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Predicting individual mental traits and behavioral dispositions from brain imaging data through machine-learning approaches is becoming a rapidly evolving field in neuroscience. Beyond scientific and clinical applications, such approaches also hold the potential to gain substantial influence in fields such as human resource management, education, or criminal law. Although several challenges render real-life applications of such tools difficult, future conflicts of individual, economic, and public interests are preprogrammed, given the prospect of improved personalized predictions across many domains. In this Perspective paper, we thus argue for the need to engage in a discussion on the ethical, legal, and societal implications of the emergent possibilities for brain-based predictions and outline some of the aspects for this discourse., Advances in machine learning on neuroimaging data have opened up the possibility of objectively predicting individual traits like intelligence, personality, or clinical risks from brain scans. This Perspective article discusses the methodological and ethical challenges arising from these advances.

The encoding of sensory information in the human brain is thought to be optimised by two principal processes: ‘prediction’ uses stored information to guide the interpretation of forthcoming sensory events, and ‘attention’ prioritizes these events according to their behavioural relevance. Despite the ubiquitous contributions of attention and prediction to various aspects of perception and cognition, it remains unknown how they interact to modulate information processing in the brain. A recent extension of predictive coding theory suggests that attention optimises the expected precision of predictions by modulating the synaptic gain of prediction error units. Because prediction errors code for the difference between predictions and sensory signals, this model would suggest that attention increases the selectivity for mismatch information in the neural response to a surprising stimulus. Alternative predictive coding models propose that attention increases the activity of prediction (or ‘representation’) neurons and would therefore suggest that attention and prediction synergistically modulate selectivity for ‘feature information’ in the brain. Here, we applied forward encoding models to neural activity recorded via electroencephalography (EEG) as human observers performed a simple visual task to test for the effect of attention on both mismatch and feature information in the neural response to surprising stimuli. Participants attended or ignored a periodic stream of gratings, the orientations of which could be either predictable, surprising, or unpredictable. We found that surprising stimuli evoked neural responses that were encoded according to the difference between predicted and observed stimulus features, and that attention facilitated the encoding of this type of information in the brain. These findings advance our understanding of how attention and prediction modulate information processing in the brain, as well as support the theory that attention optimises precision expectations during hierarchical inference by increasing the gain of prediction errors., Author summary The human brain is theorised to operate like a sophisticated hypothesis tester, using past experience to generate a model of the external world, testing predictions of this model against incoming sensory evidence, and generating a ‘prediction error’ signal that updates the model when predictions and sensory evidence do not match. In addition to predicting the content of sensory signals, an optimal system should also predict the reliability (or ‘precision’) of those signals to minimise the influence of unreliable sensory information. It has been proposed that attention optimises this process by boosting prediction error signals, which are coded as the difference (or ‘mismatch’) between predicted and observed stimulus features. Accordingly, this theory predicts that attention should increase the selectivity for mismatch information in the neural response to surprising stimuli. We tested this hypothesis in human participants by training a decoding algorithm to identify ‘mismatch information’ in the brain, recorded by electroencephalography (EEG), following the presentation of surprising stimuli that were either attended or ignored. We found that attention did indeed increase the selectivity for mismatch information in the neural response, supporting the notion that attention and prediction are intricately related processes.

Many decisions rely on how we evaluate potential outcomes and estimate their corresponding probabilities of occurrence. Outcome evaluation is subjective because it requires consulting internal preferences and is sensitive to context. In contrast, probability estimation requires extracting statistics from the environment and therefore imposes unique challenges to the decision maker. Here, we show that probability estimation, like outcome evaluation, is subject to context effects that bias probability estimates away from other events present in the same context. However, unlike valuation, these context effects appeared to be scaled by estimated uncertainty, which is largest at intermediate probabilities. Blood-oxygen-level-dependent (BOLD) imaging showed that patterns of multivoxel activity in the dorsal anterior cingulate cortex (dACC), ventromedial prefrontal cortex (VMPFC), and intraparietal sulcus (IPS) predicted individual differences in context effects on probability estimates. These results establish VMPFC as the neurocomputational substrate shared between valuation and probability estimation and highlight the additional involvement of dACC and IPS that can be uniquely attributed to probability estimation. Because probability estimation is a required component of computational accounts from sensory inference to higher cognition, the context effects found here may affect a wide array of cognitive computations., This study shows how probability estimation can be affected by the context of our recent experience, namely, how the presence of multiple events experienced closed in time can influence their respective probability estimates.

Psychological and personality factors, socioeconomic status, and brain properties all contribute to chronic pain but have essentially been studied independently. Here, we administered a broad battery of questionnaires to patients with chronic back pain (CBP) and collected repeated sessions of resting-state functional magnetic resonance imaging (fMRI) brain scans. Clustering and network analyses applied on the questionnaire data revealed four orthogonal dimensions accounting for 56% of the variance and defining chronic pain traits. Two of these traits—Pain-trait and Emote-trait—were associated with back pain characteristics and could be related to distinct distributed functional networks in a cross-validation procedure, identifying neurotraits. These neurotraits showed good reliability across four fMRI sessions acquired over five weeks. Further, traits and neurotraits all related to the income, emphasizing the importance of socioeconomic status within the personality space of chronic pain. Our approach is a first step in providing metrics aimed at unifying the psychology and the neurophysiology of chronic pain applicable across diverse clinical conditions., A neuroimaging study shows that psychological contributors of chronic pain are represented in patterns of resting state functional connectivity; clustering analysis of these patterns suggests the existence of subtypes of chronic pain patients with specific clinical characteristics.

Persistent neural activity that encodes online mental representations plays a central role in working memory (WM). However, there has been debate regarding the number of items that can be concurrently represented in this active neural state, which is often called the “focus of attention.” Some models propose a strict single-item limit, such that just 1 item can be neurally active at once while other items are relegated to an activity-silent state. Although past studies have decoded multiple items stored in WM, these studies cannot rule out a switching account in which only a single item is actively represented at a time. Here, we directly tested whether multiple representations can be held concurrently in an active state. We tracked spatial representations in WM using alpha-band (8–12 Hz) activity, which encodes spatial positions held in WM. Human observers remembered 1 or 2 positions over a short delay while we recorded electroencephalography (EEG) data. Using a spatial encoding model, we reconstructed active stimulus-specific representations (channel-tuning functions [CTFs]) from the scalp distribution of alpha-band power. Consistent with past work, we found that the selectivity of spatial CTFs was lower when 2 items were stored than when 1 item was stored. Critically, data-driven simulations revealed that the selectivity of spatial representations in the two-item condition could not be explained by models that propose that only a single item can exist in an active state at once. Thus, our findings demonstrate that multiple items can be concurrently represented in an active neural state., An electroencephalography-based study shows that working memory delay activity concurrently represents two items, posing a challenge for models which propose that only one item can be actively represented at a time.

Although numerous studies have convincingly demonstrated that sleep plays a critical role in motor sequence learning (MSL) consolidation, the specific contribution of the different sleep stages in this type of memory consolidation is still contentious. To probe the role of stage 2 non-REM sleep (NREM2) in this process, we used a conditioning protocol in three different groups of participants who either received an odor during initial training on a motor sequence learning task and were re-exposed to this odor during different sleep stages of the post-training night (i.e., NREM2 sleep [Cond-NREM2], REM sleep [Cond-REM], or were not conditioned during learning but exposed to the odor during NREM2 [NoCond]). Results show that the Cond-NREM2 group had significantly higher gains in performance at retest than both the Cond-REM and NoCond groups. Also, only the Cond-NREM2 group yielded significant changes in sleep spindle characteristics during cueing. Finally, we found that a change in frequency of sleep spindles during cued-memory reactivation mediated the relationship between the experimental groups and gains in performance the next day. These findings strongly suggest that cued-memory reactivation during NREM2 sleep triggers an increase in sleep spindle activity that is then related to the consolidation of motor sequence memories., Targeted reactivation of a motor sequence memory through re-exposure with a conditioned olfactory stimulus during the night reveals the specific role of stage 2 non-REM sleep and spindles in the consolidation process., Author Summary There is ample evidence that sleep contributes to the consolidation (from a labile to a robust state) of a memory trace formed through learning of a new motor sequence, such as piano-playing. Sleep, however, is a complex neurophysiological state comprising several phases, and the role that each phase plays in this memory process remains controversial. To address this issue, we used a conditioning paradigm with human volunteers in which an odor was first associated (or not) with the practice of a motor sequence learning task. The odor was then presented again in one of two different sleep phases—rapid-eye movement (REM) or stage 2 non-REM (NREM2)—during the second half of the night, as a means of facilitating reactivation of the memory trace. As predicted, we found that participants cued with the odor during NREM2 showed greater gains in performance (reflecting better consolidation) the following morning compared with those who were cued during REM sleep or who had not previously been exposed to the odor during training. We also observed that reactivation during NREM2 sleep prompted significant changes in a type of brain activity known as sleep spindles. We conclude that NREM2 sleep—and spindles in particular—contribute critically to the consolidation of motor sequence memories.

In human studies, how averaged activation in a brain region relates to human behavior has been extensively investigated. This approach has led to the finding that positive and negative facial preferences are represented by different brain regions. However, using a functional magnetic resonance imaging (fMRI) decoded neurofeedback (DecNef) method, we found that different patterns of neural activations within the cingulate cortex (CC) play roles in representing opposite directions of facial preference. In the present study, while neutrally preferred faces were presented, multi-voxel activation patterns in the CC that corresponded to higher (or lower) preference were repeatedly induced by fMRI DecNef. As a result, previously neutrally preferred faces became more (or less) preferred. We conclude that a different activation pattern in the CC, rather than averaged activation in a different area, represents and suffices to determine positive or negative facial preference. This new approach may reveal the importance of an activation pattern within a brain region in many cognitive functions., A newly developed fMRI method, decoded neurofeedback (DecNef), reveals that specific activation patterns in the cingulate cortex are largely responsible for determining human facial preferences., Author Summary Although it is well studied how averaged activation of a brain region relates to behavior, it is still unclear if specific patterns of activation within regions also relate to cognitive function. In recent years, several methods have been developed for manipulating brain activity in humans. Real-time functional magnetic resonance imaging decoded neurofeedback (fMRI DecNef) is a method that allows the induction of specific patterns of brain activity by measuring the current pattern, comparing this to the pattern to be induced, and giving the subjects feedback on how close the two patterns of neuronal activity are. Using fMRI DecNef, we manipulated the pattern of activation in the cingulate cortex—a part of the cerebral cortex that plays a role in preference to different categories including faces and daily items—and tested whether we could change these preferences. In the experiment, a specific activation pattern in the cingulate cortex corresponding to higher (or lower) preference was induced by fMRI DecNef while subjects were seeing a neutrally preferred face. As a result, these neutrally preferred faces became more (or less) preferred. Our finding suggests that different patterns of activation in the cingulate cortex represent, and are sufficient to determine, different emotional states. Our new approach using fMRI DecNef may reveal the importance of activation patterns within a brain region, rather than activation in a whole region, in many cognitive functions.

In a crowded visual scene, attention must be distributed efficiently and flexibly over time and space to accommodate different contexts. It is well established that selective attention enhances the corresponding neural responses, presumably implying that attention would persistently dwell on the task-relevant item. Meanwhile, recent studies, mostly in divided attentional contexts, suggest that attention does not remain stationary but samples objects alternately over time, suggesting a rhythmic view of attention. However, it remains unknown whether the dynamic mechanism essentially mediates attentional processes at a general level. Importantly, there is also a complete lack of direct neural evidence reflecting whether and how the brain rhythmically samples multiple visual objects during stimulus processing. To address these issues, in this study, we employed electroencephalography (EEG) and a temporal response function (TRF) approach, which can dissociate responses that exclusively represent a single object from the overall neuronal activity, to examine the spatiotemporal characteristics of attention in various attentional contexts. First, attention, which is characterized by inhibitory alpha-band (approximately 10 Hz) activity in TRFs, switches between attended and unattended objects every approximately 200 ms, suggesting a sequential sampling even when attention is required to mostly stay on the attended object. Second, the attentional spatiotemporal pattern is modulated by the task context, such that alpha-mediated switching becomes increasingly prominent as the task requires a more uniform distribution of attention. Finally, the switching pattern correlates with attentional behavioral performance. Our work provides direct neural evidence supporting a generally central role of temporal organization mechanism in attention, such that multiple objects are sequentially sorted according to their priority in attentional contexts. The results suggest that selective attention, in addition to the classically posited attentional “focus,” involves a dynamic mechanism for monitoring all objects outside of the focus. Our findings also suggest that attention implements a space (object)-to-time transformation by acting as a series of concatenating attentional chunks that operate on 1 object at a time., Author summary In a crowded visual scene, attention must be efficiently and flexibly distributed over time and space to accommodate different contexts in a task. Recent studies have proposed that attention is a dynamic process that organizes copious information temporally. However, how the brain coordinates attention among multiple visual objects and whether this dynamic mechanism mediates attention at a general level remain largely unknown. In this study, we analyze electroencephalography (EEG) recordings during a multi-object selective attention task to extract object-specific neuronal responses. We demonstrate that attention rhythmically switches between visual objects every approximately 200 ms. Furthermore, the spatiotemporal sampling profile of attention adaptively changes in various task contexts and correlates with behavioral performance during attention. Our work provides direct neural evidence supporting the idea that multiple objects are sequentially sorted according to their priority in attentional contexts. The results suggest that attention is intrinsically dynamic, acting as a series of concatenating chunks of attention that operate on 1 object at a time to maintain awareness of the whole scene.