal pole more closely resembled area 46, rather than the frontal pole, of the macaque. Overall the pattern of results suggest important similarities in frontal cortex organization in humans and other primates, even in the case of regions thought to carry out uniquely human functions. The patterns of interspecies correspondences are not, however, always those that are widely assumed.
PMCID: PMC3744647  PMID: 23884933
5.  Brain Systems for Probabilistic and Dynamic Prediction: Computational Specificity and Integration 
PLoS Biology  2013;11(9):e1001662.
Using computational modelling and neuroimaging, two distinct brain systems are shown to use distinct algorithms to make parallel predictions about the environment. The predictions are then optimally combined to control behavior.
A computational approach to functional specialization suggests that brain systems can be characterized in terms of the types of computations they perform, rather than their sensory or behavioral domains. We contrasted the neural systems associated with two computationally distinct forms of predictive model: a reinforcement-learning model of the environment obtained through experience with discrete events, and continuous dynamic forward modeling. By manipulating the precision with which each type of prediction could be used, we caused participants to shift computational strategies within a single spatial prediction task. Hence (using fMRI) we showed that activity in two brain systems (typically associated with reward learning and motor control) could be dissociated in terms of the forms of computations that were performed there, even when both systems were used to make parallel predictions of the same event. A region in parietal cortex, which was sensitive to the divergence between the predictions of the models and anatomically connected to both computational networks, is proposed to mediate integration of the two predictive modes to produce a single behavioral output.
Author Summary
To interact effectively with the environment, brains must predict future events based on past and current experience. Predictions associated with different behavioural domains of the brain are often associated with different algorithmic forms. For example, whereas the motor system makes dynamic moment-by-moment predictions based on physical world models, the reward system is more typically associated with statistical predictions learned over discrete events. However, in perceptually rich natural environments, behaviour is not neatly segmented into tasks like “reward learning” and “motor control.” Instead, many different types of information are available in parallel. The brain must both select behaviourally relevant information and arbitrate between conflicting predictions. To investigate how the brain balances and integrates different types of predictive information, we set up a task in which humans predicted an object's flight trajectory by using one of two strategies: either a statistical model (based on where objects had often landed in the past) or dynamic calculation of the current flight trajectory. Using fMRI, we show that brain activity switches between different regions of the brain, depending on which predictive strategy was used, even though behavioural output remained the same. Furthermore, we found that brain regions involved in selecting actions took into account the predictions from both competing algorithms, weighting each algorithm optimally in terms of the precision with which it could predict the event of interest. Thus, these distinct brain systems compete to control predictive behaviour.
PMCID: PMC3782423  PMID: 24086106
6.  Tools of the trade: psychophysiological interactions and functional connectivity 
Psychophysiological interactions (PPIs) analysis is a method for investigating task-specific changes in the relationship between activity in different brain areas, using functional magnetic resonance imaging (fMRI) data. Specifically, PPI analyses identify voxels in which activity is more related to activity in a seed region of interest (seed ROI) in a given psychological context, such as during attention or in the presence of emotive stimuli. In this tutorial, we aim to give a simple conceptual explanation of how PPI analysis works, in order to assist readers in planning and interpreting their own PPI experiments.
PMCID: PMC3375893  PMID: 22569188
psychophysiological interactions; PPI; functional connectivity; resting state
7.  A Potential Spatial Working Memory Training Task to Improve Both Episodic Memory and Fluid Intelligence 
PLoS ONE  2012;7(11):e50431.
One current challenge in cognitive training is to create a training regime that benefits multiple cognitive domains, including episodic memory, without relying on a large battery of tasks, which can be time-consuming and difficult to learn. By giving careful consideration to the neural correlates underlying episodic and working memory, we devised a computerized working memory training task in which neurologically healthy participants were required to monitor and detect repetitions in two streams of spatial information (spatial location and scene identity) presented simultaneously (i.e. a dual n-back paradigm). Participants’ episodic memory abilities were assessed before and after training using two object and scene recognition memory tasks incorporating memory confidence judgments. Furthermore, to determine the generalizability of the effects of training, we also assessed fluid intelligence using a matrix reasoning task. By examining the difference between pre- and post-training performance (i.e. gain scores), we found that the trainers, compared to non-trainers, exhibited a significant improvement in fluid intelligence after 20 days. Interestingly, pre-training fluid intelligence performance, but not training task improvement, was a significant predictor of post-training fluid intelligence improvement, with lower pre-training fluid intelligence associated with greater post-training gain. Crucially, trainers who improved the most on the training task also showed an improvement in recognition memory as captured by d-prime scores and estimates of recollection and familiarity memory. Training task improvement was a significant predictor of gains in recognition and familiarity memory performance, with greater training improvement leading to more marked gains. In contrast, lower pre-training recollection memory scores, and not training task improvement, led to greater recollection memory performance after training. Our findings demonstrate that practice on a single working memory task can potentially improve aspects of both episodic memory and fluid intelligence, and that an extensive training regime with multiple tasks may not be necessary.
PMCID: PMC3508978  PMID: 23209740
Despite the prominence of parietal activity in human neuromaging investigations of sensorimotor and cognitive processes there remains uncertainty about basic aspects of parietal cortical anatomical organization. Descriptions of human parietal cortex draw heavily on anatomical schemes developed in other primate species but the validity of such comparisons has been questioned by claims that there are fundamental differences between the parietal cortex in humans and other primates. A scheme is presented for parcellation of human lateral parietal cortex into component regions on the basis of anatomical connectivity and the functional interactions of the resulting clusters with other brain regions. Anatomical connectivity was estimated using diffusion-weighted magnetic resonance image (MRI) based tractography and functional interactions were assessed by correlations in activity measured with functional MRI (fMRI) at rest. Resting state functional connectivity was also assessed directly in the rhesus macaque lateral parietal cortex in an additional experiment and the patterns found reflected known neuroanatomical connections. Cross-correlation in the tractography-based connectivity patterns of parietal voxels reliably parcellated human lateral parietal cortex into ten component clusters. The resting state functional connectivity of human superior parietal and intraparietal clusters with frontal and extrastriate cortex suggested correspondences with areas in macaque superior and intraparietal sulcus. Functional connectivity patterns with parahippocampal cortex and premotor cortex again suggested fundamental correspondences between inferior parietal cortex in humans and macaques. In contrast, the human parietal cortex differs in the strength of its interactions between the central inferior parietal lobule region and the anterior prefrontal cortex.
PMCID: PMC3091022  PMID: 21411650
9.  Effort-based cost-benefit valuation and the human brain 
In both the wild and the laboratory, animals' preferences for one course of action over another reflect not just reward expectations but also the cost in terms of effort that must be invested in pursuing the course of action. The ventral striatum and dorsal anterior cingulate cortex (ACCd) are implicated in the making of cost-benefit decisions in the rat but there is little information about how effort costs are processed and influence calculations of expected net value in other mammals including the human. We carried out a functional magnetic resonance imaging (fMRI) study to determine whether and where activity in the human brain was available to guide effort-based cost-benefit valuation. Subjects were scanned while they performed a series of effortful actions to obtain secondary reinforcers. At the beginning of each trial, subjects were presented with one of eight different visual cues which they had learned indicated how much effort the course of action would entail and how much reward could be expected at its completion. Cue-locked activity in the ventral striatum and midbrain reflected the net value of the course of action, signaling the expected amount of reward discounted by the amount of effort to be invested. Activity in ACCd also reflected the interaction of both expected reward and effort costs. Posterior orbitofrontal and insular activity, however, only reflected the expected reward magnitude. The ventral striatum and anterior cingulate cortex may be the substrate of effort-based cost-benefit valuation in primates as well as in rats.
PMCID: PMC2954048  PMID: 19357278
anterior cingulate cortex; striatum; decision making; reward; effort; ventral tegmental area

Results 1-9 (9)