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1.  Primate comparative neuroscience using magnetic resonance imaging: promises and challenges 
Primate comparative anatomy is an established field that has made rich and substantial contributions to neuroscience. However, the labor-intensive techniques employed mean that most comparisons are often based on a small number of species, which limits the conclusions that can be drawn. In this review we explore how new developments in magnetic resonance imaging have the potential to apply comparative neuroscience to a much wider range of species, allowing it to realize an even greater potential. We discuss (1) new advances in the types of data that can be acquired, (2) novel methods for extracting meaningful measures from such data that can be compared between species, and (3) methods to analyse these measures within a phylogenetic framework. Together these developments will allow researchers to characterize the relationship between different brains, the ecological niche they occupy, and the behavior they produce in more detail than ever before.
PMCID: PMC4186285  PMID: 25339857
neuroecology; MRI; diffusion MRI; connectivity; phylogenetics
2.  Model-based analyses: Promises, pitfalls, and example applications to the study of cognitive control 
We discuss a recent approach to investigating cognitive control, which has the potential to deal with some of the challenges inherent in this endeavour. In a model-based approach, the researcher defines a formal, computational model that performs the task at hand and whose performance matches that of a research participant. The internal variables in such a model might then be taken as proxies for latent variables computed in the brain. We discuss the potential advantages of such an approach for the study of the neural underpinnings of cognitive control and its pitfalls, and we make explicit the assumptions underlying the interpretation of data obtained using this approach.
PMCID: PMC3335278  PMID: 20437297
Cognitive control; Model-based approach; Model; Reinforcement learning; Action regulation
3.  On the relationship between the “default mode network” and the “social brain” 
The default mode network (DMN) of the brain consists of areas that are typically more active during rest than during active task performance. Recently however, this network has been shown to be activated by certain types of tasks. Social cognition, particularly higher-order tasks such as attributing mental states to others, has been suggested to activate a network of areas at least partly overlapping with the DMN. Here, we explore this claim, drawing on evidence from meta-analyses of functional MRI data and recent studies investigating the structural and functional connectivity of the social brain. In addition, we discuss recent evidence for the existence of a DMN in non-human primates. We conclude by discussing some of the implications of these observations.
PMCID: PMC3380415  PMID: 22737119
default mode network; mentalizing; social cognition; fMRI; theory of mind; TPJ; posterior cingulate; medial frontal cortex
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
Previous research has identified the anterior cingulate cortex (ACC) as an important node in the neural network underlying decision making in primates. Decision making can, however, be studied under large variety of circumstances, ranging from the standard well-controlled lab situation to more natural, stochastic settings during which multiple agents interact. Here, we illustrate how these different varieties of decision making studied can influence theories of ACC function in monkeys. Converging evidence from unit recordings and lesions studies now suggest that the ACC is important for interpreting outcome information according to the current task context to guide future action selection. We then apply this framework to the study of human ACC function and discuss its potential implications.
PMCID: PMC2519031  PMID: 18189014
Anterior cingulate cortex; ACC; decision making; action selection; reward; monkey; human; foraging theory
6.  Causal manipulation of functional connectivity in a specific neural pathway during behaviour and at rest 
eLife  null;4:e04585.
Correlations in brain activity between two areas (functional connectivity) have been shown to relate to their underlying structural connections. We examine the possibility that functional connectivity also reflects short-term changes in synaptic efficacy. We demonstrate that paired transcranial magnetic stimulation (TMS) near ventral premotor cortex (PMv) and primary motor cortex (M1) with a short 8-ms inter-pulse interval evoking synchronous pre- and post-synaptic activity and which strengthens interregional connectivity between the two areas in a pattern consistent with Hebbian plasticity, leads to increased functional connectivity between PMv and M1 as measured with functional magnetic resonance imaging (fMRI). Moreover, we show that strengthening connectivity between these nodes has effects on a wider network of areas, such as decreasing coupling in a parallel motor programming stream. A control experiment revealed that identical TMS pulses at identical frequencies caused no change in fMRI-measured functional connectivity when the inter-pulse-interval was too long for Hebbian-like plasticity.
eLife digest
When a person has their brain scanned, the resulting images show that regions with similar roles tend to be active at the same time. These coordinated patterns of activity are often altered in the brains of patients with neurological or psychiatric disorders. However, relatively little is known about how the patterns are generated.
The degree to which brain regions are active at the same time is thought to depend partly on how well they are connected by brain cells. However, it is also possible that the coordinated activity reflects the extent to which one brain region is able to influence the activity of another. More than 50 years ago, it was demonstrated that this is the case between individual brain cells. If one brain cell repeatedly helps to activate another, the connection between the two cells will be strengthened. This process—known as synaptic plasticity—is thought to support learning and memory.
Now, Johnen, Neubert et al. have shown that the same process can also act between different brain regions. A technique called transcranial magnetic stimulation—in which magnetic fields are applied to specific areas of the scalp to excite brain tissue—was used on human volunteers to activate two regions involved in producing grasping movements with their hands.
If the first region of the brain was repeatedly activated a few milliseconds before the second region as the volunteers reached towards objects, the ability of the first region to activate the second increased. Notably, the effect was not seen when the interval between the activation of the regions was increased to 500 milliseconds: a delay long enough to ensure that brain cells in the first region were no longer active when the second region was stimulated.
This suggests that coordinated changes in the activity of brain regions might reflect the same plasticity processes as changes in activity seen between individual brain cells. This finding raises the possibility that, by deliberately altering the degree of coordinated activity between specific brain regions, it might be possible to recover abilities that have been lost as a result of disorders such as stroke.
PMCID: PMC4353194  PMID: 25664941
plasticity; resting-state connectivity; functional connectivity; premotor cortex; motor system; TMS; human
7.  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
8.  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
9.  Psychopathy-related traits and the use of reward and social information: a computational approach 
Psychopathy is often linked to disturbed reinforcement-guided adaptation of behavior in both clinical and non-clinical populations. Recent work suggests that these disturbances might be due to a deficit in actively using information to guide changes in behavior. However, how much information is actually used to guide behavior is difficult to observe directly. Therefore, we used a computational model to estimate the use of information during learning. Thirty-six female subjects were recruited based on their total scores on the Psychopathic Personality Inventory (PPI), a self-report psychopathy list, and performed a task involving simultaneous learning of reward-based and social information. A Bayesian reinforcement-learning model was used to parameterize the use of each source of information during learning. Subsequently, we used the subscales of the PPI to assess psychopathy-related traits, and the traits that were strongly related to the model's parameters were isolated through a formal variable selection procedure. Finally, we assessed how these covaried with model parameters. We succeeded in isolating key personality traits believed to be relevant for psychopathy that can be related to model-based descriptions of subject behavior. Use of reward-history information was negatively related to levels of trait anxiety and fearlessness, whereas use of social advice decreased as the perceived ability to manipulate others and lack of anxiety increased. These results corroborate previous findings suggesting that sub-optimal use of different types of information might be implicated in psychopathy. They also further highlight the importance of considering the potential of computational modeling to understand the role of latent variables, such as the weight people give to various sources of information during goal-directed behavior, when conducting research on psychopathy-related traits and in the field of forensic psychiatry.
PMCID: PMC3868018  PMID: 24391615
psychopathy; psychopathic traits; personality traits; individual differences; reinforcement learning; social learning; associative learning; computational modeling
10.  Error-Likelihood Prediction in the Medial Frontal Cortex: A Critical Evaluation 
A recent study has proposed that posterior regions of the medial frontal cortex (pMFC) learn to predict the likelihood of errors occurring in a given task context. A key prediction of the error-likelihood (EL) hypothesis is that the pMFC should exhibit enhanced activity to cues that are predictive of high compared with low error rates. We conducted 3 experiments, 2 using functional neuroimaging and 1 using event-related potentials, to test this prediction in human volunteers. The 3 experiments replicated previous research in showing clear evidence of increased pMFC activity associated with errors, conflict, negative feedback, and other aspects of task performance. However, none of the experiments yielded evidence for an effect of cue-signaled EL on pMFC activity or any indication that such an effect developed with learning. We conclude that although the EL hypothesis presents an elegant integrative account of pMFC function, it requires additional empirical support to remain tenable.
PMCID: PMC3752593  PMID: 16956979
ACC; dopamine; error processing; fMRI; reinforcement learning; stop signal
11.  Paired-pulse transcranial magnetic stimulation reveals probability-dependent changes in functional connectivity between right inferior frontal cortex and primary motor cortex during go/no-go performance 
The functional role of the right inferior frontal cortex (rIFC) in mediating human behavior is the subject of ongoing debate. Activation of the rIFC has been associated with both response inhibition and with signaling action adaptation demands resulting from unpredicted events. The goal of this study is to investigate the role of rIFC by combining a go/no-go paradigm with paired-pulse transcranial magnetic stimulation (ppTMS) over rIFC and the primary motor cortex (M1) to probe the functional connectivity between these brain areas. Participants performed a go/no-go task with 20% or 80% of the trials requiring response inhibition (no-go trials) in a classic and a reversed version of the task, respectively. Responses were slower to infrequent compared to frequent go trials, while commission errors were more prevalent to infrequent compared to frequent no-go trials. We hypothesized that if rIFC is involved primarily in response inhibition, then rIFC should exert an inhibitory influence over M1 on no-go (inhibition) trials regardless of no-go probability. If, by contrast, rIFC has a role on unexpected trials other than just response inhibition then rIFC should influence M1 on infrequent trials regardless of response demands. We observed that rIFC suppressed M1 excitability during frequent no-go trials, but not during infrequent no-go trials, suggesting that the role of rIFC in response inhibition is context dependent rather than generic. Importantly, rIFC was found to facilitate M1 excitability on all low frequent trials, irrespective of whether the infrequent event involved response inhibition, a finding more in line with a predictive coding framework of cognitive control.
PMCID: PMC3825091  PMID: 24282398
rIFC; go/no-go task; paired-pulse; TMS; motor cortex; prediction; inhibition
12.  Neural Mechanisms of Foraging 
Science (New York, N.Y.)  2012;336(6077):95-98.
Behavioural economic studies, involving limited numbers of choices, have provided key insights into neural decision-making mechanisms. By contrast, animals’ foraging choices arise in the context of sequences of encounters with prey/food. On each encounter the animal chooses to engage or whether the environment is sufficiently rich that searching elsewhere is merited. The cost of foraging is also critical. We demonstrate humans can alternate between two modes of choice, comparative decision-making and foraging, dependent on distinct neural mechanisms in ventromedial prefrontal (vmPFC) and anterior cingulate cortex (ACC) employing distinct reference frames; in ACC choice variables are represented in invariant reference to foraging/searching for alternatives. While vmPFC encodes values of specific well-defined options, ACC encodes the average value of the foraging environment and cost of foraging.
PMCID: PMC3440844  PMID: 22491854
13.  When the Brain Changes Its Mind: Flexibility of Action Selection in Instructed and Free Choices 
Cerebral Cortex (New York, NY)  2009;19(10):2352-2360.
The neural mechanisms underlying the selection and initiation of voluntary actions in the absence of external instructions are poorly understood. These mechanisms are usually investigated using a paradigm where different movement choices are self-generated by a participant on each trial. These “free choices” are compared with “instructed choices,” in which a stimulus informs subjects which action to make on each trial. Here, we introduce a novel paradigm to investigate these modes of action selection, by measuring brain processes evoked by an instruction to either reverse or maintain free and instructed choices in the period before a “go” signal. An unpredictable instruction to change a response plan had different effects on free and instructed choices. In instructed trials, change cues evoked a larger P300 than no-change cues, leading to a significant interaction of choice and change condition. Free-choice trials displayed a trend toward the opposite pattern. These results suggest a difference between updating of free and instructed action choices. We propose a theoretical framework for internally generated action in which representations of alternative actions remain available until a late stage in motor preparation. This framework emphasizes the high modifiability of voluntary action.
PMCID: PMC2742594  PMID: 19211661
action selection; event-related potential; motor preparation; voluntary action
14.  On the neural control of social emotional behavior 
It is known that the orbitofrontal cortex (OFC) is crucially involved in emotion regulation. However, the specific role of the OFC in controlling the behavior evoked by these emotions, such as approach–avoidance (AA) responses, remains largely unexplored. We measured behavioral and neural responses (using fMRI) during the performance of a social task, a reaction time (RT) task where subjects approached or avoided visually presented emotional faces by pulling or pushing a joystick, respectively. RTs were longer for affect-incongruent responses (approach angry faces and avoid happy faces) as compared to affect-congruent responses (approach–happy; avoid–angry). Moreover, affect-incongruent responses recruited increased activity in the left lateral OFC. These behavioral and neural effects emerged only when the subjects responded explicitly to the emotional value of the faces (AA-task) and largely disappeared when subjects responded to an affectively irrelevant feature of the faces during a control (gender evaluation: GE) task. Most crucially, the size of the OFC-effect correlated positively with the size of the behavioral costs of approaching angry faces. These findings qualify the role of the lateral OFC in the voluntary control of social–motivational behavior, emphasizing the relevance of this region for selecting rule-driven stimulus–response associations, while overriding automatic (affect-congruent) stimulus–response mappings.
PMCID: PMC2656885  PMID: 19047074
orbitofrontal cortex; approach–avoidance; motivational behavior; angry facial expression; social–emotional behavior
15.  Influence of Uncertainty and Surprise on Human Corticospinal Excitability during Preparation for Action 
Current Biology  2008;18(10):775-780.
Actions are guided by prior sensory information [1–10], which is inherently uncertain. However, how the motor system is sculpted by trial-by-trial content of current sensory information remains largely unexplored. Previous work suggests that conditional probabilities, learned under a particular context, can be used preemptively to influence the output of the motor system [11–14]. To test this we used transcranial magnetic stimulation (TMS) to read out corticospinal excitability (CSE) during preparation for action in an instructed delay task [15, 16]. We systematically varied the uncertainty about an impending action by changing the validity of the instructive visual cue. We used two information-theoretic quantities to predict changes in CSE, prior to action, on a trial-by-trial basis: entropy (average uncertainty) and surprise (the stimulus-bound information conveyed by a visual cue) [17–19]. Our data show that during preparation for action, human CSE varies according to the entropy and surprise conveyed by visual events guiding action. CSE increases on trials with low entropy about the impending action and low surprise conveyed by an event. Commensurate effects were observed in reaction times. We suggest that motor output is biased according to contextual probabilities that are represented dynamically in the brain.
PMCID: PMC2387198  PMID: 18485711

Results 1-15 (15)