Specific neural correlates of successful learning and adaptation during social exchanges

Cooperation and betrayal are universal features of social interactions, and knowing who to trust is vital in human society. Previous studies have identified brain regions engaged by decision making during social encounters, but the mechanisms supporting modification of future behaviour by utilizing social experience are not well characterized. Using functional magnetic resonance imaging (fMRI), we show that cooperation and betrayal during social exchanges elicit specific patterns of neural activity associated with future behaviour. Unanticipated cooperation leads to greater behavioural adaptation than unexpected betrayal, and is signalled by specific neural responses in the striatum and midbrain. Neural responses to betrayal and willingness to trust novel partners both decrease as the number of individuals encountered during repeated social encounters increases. We propose that, as social groups increase in size, uncooperative or untrustworthy behaviour becomes progressively less surprising, with cooperation becoming increasingly important as a stimulus for social learning. Effects on reputation of non-trusting decisions may also act to drive pro-social behaviour. Our findings characterize the dynamic neural processes underlying social adaptation, and suggest that the brain is optimized to cooperate with trustworthy partners, rather than avoiding those who might betray us.     

Distinct neural systems underlie learning visuomotor and spatial representations of motor skills

Motor skill learning depends upon acquiring knowledge about multiple features of sequential behaviors, including their visuomotor and spatial properties. To investigate the neural systems that distinguish these representations, we carried out functional magnetic resonance imaging (fMRI) as healthy adults learned to type sequences on a novel keyboard. On the initial training day, learning-related changes in brain activation were found in distributed cortical regions, only a subset of which correlated with improvements in movement time (MT), suggesting their preeminence in controlling movements online. Subjects received extended training on the sequences during the ensuing week, after which they returned to the scanner for another imaging session. Relative to performance at the end of the first training day, continued plasticity was most striking in the inferior parietal cortex and new areas of plasticity were uncovered in the caudate and cerebellum. Plasticity in these regions correlated with reaction time (RT), suggesting their role in planning sequences before movement onset. Two transfer conditions probed for "what" subjects learned. The probe for visuomotor learning produced increased activation in visual analysis (left inferior visual cortex) and advance planning (left caudate) systems. The probe for spatial learning produced increased activation in visuomotor-transformation (left dorsal visual pathway) and retrieval (left precuneus) systems. Increased activity in all of these regions correlated with increased RT, but not MT, indicating that both transfer conditions interfered with the neural representation of plans for the sequences, but not processes that controlled their implementation. These findings demonstrated that neuroanatomically dissociable systems support the acquisition of visuomotor and spatial representations of actions.     

Evidence for neural accommodation to a writing system following learning

Native English speakers with no knowledge of Chinese were trained on 60 Chinese characters according to one of three mapping conditions: orthography to pronunciation and meaning (P + M), orthography to pronunciation (P), and orthography to meaning (M). Following the training, fMRI scans taken during passive viewing of Chinese characters showed activation in brain regions that partially overlap the regions found in studies of skilled Chinese readers, but typically not found in alphabetic readers. Areas include bilateral middle frontal (BA 9), right occipital (BA 18/19), and fusiform (BA 37) regions. The activation pattern of Chinese characters was similar across the three groups. However, peak location was different in the left middle frontal region between groups. Direct contrasts between the groups also revealed stronger activation of left middle frontal in the P + M group. The results suggest that learners acquired skill in reading Chinese characters using a brain network similar to that used by Chinese native speakers. The results are consistent with the system accommodation hypothesis: The brain's reading network accommodates to features of an acquired writing system.     

Getting to know you: general and specific neural computations for learning about people

Learning about other peoples'' attributes, e.g. whether an individual is generous or selfish, is central to human social cognition. It is well documented that a network of cortical regions is reliably activated when we engage social processes. However, little is known about the specific computations performed by these regions or whether such processing is specialized for the social domain. We investigated these questions using a task in which participants (N = 26) learned about four peoples’ generosity by watching them choose to share money with third party partners, or not. In a non-social control condition, participants learned the win/loss rates of four lotteries. fMRI analysis revealed learning-related general (social + non-social) prediction error signals in the dorsomedial and dorsolateral prefrontal cortices (bilaterally), and in the right lateral parietal cortex. Socially specific (social > non-social) prediction error signals were found in the precuneus. Interestingly, the region that exhibited social prediction errors was a distinct subregion of the area in the precuneus and posterior cingulate cortex that exhibited a commonly reported main effect of higher overall activity for social vs non-social stimuli. These findings elucidate the domain—general and—specific computations underlying learning about other people and demonstrate the increased explanatory power of computational approaches to social cognition.     

The influence of personality on neural mechanisms of observational fear and reward learning

Fear and reward learning can occur through direct experience or observation. Both channels can enhance survival or create maladaptive behavior. We used fMRI to isolate neural mechanisms of observational fear and reward learning and investigate whether neural response varied according to individual differences in neuroticism and extraversion. Participants learned object-emotion associations by observing a woman respond with fearful (or neutral) and happy (or neutral) facial expressions to novel objects. The amygdala-hippocampal complex was active when learning the object-fear association, and the hippocampus was active when learning the object-happy association. After learning, objects were presented alone; amygdala activity was greater for the fear (vs. neutral) and happy (vs. neutral) associated object. Importantly, greater amygdala-hippocampal activity during fear (vs. neutral) learning predicted better recognition of learned objects on a subsequent memory test. Furthermore, personality modulated neural mechanisms of learning. Neuroticism positively correlated with neural activity in the amygdala and hippocampus during fear (vs. neutral) learning. Low extraversion/high introversion was related to faster behavioral predictions of the fearful and neutral expressions during fear learning. In addition, low extraversion/high introversion was related to greater amygdala activity during happy (vs. neutral) learning, happy (vs. neutral) object recognition, and faster reaction times for predicting happy and neutral expressions during reward learning. These findings suggest that neuroticism is associated with an increased sensitivity in the neural mechanism for fear learning which leads to enhanced encoding of fear associations, and that low extraversion/high introversion is related to enhanced conditionability for both fear and reward learning.     

Perceiving actions before they happen: psychological dimensions scaffold neural action prediction

The social world buzzes with action. People constantly walk, talk, eat, work, play, snooze and so on. To interact with others successfully, we need to both understand their current actions and predict their future actions. Here we used functional neuroimaging to test the hypothesis that people do both at the same time: when the brain perceives an action, it simultaneously encodes likely future actions. Specifically, we hypothesized that the brain represents perceived actions using a map that encodes which actions will occur next: the six-dimensional Abstraction, Creation, Tradition, Food(-relevance), Animacy and Spiritualism Taxonomy (ACT-FAST) action space. Within this space, the closer two actions are, the more likely they are to precede or follow each other. To test this hypothesis, participants watched a video featuring naturalistic sequences of actions while undergoing functional magnetic resonance imaging (fMRI) scanning. We first use a decoding model to demonstrate that the brain uses ACT-FAST to represent current actions. We then successfully predicted as-yet unseen actions, up to three actions into the future, based on their proximity to the current action’s coordinates in ACT-FAST space. This finding suggests that the brain represents actions using a six-dimensional action space that gives people an automatic glimpse of future actions.     

Attentional modulation in visual cortex is modified during perceptual learning

Practicing a visual task commonly results in improved performance. Often the improvement does not transfer well to a new retinal location, suggesting that it is mediated by changes occurring in early visual cortex, and indeed neuroimaging and neurophysiological studies both demonstrate that perceptual learning is associated with altered activity in visual cortex. Theoretical treatments tend to invoke neuroplasticity that refines early sensory processing. An alternative possibility is that performance is improved because of an altered attentional strategy and that the changes in early visual areas reflect locally altered top-down attentional modulation. To test this idea, we have used functional MRI to examine changes in attentional modulation in visual cortex while participants learn an orientation discrimination task. By examining activity in visual cortex during the preparatory period when the participant has been cued to attend to an upcoming stimulus, we isolated the top-down modulatory signal received by the visual cortex. We show that this signal changes as learning progresses, possibly reflecting gradual automation of the task. By manipulating task difficulty, we show that the change mirrors performance, occurring most quickly for easier stimuli. The effects were seen only at the retinal locus of the stimulus, ruling out a generalized change in alertness. The results suggest that spatial attention changes during perceptual learning and that this may account for some of the concomitant changes seen in visual cortex.     

Associations between polygenic risk for schizophrenia and brain function during probabilistic learning in healthy individuals

A substantial proportion of schizophrenia liability can be explained by additive genetic factors. Risk profile scores (RPS) directly index risk using a summated total of common risk variants weighted by their effect. Previous studies suggest that schizophrenia RPS predict alterations to neural networks that support working memory and verbal fluency. In this study, we apply schizophrenia RPS to fMRI data to elucidate the effects of polygenic risk on functional brain networks during a probabilistic‐learning neuroimaging paradigm. The neural networks recruited during this paradigm have previously been shown to be altered to unmedicated schizophrenia patients and relatives of schizophrenia patients, which may reflect genetic susceptibility. We created schizophrenia RPS using summary data from the Psychiatric Genetic Consortium (Schizophrenia Working Group) for 83 healthy individuals and explore associations between schizophrenia RPS and blood oxygen level dependency (BOLD) during periods of choice behavior (switch–stay) and reflection upon choice outcome (reward–punishment). We show that schizophrenia RPS is associated with alterations in the frontal pole (P_{WHOLE‐BRAIN‐CORRECTED} = 0.048) and the ventral striatum (P_{ROI‐CORRECTED} = 0.036), during choice behavior, but not choice outcome. We suggest that the common risk variants that increase susceptibility to schizophrenia can be associated with alterations in the neural circuitry that support the processing of changing reward contingencies. Hum Brain Mapp 37:491–500, 2016. © 2015 Wiley Periodicals, Inc.     

The developmental neural substrates of Hebb repetition learning and their link with reading ability

Hebb repetition learning is a fundamental learning mechanism for sequential knowledge, such as language. However, still little is known about its development. This fMRI study examined the developmental neural substrates of Hebb repetition learning and its relation with reading abilities in a group of 49 children aged from 6 to 12 years. In the scanner, the children carried out an immediate serial recall task for syllable sequences of which some sequences were repeated several times over the course of the session (Hebb repetition sequences). The rate of Hebb repetition learning was associated with modulation of activity in the medial temporal lobe. Importantly, for the age range studied here, learning‐related medial temporal lobe modulation was independent of the age of the children. Furthermore, we observed an association between regular and irregular word reading abilities and the neural substrates of Hebb repetition learning. This study suggests that the functional neural substrates of Hebb repetition learning do not undergo further maturational changes in school age children, possibly because they are sustained by implicit sequential learning mechanisms which are considered to be fully developed by that age. Importantly, the neural substrates of Hebb learning remain significant determinants of children's learning abilities, such as reading.     

Changes in corticostriatal connectivity during reinforcement learning in humans

Many computational models assume that reinforcement learning relies on changes in synaptic efficacy between cortical regions representing stimuli and striatal regions involved in response selection, but this assumption has thus far lacked empirical support in humans. We recorded hemodynamic signals with fMRI while participants navigated a virtual maze to find hidden rewards. We fitted a reinforcement‐learning algorithm to participants' choice behavior and evaluated the neural activity and the changes in functional connectivity related to trial‐by‐trial learning variables. Activity in the posterior putamen during choice periods increased progressively during learning. Furthermore, the functional connections between the sensorimotor cortex and the posterior putamen strengthened progressively as participants learned the task. These changes in corticostriatal connectivity differentiated participants who learned the task from those who did not. These findings provide a direct link between changes in corticostriatal connectivity and learning, thereby supporting a central assumption common to several computational models of reinforcement learning. Hum Brain Mapp 36:793–803, 2015. © 2014 Wiley Periodicals, Inc .     

Sequential neural changes during motor learning in schizophrenia

Positron emission tomography (PET) was used to investigate differences in neural plasticity associated with learning a unique motor task in patients with schizophrenia and healthy volunteers. Working with a robotic manipulandum, subjects learned reaching movements in a force field. Visual cues were provided to guide the reaching movements. PET rCBF measures were acquired while participants learned the motor skill over successive runs. The groups did not differ in behavioral performance but did differ in their rCBF activity patterns. Healthy volunteers displayed blood flow increases in primary motor cortex and supplementary motor area with motor learning. The patients with schizophrenia displayed an increase in the primary visual cortex with motor learning. Changes in these regions were positively correlated with changes in each group's motor accuracy, respectively. This is the first study to employ a unique arm-reaching motor learning test to assess neural plasticity during multiple phases of motor learning in patients with schizophrenia. The patients may have an inability to rapidly tune motor cortical neural populations to a preferred direction. The visual system, however, appears to be highly compensated in schizophrenia and the inability to rapidly modulate the motor cortex may be substantially corrected by the schizophrenic group's visuomotor adaptations.     

Prefrontal and striatal activation during sequence learning in geriatric depression.

BACKGROUND: Frontostriatal dysfunction is a primary hypothesis for the neurocognitive changes of depression in late life. The aim of the present study was to test this hypothesis with the use of functional magnetic resonance imaging (fMRI) tasks that are known to engage the prefrontal and neostriatal cognitive circuits. METHODS: Twenty-three elderly subjects (mean age, 69.9 years) participated: 11 subjects with a current major depressive episode and 12 nondepressed elderly control subjects. Subjects underwent fMRI while performing a concurrent implicit and explicit sequence learning task. Region of interest (ROI)-based analyses were conducted, focusing on the dorsal anterior cingulate cortex, the dorsolateral prefrontal cortex, and the neostriatum. RESULTS: As expected, both the control and depressed subjects learned the sequence during both implicit and explicit conditions. During explicit learning, decreased prefrontal activation was found in the depressed subjects, along with increased striatal activation. The increased striatal activity in the depressed subjects was due to increased activity on the trials that violated the sequence. During implicit learning, no significant differences were found between the groups in the identified ROIs. CONCLUSIONS: The increased striatal activation on trials that violated the sequence demonstrates a greater response to negative feedback for depressed compared with control subjects. Our observations of significant differences in both prefrontal and striatal regions in the depressed elderly subjects relative to elderly control subjects supports the frontostriatal dysfunction hypothesis of late-life depression.     

Lexical learning in a new language leads to neural pattern similarity with word reading in native language

Previous neuroimaging studies have suggested similar neural activations for word reading in native and second languages. However, such similarities were qualitatively determined (i.e., overlapping activation based on traditional univariate activation analysis). In this study, using representational similarity analysis and an artificial language training paradigm, we quantitatively computed cross‐language neural pattern similarity to examine the modulatory effect of proficiency in the new language. Twenty‐four native Chinese speakers were trained to learn 30 words in a logographic artificial language for 12 days and scanned while performing a semantic decision task after 4‐day training and after 12‐day training. Results showed that higher proficiency in the new language was associated with higher cross‐language pattern similarity in select regions of the reading network.     

Hippocampal function during associative learning in patients with posttraumatic stress disorder

In the last decade several studies have shown memory deficits in patients with posttraumatic stress disorder (PTSD) which have been associated with a reduced hippocampus volume. However, until now we do not know how or whether these structural abnormalities turn into functional abnormalities. Thus, the primary purpose of the present study was the investigation of the hippocampal function using functional magnet resonance imaging (fMRI).We compared PTSD patients and healthy control participants using an associative learning paradigm consisting of two encoding and one retrieval condition. During fMRI scanning participants had to learn face-profession pairs. Afterwards only faces were presented as cue stimuli for associating the category of the prior learned target profession and the participants had to decide whether this face belonged to a scientific or an artistic profession. Additionally, cognitive functioning, i.e. memory and attention, was examined using neuropsychological standard tests.During encoding PTSD patients showed stronger hippocampal and weaker prefrontal activation compared to healthy control participants. During retrieval the two groups did not differ neither in hippocampus activation nor in accuracy of retrieval. PTSD patients however showed a reduced activation in the left parahippocampal gyrus and other memory-related brain regions. We did not find any significant memory differences between PTSD patients and healthy control participants.The results suggest that PTSD has an effect on memory-related brain function despite intact memory functioning. In particular the hippocampal/parahippocampal regions and the prefrontal cortex show functional alterations during associative learning and memory.     

Gamma‐band neural coupling during conceptual alignment

Conceptual alignment is a prerequisite for mutual understanding. However, little is known about the neurophysiological brain‐to‐brain underpinning during conceptual alignment for mutual understanding. Here, we recorded multi‐channel electroencephalogram (EEG) simultaneously from two participants in Experiment 1 and adopted the dual‐tACS techniques in Experiment 2 to investigate the underlying brain‐to‐brain EEG coupling during conceptual alignment and the possible enhancement effect. Our results showed that 1) higher phase‐locking value (PLV), a sensitive measure for quantifying neural coupling strength between EEG signals, at the gamma frequency band (28–40 Hz), was observed in the left temporoparietal site (left TP) area between successful versus unsuccessful conceptual alignment. The left TP gamma coupling strength correlated with the accuracy of conceptual alignment and differentiated whether subjects belonged to the SUCCESS or FAILURE groups in our study. 2) In‐phase gamma‐band transcranial alternating current stimulation (tACS) over the left TP area increased the accuracy of subjects in the SUCCESS group but not the FAILURE group. 3) The effect of perspective‐taking on the accuracy was mediated by the gamma coupling strength within the left TP area. Our results support the role of gamma‐band coupling between brains for interpersonal conceptual alignment. We provide dynamic interpersonal neurophysiological insights into the formation of successful communication.     

Altered neural function in pediatric bipolar disorder during reversal learning

Dickstein DP, Finger EC, Skup M, Pine DS, Blair JR, Leibenluft E. Altered neural function in pediatric bipolar disorder during reversal learning.
Bipolar Disord 2010: 12: 707–719. © 2010 The Authors.
Journal compilation © 2010 John Wiley & Sons A/S. Objective: Data documenting the functional impairment associated with the diagnosis of bipolar disorder (BD) in children and adolescents highlight the need for greater understanding of its pathophysiology. Toward that end, we demonstrated previously that BD youth have behavioral deficits on reversal learning tasks. On such tasks, participants must first acquire a stimulus/response relationship through trial‐and‐error learning, and then discern when the stimulus/reward relationship reverses. Here, we use event‐related functional magnetic resonance imaging (fMRI) to elucidate neural correlates of reversal learning deficits in euthymic BD youth compared to typically developing controls. Method: We compared euthymic pediatric BD participants (n = 16) versus age‐, sex‐, and IQ‐matched controls (n = 16). Our main outcome measure was blood oxygen level‐dependent (BOLD) signal measured with fMRI during an event‐related probabilistic reversal task. Results: Pediatric BD participants had significantly greater neural activity than controls in fronto‐parietal regions during the reversal phase, particularly in response to punished reversal errors (p < 0.05 corrected for multiple comparisons). Conclusions: Our current study suggests that during reversal learning, BD youths inefficiently recruit regions associated with processing response conflict and implementing alternative responses, including subdivisions of the frontal cortex and the parietal cortex. Such deficits are present in euthymic BD youth. Further work is necessary to evaluate the specificity of such alterations.     

A correlation‐based method for extracting subject‐specific components and artifacts from group‐fMRI data

We present a simple but effective correlation‐based method (maxCorr) for extracting subject‐specific components from group‐fMRI data. The method finds signal components that correlate maximally with the data set of one subject and minimally with the data sets of the other subjects. We show that such subject‐specific components are often related to movement and physiological noise (e.g. cardiac cycle, respiration). We further demonstrate that removing the most subject‐specific components for each subject reduces the overall data variance and improves the statistical identification of true fMRI activations. We compare the performance of maxCorr with CompCor, a commonly used artifact‐finding method in fMRI analysis. We show that maxCorr is less likely than CompCor to remove actual stimulus‐related activity, especially when no information about the stimulus is available. MaxCorr operates without stimulus information and is therefore well suitable for analyses of fMRI experiments employing naturalistic stimuli, such as movies, where stimulus regressors are difficult to construct, and for brain decoding techniques benefiting from reduced subject‐specific variance in each subject's data.     

Interoceptive awareness enhances neural activity during empathy

Empathy is a multicomponent function that includes sensorimotor, affective, and cognitive components. Although especially the affective component may implicate interoception and interoceptive awareness, the impact of interoception on empathy has never been evaluated behaviorally or neurophysiologically. Here, we tested how a preceding period of interoceptive awareness impacts and modulates neural activity during subsequent empathy. We used functional magnetic resonance imaging (fMRI) and measured the sequential interaction between interoception and empathy using fMRI in 18 healthy subjects. We found that the preceding interoceptive awareness period significantly enhanced neural activity during empathy in bilateral anterior insula and various cortical midline regions. The enhancement of neural activity during empathy in both interoceptive and empathy networks by preceding interoceptive awareness suggests a close relationship between interoception and empathy; thereby, interoception seems to be implicated to yielding empathy. Hum Brain Mapp, 2013. © 2012 Wiley Periodicals, Inc.     

Dual-task interference during initial learning of a new motor task results from competition for the same brain areas

Cerebral patterns of activity elicited by dual-task performance throughout the learning of a complex bimanual coordination pattern were addressed. Subjects (N = 12) were trained on the coordination pattern and scanned using fMRI at early (PRE) and late (POST) learning stages. During scanning, the coordination pattern was performed either as a single task or in concurrence with a simultaneous visual search task (i.e. dual task). Kinematics data revealed a significant performance improvement as a result of learning. In PRE-scanning, the dual-task condition induced deterioration of motor performance, relative to the single-task condition. Activity in lateral frontal and parietal regions involved in both visual search and motor coordination tasks (i.e. ‘overlapping’ regions) was reduced when the tasks were performed simultaneously. In POST-scanning, kinematics performance was equivalent under single- and dual-task conditions, suggesting automaticity of the coordination pattern. Furthermore, overlap between regions involved in visual search and motor tasks was reduced, and dual-task performance was no longer associated with reduction of frontal and parietal activity. Our results suggest that behavioral interference between a complex motor coordination task and a simple simultaneous visual search task occurs when both tasks recruit overlapping regions in the frontal and parietal cortices. This may provide a neural basis for dissipation of dual-task interference following extensive motor practice, which is a traditional behavioral marker of motor automaticity.