Six types of loves differentially recruit reward and social cognition brain areas.

Feelings of love are among the most significant human phenomena. Love informs the formation and maintenance of pair bonds, parent-offspring attachments, and influences relationships with others and even nature. However, little is known about the neural mechanisms of love beyond romantic and maternal types. Here, we characterize the brain areas involved in love for six different objects: romantic partner, one's children, friends, strangers, pets, and nature. We used functional magnetic resonance imaging (fMRI) to measure brain activity, while we induced feelings of love using short stories. Our results show that neural activity during a feeling of love depends on its object. Interpersonal love recruited social cognition brain areas in the temporoparietal junction and midline structures significantly more than love for pets or nature. In pet owners, love for pets activated these same regions significantly more than in participants without pets. Love in closer affiliative bonds was associated with significantly stronger and more widespread activation in the brain's reward system than love for strangers, pets, or nature. We suggest that the experience of love is shaped by both biological and cultural factors, originating from fundamental neurobiological mechanisms of attachment.

Atypical gaze patterns in autistic adults are heterogeneous across but reliable within individuals.

BACKGROUND: Across behavioral studies, autistic individuals show greater variability than typically developing individuals. However, it remains unknown to what extent this variability arises from heterogeneity across individuals, or from unreliability within individuals. Here, we focus on eye tracking, which provides rich dependent measures that have been used extensively in studies of autism. Autistic individuals have an atypical gaze onto both static visual images and dynamic videos that could be leveraged for diagnostic purposes if the above open question could be addressed. METHODS: We tested three competing hypotheses: (1) that gaze patterns of autistic individuals are less reliable or noisier than those of controls, (2) that atypical gaze patterns are individually reliable but heterogeneous across autistic individuals, or (3) that atypical gaze patterns are individually reliable and also homogeneous among autistic individuals. We collected desktop-based eye tracking data from two different full-length television sitcom episodes, at two independent sites (Caltech and Indiana University), in a total of over 150 adult participants (N = 48 autistic individuals with IQ in the normal range, 105 controls) and quantified gaze onto features of the videos using automated computer vision-based feature extraction. RESULTS: We found support for the second of these hypotheses. Autistic people and controls showed equivalently reliable gaze onto specific features of videos, such as faces, so much so that individuals could be identified significantly above chance using a fingerprinting approach from video epochs as short as 2 min. However, classification of participants into diagnostic groups based on their eye tracking data failed to produce clear group classifications, due to heterogeneity in the autistic group. LIMITATIONS: Three limitations are the relatively small sample size, assessment across only two videos (from the same television series), and the absence of other dependent measures (e.g., neuroimaging or genetics) that might have revealed individual-level variability that was not evident with eye tracking. Future studies should expand to larger samples across longer longitudinal epochs, an aim that is now becoming feasible with Internet- and phone-based eye tracking. CONCLUSIONS: These findings pave the way for the investigation of autism subtypes, and for elucidating the specific visual features that best discriminate gaze patterns-directions that will also combine with and inform neuroimaging and genetic studies of this complex disorder.

Classification of emotion categories based on functional connectivity patterns of the human brain.

Neurophysiological and psychological models posit that emotions depend on connections across wide-spread corticolimbic circuits. While previous studies using pattern recognition on neuroimaging data have shown differences between various discrete emotions in brain activity patterns, less is known about the differences in functional connectivity. Thus, we employed multivariate pattern analysis on functional magnetic resonance imaging data (i) to develop a pipeline for applying pattern recognition in functional connectivity data, and (ii) to test whether connectivity patterns differ across emotion categories. Six emotions (anger, fear, disgust, happiness, sadness, and surprise) and a neutral state were induced in 16 participants using one-minute-long emotional narratives with natural prosody while brain activity was measured with functional magnetic resonance imaging (fMRI). We computed emotion-wise connectivity matrices both for whole-brain connections and for 10 previously defined functionally connected brain subnetworks and trained an across-participant classifier to categorize the emotional states based on whole-brain data and for each subnetwork separately. The whole-brain classifier performed above chance level with all emotions except sadness, suggesting that different emotions are characterized by differences in large-scale connectivity patterns. When focusing on the connectivity within the 10 subnetworks, classification was successful within the default mode system and for all emotions. We thus show preliminary evidence for consistently different sustained functional connectivity patterns for instances of emotion categories particularly within the default mode system.

Naturalistic Stimuli in Affective Neuroimaging: A Review.

Naturalistic stimuli such as movies, music, and spoken and written stories elicit strong emotions and allow brain imaging of emotions in close-to-real-life conditions. Emotions are multi-component phenomena: relevant stimuli lead to automatic changes in multiple functional components including perception, physiology, behavior, and conscious experiences. Brain activity during naturalistic stimuli reflects all these changes, suggesting that parsing emotion-related processing during such complex stimulation is not a straightforward task. Here, I review affective neuroimaging studies that have employed naturalistic stimuli to study emotional processing, focusing especially on experienced emotions. I argue that to investigate emotions with naturalistic stimuli, we need to define and extract emotion features from both the stimulus and the observer.

Statistical pattern recognition reveals shared neural signatures for displaying and recognizing specific facial expressions.

Human neuroimaging and behavioural studies suggest that somatomotor 'mirroring' of seen facial expressions may support their recognition. Here we show that viewing specific facial expressions triggers the representation corresponding to that expression in the observer's brain. Twelve healthy female volunteers underwent two separate fMRI sessions: one where they observed and another where they displayed three types of facial expressions (joy, anger and disgust). Pattern classifier based on Bayesian logistic regression was trained to classify facial expressions (i) within modality (trained and tested with data recorded while observing or displaying expressions) and (ii) between modalities (trained with data recorded while displaying expressions and tested with data recorded while observing the expressions). Cross-modal classification was performed in two ways: with and without functional realignment of the data across observing/displaying conditions. All expressions could be accurately classified within and also across modalities. Brain regions contributing most to cross-modal classification accuracy included primary motor and somatosensory cortices. Functional realignment led to only minor increases in cross-modal classification accuracy for most of the examined ROIs. Substantial improvement was observed in the occipito-ventral components of the core system for facial expression recognition. Altogether these results support the embodied emotion recognition model and show that expression-specific somatomotor neural signatures could support facial expression recognition.

Emotions amplify speaker-listener neural alignment.

Individuals often align their emotional states during conversation. Here, we reveal how such emotional alignment is reflected in synchronization of brain activity across speakers and listeners. Two "speaker" subjects told emotional and neutral autobiographical stories while their hemodynamic brain activity was measured with functional magnetic resonance imaging (fMRI). The stories were recorded and played back to 16 "listener" subjects during fMRI. After scanning, both speakers and listeners rated the moment-to-moment valence and arousal of the stories. Time-varying similarity of the blood-oxygenation-level-dependent (BOLD) time series was quantified by intersubject phase synchronization (ISPS) between speaker-listener pairs. Telling and listening to the stories elicited similar emotions across speaker-listener pairs. Arousal was associated with increased speaker-listener neural synchronization in brain regions supporting attentional, auditory, somatosensory, and motor processing. Valence was associated with increased speaker-listener neural synchronization in brain regions involved in emotional processing, including amygdala, hippocampus, and temporal pole. Speaker-listener synchronization of subjective feelings of arousal was associated with increased neural synchronization in somatosensory and subcortical brain regions; synchronization of valence was associated with neural synchronization in parietal cortices and midline structures. We propose that emotion-dependent speaker-listener neural synchronization is associated with emotional contagion, thereby implying that listeners reproduce some aspects of the speaker's emotional state at the neural level.

Emotions as discrete patterns of systemic activity.

Emotions organize human and animal behaviour by automatically adjusting their actions at multiple physiological and behavioural scales. Recently, pattern recognition techniques have emerged as an important tool for quantifying the neural, physiological, and phenomenological organization of emotions in humans. Here we review recent advances in our understanding of the human emotion system from the viewpoint of pattern recognition studies, focussing on neuroimaging experiments. These studies suggest, in general, clear and consistent categorical structure of emotions across multiple levels of analysis spanning expressive behaviour, subjective experiences, physiological activity, and neural activation patterns. In particular, the neurophysiological data support the view of multiple discrete emotion systems that are organized in a distributed fashion across the brain, with no clear one-to-one mapping between emotions and brain regions. However, these techniques are inherently limited by the choice of a priori emotion categories used in the studies, and cannot provide direct causal evidence for brain activity-emotion relationships.

Reproducibility of importance extraction methods in neural network based fMRI classification.

Recent advances in machine learning allow faster training, improved performance and increased interpretability of classification techniques. Consequently, their application in neuroscience is rapidly increasing. While classification approaches have proved useful in functional magnetic resonance imaging (fMRI) studies, there are concerns regarding extraction, reproducibility and visualization of brain regions that contribute most significantly to the classification. We addressed these issues using an fMRI classification scheme based on neural networks and compared a set of methods for extraction of category-related voxel importances in three simulated and two empirical datasets. The simulation data revealed that the proposed scheme successfully detects spatially distributed and overlapping activation patterns upon successful classification. Application of the proposed classification scheme to two previously published empirical fMRI datasets revealed robust importance maps that extensively overlap with univariate maps but also provide complementary information. Our results demonstrate increased statistical power of importance maps compared to univariate approaches for both detection of overlapping patterns and patterns with weak univariate information.

Distributed affective space represents multiple emotion categories across the human brain.

The functional organization of human emotion systems as well as their neuroanatomical basis and segregation in the brain remains unresolved. Here, we used pattern classification and hierarchical clustering to characterize the organization of a wide array of emotion categories in the human brain. We induced 14 emotions (6 'basic', e.g. fear and anger; and 8 'non-basic', e.g. shame and gratitude) and a neutral state using guided mental imagery while participants' brain activity was measured with functional magnetic resonance imaging (fMRI). Twelve out of 14 emotions could be reliably classified from the haemodynamic signals. All emotions engaged a multitude of brain areas, primarily in midline cortices including anterior and posterior cingulate gyri and precuneus, in subcortical regions, and in motor regions including cerebellum and premotor cortex. Similarity of subjective emotional experiences was associated with similarity of the corresponding neural activation patterns. We conclude that different basic and non-basic emotions have distinguishable neural bases characterized by specific, distributed activation patterns in widespread cortical and subcortical circuits. Regionally differentiated engagement of these circuits defines the unique neural activity pattern and the corresponding subjective feeling associated with each emotion.

Effects of spatial smoothing on functional brain networks.

Graph-theoretical methods have rapidly become a standard tool in studies of the structure and function of the human brain. Whereas the structural connectome can be fairly straightforwardly mapped onto a complex network, there are more degrees of freedom in constructing networks that represent functional connections between brain areas. For functional magnetic resonance imaging (fMRI) data, such networks are typically built by aggregating the blood-oxygen-level dependent signal time series of voxels into larger entities (such as Regions of Interest in some brain atlas) and determining their connection strengths from some measure of time-series correlations. Although it is evident that the outcome must be affected by how the voxel-level time series are treated at the preprocessing stage, there is a lack of systematic studies of the effects of preprocessing on network structure. Here, we focus on the effects of spatial smoothing, a standard preprocessing method for fMRI. We apply various levels of spatial smoothing to resting-state fMRI data and measure the changes induced in functional networks. We show that the level of spatial smoothing clearly affects the degrees and other centrality measures of functional network nodes; these changes are non-uniform, systematic, and depend on the geometry of the brain. The composition of the largest connected network component is also affected in a way that artificially increases the similarity of the networks of different subjects. Our conclusion is that wherever possible, spatial smoothing should be avoided when preprocessing fMRI data for network analysis.

Consistency of Regions of Interest as nodes of fMRI functional brain networks.

The functional network approach, where fMRI BOLD time series are mapped to networks depicting functional relationships between brain areas, has opened new insights into the function of the human brain. In this approach, the choice of network nodes is of crucial importance. One option is to consider fMRI voxels as nodes. This results in a large number of nodes, making network analysis and interpretation of results challenging. A common alternative is to use predefined clusters of anatomically close voxels, Regions of Interest (ROIs). This approach assumes that voxels within ROIs are functionally similar. Because these two approaches result in different network structures, it is crucial to understand what happens to network connectivity when moving from the voxel level to the ROI level. We show that the consistency of ROIs, defined as the mean Pearson correlation coefficient between the time series of their voxels, varies widely in resting-state experimental data. Therefore the assumption of similar voxel dynamics within each ROI does not generally hold. Further, the time series of low-consistency ROIs may be highly correlated, resulting in spurious links in ROI-level networks. Based on these results, we recommend that averaging BOLD signals over anatomically defined ROIs should be carefully considered.

Discrete Neural Signatures of Basic Emotions.

Categorical models of emotions posit neurally and physiologically distinct human basic emotions. We tested this assumption by using multivariate pattern analysis (MVPA) to classify brain activity patterns of 6 basic emotions (disgust, fear, happiness, sadness, anger, and surprise) in 3 experiments. Emotions were induced with short movies or mental imagery during functional magnetic resonance imaging. MVPA accurately classified emotions induced by both methods, and the classification generalized from one induction condition to another and across individuals. Brain regions contributing most to the classification accuracy included medial and inferior lateral prefrontal cortices, frontal pole, precentral and postcentral gyri, precuneus, and posterior cingulate cortex. Thus, specific neural signatures across these regions hold representations of different emotional states in multimodal fashion, independently of how the emotions are induced. Similarity of subjective experiences between emotions was associated with similarity of neural patterns for the same emotions, suggesting a direct link between activity in these brain regions and the subjective emotional experience.

Memory binding and white matter integrity in familial Alzheimer's disease.

Binding information in short-term and long-term memory are functions sensitive to Alzheimer's disease. They have been found to be affected in patients who meet criteria for familial Alzheimer's disease due to the mutation E280A of the PSEN1 gene. However, only short-term memory binding has been found to be affected in asymptomatic carriers of this mutation. The neural correlates of this dissociation are poorly understood. The present study used diffusion tensor magnetic resonance imaging to investigate whether the integrity of white matter structures could offer an account. A sample of 19 patients with familial Alzheimer's disease, 18 asymptomatic carriers and 21 non-carrier controls underwent diffusion tensor magnetic resonance imaging, neuropsychological and memory binding assessment. The short-term memory binding task required participants to detect changes across two consecutive screens displaying arrays of shapes, colours, or shape-colour bindings. The long-term memory binding task was a Paired Associates Learning Test. Performance on these tasks were entered into regression models. Relative to controls, patients with familial Alzheimer's disease performed poorly on both memory binding tasks. Asymptomatic carriers differed from controls only in the short-term memory binding task. White matter integrity explained poor memory binding performance only in patients with familial Alzheimer's disease. White matter water diffusion metrics from the frontal lobe accounted for poor performance on both memory binding tasks. Dissociations were found in the genu of corpus callosum which accounted for short-term memory binding impairments and in the hippocampal part of cingulum bundle which accounted for long-term memory binding deficits. The results indicate that white matter structures in the frontal and temporal lobes are vulnerable to the early stages of familial Alzheimer's disease and their damage is associated with impairments in two memory binding functions known to be markers for Alzheimer's disease.

Emotional speech synchronizes brains across listeners and engages large-scale dynamic brain networks.

Speech provides a powerful means for sharing emotions. Here we implement novel intersubject phase synchronization and whole-brain dynamic connectivity measures to show that networks of brain areas become synchronized across participants who are listening to emotional episodes in spoken narratives. Twenty participants' hemodynamic brain activity was measured with functional magnetic resonance imaging (fMRI) while they listened to 45-s narratives describing unpleasant, neutral, and pleasant events spoken in neutral voice. After scanning, participants listened to the narratives again and rated continuously their feelings of pleasantness-unpleasantness (valence) and of arousal-calmness. Instantaneous intersubject phase synchronization (ISPS) measures were computed to derive both multi-subject voxel-wise similarity measures of hemodynamic activity and inter-area functional dynamic connectivity (seed-based phase synchronization, SBPS). Valence and arousal time series were subsequently used to predict the ISPS and SBPS time series. High arousal was associated with increased ISPS in the auditory cortices and in Broca's area, and negative valence was associated with enhanced ISPS in the thalamus, anterior cingulate, lateral prefrontal, and orbitofrontal cortices. Negative valence affected functional connectivity of fronto-parietal, limbic (insula, cingulum) and fronto-opercular circuitries, and positive arousal affected the connectivity of the striatum, amygdala, thalamus, cerebellum, and dorsal frontal cortex. Positive valence and negative arousal had markedly smaller effects. We propose that high arousal synchronizes the listeners' sound-processing and speech-comprehension networks, whereas negative valence synchronizes circuitries supporting emotional and self-referential processing.