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1.  Neural basis of irony comprehension in children with autism: the role of prosody and context 
Brain : a journal of neurology  2006;129(0 4):932-943.
While individuals with autism spectrum disorders (ASD) are typically impaired in interpreting the communicative intent of others, little is known about the neural bases of higher-level pragmatic impairments. Here, we used functional MRI (fMRI) to examine the neural circuitry underlying deficits in understanding irony in high-functioning children with ASD. Participants listened to short scenarios and decided whether the speaker was sincere or ironic. Three types of scenarios were used in which we varied the information available to guide this decision. Scenarios included (i) both knowledge of the event outcome and strong prosodic cues (sincere or sarcastic intonation), (ii) prosodic cues only or (iii) knowledge of the event outcome only. Although children with ASD performed well above chance, they were less accurate than typically developing (TD) children at interpreting the communicative intent behind a potentially ironic remark, particularly with regard to taking advantage of available contextual information. In contrast to prior research showing hypoactivation of regions involved in understanding the mental states of others, children with ASD showed significantly greater activity than TD children in the right inferior frontal gyrus (IFG) as well as in bilateral temporal regions. Increased activity in the ASD group fell within the network recruited in the TD group and may reflect more effortful processing needed to interpret the intended meaning of an utterance. These results confirm that children with ASD have difficulty interpreting the communicative intent of others and suggest that these individuals can recruit regions activated as part of the normative neural circuitry when task demands require explicit attention to socially relevant cues.
PMCID: PMC3713234  PMID: 16481375
autism; brain development; fMRI; language pragmatics; social cognition
2.  Atypical Neural Processing of Ironic and Sincere Remarks in Children and Adolescents with Autism Spectrum Disorders 
Metaphor and symbol  2012;27(1):70-92.
Individuals with ASD show consistent impairment in processing pragmatic language when attention to multiple social cues (e.g., facial expression, tone of voice) is often needed to navigate social interactions. Building upon prior fMRI work examining how facial affect and prosodic cues are used to infer a speaker's communicative intent, the authors examined whether children and adolescents with ASD differ from typically developing (TD) controls in their processing of sincere versus ironic remarks. At the behavioral level, children and adolescents with ASD and matched TD controls were able to determine whether a speaker's remark was sincere or ironic equally well, with both groups showing longer response times for ironic remarks. At the neural level, for both sincere and ironic scenarios, an extended cortical network—including canonical language areas in the left hemisphere and their right hemisphere counterparts—was activated in both groups, albeit to a lesser degree in the ASD sample. Despite overall similar patterns of activity observed for the two conditions in both groups, significant modulation of activity was detected when directly comparing sincere and ironic scenarios within and between groups. While both TD and ASD groups showed significantly greater activity in several nodes of this extended network when processing ironic versus sincere remarks, increased activity was largely confined to left language areas in TD controls, whereas the ASD sample showed a more bilateral activation profile which included both language and “theory of mind” areas (i.e., ventromedial prefrontal cortex). These findings suggest that, for high-functioning individuals with ASD, increased activity in right hemisphere homologues of language areas in the left hemisphere, as well as regions involved in social cognition, may reflect compensatory mechanisms supporting normative behavioral task performance.
PMCID: PMC3909704  PMID: 24497750
3.  Isn’t it ironic? Neural Correlates of Irony Comprehension in Schizophrenia 
PLoS ONE  2013;8(9):e74224.
Ironic remarks are frequent in everyday language and represent an important form of social cognition. Increasing evidence indicates a deficit in comprehension in schizophrenia. Several models for defective comprehension have been proposed, including possible roles of the medial prefrontal lobe, default mode network, inferior frontal gyri, mirror neurons, right cerebral hemisphere and a possible mediating role of schizotypal personality traits. We investigated the neural correlates of irony comprehension in schizophrenia by using event-related functional magnetic resonance imaging (fMRI). In a prosody-free reading paradigm, 15 female patients with schizophrenia and 15 healthy female controls silently read ironic and literal text vignettes during fMRI. Each text vignette ended in either an ironic (n = 22) or literal (n = 22) statement. Ironic and literal text vignettes were matched for word frequency, length, grammatical complexity, and syntax. After fMRI, the subjects performed an off-line test to detect error rate. In this test, the subjects indicated by button press whether the target sentence has ironic, literal, or meaningless content. Schizotypal personality traits were assessed using the German version of the schizotypal personality questionnaire (SPQ). Patients with schizophrenia made significantly more errors than did the controls (correct answers, 85.3% vs. 96.3%) on a behavioural level. Patients showed attenuated blood oxygen level-dependent (BOLD) response during irony comprehension mainly in right hemisphere temporal regions (ironic>literal contrast) and in posterior medial prefrontal and left anterior insula regions (for ironic>visual baseline, but not for literal>visual baseline). In patients with schizophrenia, the parahippocampal gyrus showed increased activation. Across all subjects, BOLD response in the medial prefrontal area was negatively correlated with the SPQ score. These results highlight the role of the posterior medial prefrontal and right temporal regions in defective irony comprehension in schizophrenia and the mediating role of schizotypal personality traits.
PMCID: PMC3769349  PMID: 24040207
4.  Individuals with Autism Spectrum Disorders Do Not Use Social Stereotypes in Irony Comprehension 
PLoS ONE  2014;9(4):e95568.
Social and communication impairments are part of the essential diagnostic criteria used to define Autism Spectrum Disorders (ASDs). Difficulties in appreciating non-literal speech, such as irony in ASDs have been explained as due to impairments in social understanding and in recognizing the speaker’s communicative intention. It has been shown that social-interactional factors, such as a listener’s beliefs about the speaker’s attitudinal propensities (e.g., a tendency to use sarcasm, to be mocking, less sincere and more prone to criticism), as conveyed by an occupational stereotype, do influence a listener’s interpretation of potentially ironic remarks. We investigate the effect of occupational stereotype on irony detection in adults with High Functioning Autism or Asperger Syndrome (HFA/AS) and a comparison group of typically developed adults. We used a series of verbally presented stories containing ironic or literal utterances produced by a speaker having either a “sarcastic” or a “non-sarcastic” occupation. Although individuals with HFA/AS were able to recognize ironic intent and occupational stereotypes when the latter are made salient, stereotype information enhanced irony detection and modulated its social meaning (i.e., mockery and politeness) only in comparison participants. We concluded that when stereotype knowledge is not made salient, it does not automatically affect pragmatic communicative processes in individuals with HFA/AS.
PMCID: PMC3991690  PMID: 24748103
5.  Reading Affect in the Face and Voice 
Archives of general psychiatry  2007;64(6):698-708.
Understanding a speaker’s communicative intent in everyday interactions is likely to draw on cues such as facial expression and tone of voice. Prior research has shown that individuals with autism spectrum disorders (ASD) show reduced activity in brain regions that respond selectively to the face and voice. However, there is also evidence that activity in key regions can be increased if task demands allow for explicit processing of emotion.
To examine the neural circuitry underlying impairments in interpreting communicative intentions in ASD using irony comprehension as a test case, and to determine whether explicit instructions to attend to facial expression and tone of voice will elicit more normative patterns of brain activity.
Design, Setting, and Participants
Eighteen boys with ASD (aged 7–17 years, full-scale IQ >70) and 18 typically developing (TD) boys underwent functional magnetic resonance imaging at the Ahmanson-Lovelace Brain Mapping Center, University of California, Los Angeles.
Main Outcome Measures
Blood oxygenation level– dependent brain activity during the presentation of short scenarios involving irony. Behavioral performance (accuracy and response time) was also recorded.
Reduced activity in the medial prefrontal cortex and right superior temporal gyrus was observed in children with ASD relative to TD children during the perception of potentially ironic vs control scenarios. Importantly, a significant group X condition interaction in the medial prefrontal cortex showed that activity was modulated by explicit instructions to attend to facial expression and tone of voice only in the ASD group. Finally, medial prefrontal cortex activity was inversely related to symptom severity in children with ASD such that children with greater social impairment showed less activity in this region.
Explicit instructions to attend to facial expression and tone of voice can elicit increased activity in the medial prefrontal cortex, part of a network important for understanding the intentions of others, in children with ASD. These findings suggest a strategy for future intervention research.
PMCID: PMC3713233  PMID: 17548751
6.  Detecting Sarcasm from Paralinguistic Cues: Anatomic and Cognitive Correlates in Neurodegenerative Disease 
NeuroImage  2009;47(4):2005-2015.
While sarcasm can be conveyed solely through contextual cues such as counterfactual or echoic statements, face-to-face sarcastic speech may be characterized by specific paralinguistic features that alert the listener to interpret the utterance as ironic or critical, even in the absence of contextual information. We investigated the neuroanatomy underlying failure to understand sarcasm from dynamic vocal and facial paralinguistic cues. Ninety subjects (20 frontotemporal dementia, 11 semantic dementia [SemD], 4 progressive nonfluent aphasia, 27 Alzheimer’s disease, 6 corticobasal degeneration, 9 progressive supranuclear palsy, 13 healthy older controls) were tested using the Social Inference – Minimal subtest of The Awareness of Social Inference Test (TASIT). Subjects watched brief videos depicting sincere or sarcastic communication and answered yes-no questions about the speaker’s intended meaning. All groups interpreted Sincere (SIN) items normally, and only the SemD group was impaired on the Simple Sarcasm (SSR) condition. Patients failing the SSR performed more poorly on dynamic emotion recognition tasks and had more neuropsychiatric disturbances, but had better verbal and visuospatial working memory than patients who comprehended sarcasm. Voxel-based morphometry analysis of SSR scores in SPM5 demonstrated that poorer sarcasm comprehension was predicted by smaller volume in bilateral posterior parahippocampii (PHc), temporal poles, and R medial frontal pole (pFWE<0.05). This study provides lesion data suggesting that the PHc may be involved in recognizing a paralinguistic speech profile as abnormal, leading to interpretive processing by the temporal poles and right medial frontal pole that identifies the social context as sarcastic, and recognizes the speaker’s paradoxical intentions.
PMCID: PMC2720152  PMID: 19501175
7.  Cultural and linguistic effects on neural bases of ‘Theory of Mind’ in American and Japanese children 
Brain research  2007;1164:95-107.
Theory of mind (ToM) has been defined as our ability to predict behaviors of others in terms of their underlying intentions. While the developmental trajectory of ToM had been thought to be invariant across cultures, several ToM studies conducted outside the Anglo-American cultural or linguistic milieus have obtained mixed results. To examine effects of culture/language on the development of neural bases of ToM, we studied 12 American monolingual children and 12 Japanese bilingual children with second-order false-belief story and cartoon tasks, using functional magnetic resonance imaging (fMRI). While a few brain regions such as ventro-medial prefrontal cortex (vmPFC) and precuneus were recruited by the both cultural/linguistic groups, several brain areas including inferior frontal gyrus (IFG) and temporo-parietal junction (TPJ) were employed in a culture/language-dependent manner during the ToM tasks. These results suggest that the neural correlates of ToM may begin to vary depending upon cultural/linguistic background from early in life.
PMCID: PMC2964053  PMID: 17643400
8.  Structural brain alterations associated with dyslexia predate reading onset 
NeuroImage  2010;57(3):742-749.
Functional magnetic resonance imaging studies have reported reduced activation in parietotemporal and occipitotemporal areas in adults and children with developmental dyslexia compared to controls during reading and reading related tasks. These patterns of regionally reduced activation have been linked to behavioral impairments of reading-related processes (e.g., phonological skills and rapid automatized naming). The observed functional and behavioral differences in individuals with developmental dyslexia have been complemented by reports of reduced gray matter in left parietotemporal, occipitotemporal areas, fusiform and lingual gyrus and the cerebellum. An important question for education is whether these neural differences are present before reading is taught. Developmental dyslexia can only be diagnosed after formal reading education starts. However, here we investigate whether the previously detected gray matter alterations in adults and children with developmental dyslexia can already be observed in a small group of pre-reading children with a family-history of developmental dyslexia compared to age and IQ-matched children without a family-history (N = 20/mean age: 5:9 years; age range 5:1–6:5 years). Voxel-based morphometry revealed significantly reduced gray matter volume indices for pre-reading children with, compared to children without, a family-history of developmental dyslexia in left occipitotemporal, bilateral parietotemporal regions, left fusiform gyrus and right lingual gyrus. Gray matter volume indices in left hemispheric occipitotemporal and parietotemporal regions of interest also correlated positively with rapid automatized naming. No differences between the two groups were observed in frontal and cerebellar regions. This discovery in a small group of children suggests that previously described functional and structural alterations in developmental dyslexia may not be due to experience-dependent brain changes but may be present at birth or develop in early childhood prior to reading onset. Further studies using larger sample sizes and longitudinal analyses are needed in order to determine whether the identified structural alterations may be utilized as structural markers for the early identification of children at risk, which may prevent the negative clinical, social and psychological outcome of developmental dyslexia.
PMCID: PMC3499031  PMID: 20884362
fMRI; Children; Dyslexia; Voxel-based morphometry; Reading; Family history
9.  Brain correlates of discourse processing: An fMRI investigation of irony and conventional metaphor comprehension 
Neuropsychologia  2006;44(12):2348-2359.
Higher levels of discourse processing evoke patterns of cognition and brain activation that extend beyond the literal comprehension of sentences. We used fMRI to examine brain activation patterns while 16 healthy participants read brief three-sentence stories that concluded with either a literal, metaphoric, or ironic sentence. The fMRI images acquired during the reading of the critical sentence revealed a selective response of the brain to the two types of nonliteral utterances. Metaphoric utterances resulted in significantly higher levels of activation in the left inferior frontal gyrus and in bilateral inferior temporal cortex than the literal and ironic utterances. Ironic statements resulted in significantly higher activation levels than literal statements in the right superior and middle temporal gyri, with metaphoric statements resulting in intermediate levels in these regions. The findings show differential hemispheric sensitivity to these aspects of figurative language, and are relevant to models of the functional cortical architecture of language processing in connected discourse.
PMCID: PMC1894906  PMID: 16806316
Figurative language; Irony; Metaphor; Pragmatics; fMRI
10.  Children’s and adults’ neural bases of verbal and nonverbal ‘Theory of Mind’ 
Neuropsychologia  2007;45(7):1522-1532.
Theory of mind (ToM) - our ability to predict behaviors of others in terms of their underlying intentions - has been examined through verbal and nonverbal false-belief (FB) tasks. Previous brain imaging studies of ToM in adults have implicated medial prefrontal cortex (mPFC) and temporo-parietal junction (TPJ) for adults’ ToM ability. To examine age and modality related differences and similarities in neural correlates of ToM, we tested 16 adults (18-40 years-old) and 12 children (8-12 years-old) with verbal (story) and nonverbal (cartoon) FB tasks, using functional magnetic resonance imaging (fMRI). Both age groups showed significant activity in the TPJ bilaterally and right inferior parietal lobule (IPL) in a modality-independent manner, indicating that these areas are important for ToM during both adulthood and childhood, regardless of modality. We also found significant age-related differences in the ToM condition-specific activity for the story and cartoon tasks in the left inferior frontal gyrus (IFG) and left TPJ. These results suggest that depending on the modality adults may utilize different brain regions from children in understanding ToM.
PMCID: PMC1868677  PMID: 17208260
fMRI; Theory of Mind; Cognitive Development; Language; Temporo-parietal junction
11.  What’s behind a P600? Integration Operations during Irony Processing 
PLoS ONE  2013;8(6):e66839.
The combined knowledge of word meanings and grammatical rules does not allow a listener to grasp the intended meaning of a speaker’s utterance. Pragmatic inferences on the part of the listener are also required. The present work focuses on the processing of ironic utterances (imagine a slow day being described as “really productive”) because these clearly require the listener to go beyond the linguistic code. Such utterances are advantageous experimentally because they can serve as their own controls in the form of literal sentences (now imagine an active day being described as “really productive”) as we employ techniques from electrophysiology (EEG). Importantly, the results confirm previous ERP findings showing that irony processing elicits an enhancement of the P600 component (Regel et al., 2011). More original are the findings drawn from Time Frequency Analysis (TFA) and especially the increase of power in the gamma band in the 280–400 time-window, which points to an integration among different streams of information relatively early in the comprehension of an irony. This represents a departure from traditional accounts of language processing which generally view pragmatic inferences as late-arriving. We propose that these results indicate that unification operations between the linguistic code and contextual information play a critical role throughout the course of irony processing and earlier than previously thought.
PMCID: PMC3691266  PMID: 23826155
12.  Comprehension of insincere communication in neurodegenerative disease: Lies, sarcasm, and theory of mind 
Comprehension of insincere communication is an important aspect of social cognition requiring visual perspective taking, emotion reading, and understanding others’ thoughts, opinions, and intentions. Someone who is lying intends to hide their insincerity from the listener, while a sarcastic speaker wants the listener to recognize they are speaking insincerely. We investigated whether face-to-face testing of comprehending insincere communication would effectively discriminate among neurodegenerative disease patients with different patterns of real-life social deficits. We examined ability to comprehend lies and sarcasm from a third-person perspective, using contextual cues, in 102 patients with one of four neurodegenerative diseases (frontotemporal dementia [bvFTD], Alzheimer’s disease [AD], progressive supranuclear palsy [PSP], and vascular cognitive impairment) and 77 healthy older adults (NC). Participants answered questions about videos depicting social interactions involving deceptive, sarcastic, or sincere speech using The Awareness of Social Inference Test. All subjects equally understood sincere remarks, but bvFTD patients displayed impaired comprehension of lies and sarcasm compared with NCs. In other groups, impairment was not disease-specific but was proportionate to general cognitive impairment. Analysis of the task components revealed that only bvFTD patients were impaired on perspective taking and emotion reading elements and that both bvFTD and PSP patients had impaired ability to represent others’ opinions and intentions (i.e., theory of mind). Test performance correlated with informants’ ratings of subjects’ empathy, perspective taking and neuropsychiatric symptoms in everyday life. Comprehending insincere communication is complex and requires multiple cognitive and emotional processes vulnerable across neurodegenerative diseases. However, bvFTD patients show uniquely focal and severe impairments at every level of theory of mind and emotion reading, leading to an inability to identify obvious examples of deception and sarcasm. This is consistent with studies suggesting this disease targets a specific neural network necessary for perceiving social salience and predicting negative social outcomes.
PMCID: PMC3257415  PMID: 21978867
social cognition; neurodegenerative disease; frontotemporal dementia; lies; sarcasm; theory of mind
13.  Neural deficits in second language reading: fMRI evidence from Chinese children with English reading impairment 
NeuroImage  2010;57(3):760-770.
In alphabetic language systems, converging evidence indicates that developmental dyslexia represents a disorder of phonological processing both behaviorally and neurobiologically. However, it is still unknown whether, impaired phonological processing remains the core deficit of impaired English reading in individuals with English as their second language and how it is represented in the neural cortex. Using functional magnetic resonance imaging, the present study investigated the neural responses to letter rhyming judgment (phonological task) and letter same/different judgment (orthographic task) in Chinese school children with English and Chinese reading impairment compared to typically developing children. Whole brain analyses with multiple comparison correction revealed reduced activation within the left lingual/calcarine gyrus during orthographic processing in children with reading impairment compared to typical readers. An independent region of interest analysis showed reduced activation in occipitotemporal regions during orthographic processing, and reduced activation in parietotemporal regions during phonological processing, consistent with previous studies in English native speakers. These results suggest that similar neural deficits are involved for impaired phonological processing in English as both the first and the second language acquired. These findings pose implications for reading remediation, educational curriculum design, and educational policy for second language learners.
PMCID: PMC3499033  PMID: 21146615
Children; impaired reading; Phonological processing; Orthographic processing; Second language learning; fMRI developmental dyslexia
14.  A Functional Imaging Study of Self-Regulatory Capacities in Persons Who Stutter 
PLoS ONE  2014;9(2):e89891.
Developmental stuttering is a disorder of speech fluency with an unknown pathogenesis. The similarity of its phenotype and natural history with other childhood neuropsychiatric disorders of frontostriatal pathology suggests that stuttering may have a closely related pathogenesis. We investigated in this study the potential involvement of frontostriatal circuits in developmental stuttering. We collected functional magnetic resonance imaging data from 46 persons with stuttering and 52 fluent controls during performance of the Simon Spatial Incompatibility Task. We examined differences between the two groups of blood-oxygen-level-dependent activation associated with two neural processes, the resolution of cognitive conflict and the context-dependent adaptation to changes in conflict. Stuttering speakers and controls did not differ on behavioral performance on the task. In the presence of conflict-laden stimuli, however, stuttering speakers activated more strongly the cingulate cortex, left anterior prefrontal cortex, right medial frontal cortex, left supplementary motor area, right caudate nucleus, and left parietal cortex. The magnitude of activation in the anterior cingulate cortex correlated inversely in stuttering speakers with symptom severity. Stuttering speakers also showed blunted activation during context-dependent adaptation in the left dorsolateral prefrontal cortex, a brain region that mediates cross-temporal contingencies. Frontostriatal hyper-responsivity to conflict resembles prior findings in other disorders of frontostriatal pathology, and therefore likely represents a general mechanism supporting functional compensation for an underlying inefficiency of neural processing in these circuits. The reduced activation of dorsolateral prefrontal cortex likely represents the inadequate readiness of stuttering speakers to execute a sequence of motor responses.
PMCID: PMC3937393  PMID: 24587104
15.  Brain activity and desire for internet video game play 
Comprehensive psychiatry  2011;52(1):88-95.
Recent studies have suggested that the brain circuitry mediating cue induced desire for video games is similar to that elicited by cues related to drugs and alcohol. We hypothesized that desire for internet video games during cue presentation would activate similar brain regions to those which have been linked with craving for drugs or pathological gambling.
This study involved the acquisition of diagnostic MRI and fMRI data from 19 healthy male adults (ages 18–23 years) following training and a standardized 10-day period of game play with a specified novel internet video game, “War Rock” (K-network®). Using segments of videotape consisting of five contiguous 90-second segments of alternating resting, matched control and video game-related scenes, desire to play the game was assessed using a seven point visual analogue scale before and after presentation of the videotape.
In responding to internet video game stimuli, compared to neutral control stimuli, significantly greater activity was identified in left inferior frontal gyrus, left parahippocampal gyrus, right and left parietal lobe, right and left thalamus, and right cerebellum (FDR <0.05, p<0.009243). Self-reported desire was positively correlated with the beta values of left inferior frontal gyrus, left parahippocampal gyrus, and right and left thalamus. Compared to the general players, members who played more internet video game (MIGP) cohort showed significantly greater activity in right medial frontal lobe, right and left frontal pre-central gyrus, right parietal post-central gyrus, right parahippocampal gyrus, and left parietal precuneus gyrus. Controlling for total game time, reported desire for the internet video game in the MIGP cohort was positively correlated with activation in right medial frontal lobe and right parahippocampal gyrus.
The present findings suggest that cue-induced activation to internet video game stimuli may be similar to that observed during cue presentation in persons with substance dependence or pathological gambling. In particular, cues appear to commonly elicit activity in the dorsolateral prefrontal, orbitofrontal cortex, parahippocampal gyrus, and thalamus.
PMCID: PMC3039876  PMID: 21220070
internet video game play; functional MRI; frontal cortex; parahippocampal gyrus; thalamus
16.  24-hr smoking abstinence potentiates fMRI-BOLD activation to smoking cues in cerebral cortex and dorsal striatum 
Psychopharmacology  2008;204(1):25-35.
Exposure to smoking-related cues can trigger relapse in smokers attempting to maintain abstinence.
In the present study we evaluated the effect of 24-hr smoking abstinence on brain responses to smoking-related cues using functional magnetic resonance imaging (fMRI).
Eighteen adult smokers underwent fMRI scanning following smoking as usual (satiated condition) and following 24-hr abstinence (abstinent condition). During scanning they viewed blocks of photographic smoking and control cues.
Following abstinence, greater activation was found in response to smoking cues compared to control cues in parietal (BA 7/31), frontal (BA 8/9), occipital (BA 19) and central (BA 4) cortical regions and in dorsal striatum (putamen) and thalamus. In contrast, no smoking cue > control cue activations were observed following smoking as usual. Direct comparisons between conditions (satiated vs. abstinent) showed greater brain reactivity in response to smoking cues following abstinence. In addition, positive correlations between pre-scan craving in the abstinent condition and smoking cue activation were observed in right dorsomedial prefrontal cortex (dmPFC) including superior frontal gyrus (BA 6/10), anterior cingulate gyrus (BA 32) and supplementary motor area (BA 6).
The present findings indicate smoking abstinence significantly potentiates neural responses to smoking-related cues in brain regions subserving visual sensory processing, attention and action planning. Moreover, greater abstinence-induced craving was significantly correlated with increased smoking cue activation in dmPFC areas involved in action planning and decision making. These findings suggest that drug abstinence can increase the salience of conditioned cues which is consistent with incentive-motivation models of addiction.
PMCID: PMC2810714  PMID: 19107465
cue-reactivity; craving; nicotine dependence; fMRI; smoking; dorsal striatum
17.  The Role of Orbitofrontal Cortex in Processing Empathy Stories in 4- to 8-Year-Old Children 
This study investigates the neuronal correlates of empathic processing in children aged 4–8 years, an age range discussed to be crucial for the development of empathy. Empathy, defined as the ability to understand and share another person's inner life, consists of two components: affective (emotion-sharing) and cognitive empathy (Theory of Mind). We examined the hemodynamic responses of preschool and school children (N = 48), while they processed verbal (auditory) and non-verbal (cartoons) empathy stories in a passive following paradigm, using functional Near-Infrared Spectroscopy. To control for the two types of empathy, children were presented blocks of stories eliciting either affective or cognitive empathy, or neutral scenes which relied on the understanding of physical causalities. By contrasting the activations of the younger and older children, we expected to observe developmental changes in brain activations when children process stories eliciting empathy in either stimulus modality toward a greater involvement of anterior frontal brain regions. Our results indicate that children's processing of stories eliciting affective and cognitive empathy is associated with medial and bilateral orbitofrontal cortex (OFC) activation. In contrast to what is known from studies using adult participants, no additional recruitment of posterior brain regions was observed, often associated with the processing of stories eliciting empathy. Developmental changes were found only for stories eliciting affective empathy with increased activation, in older children, in medial OFC, left inferior frontal gyrus, and the left dorsolateral prefrontal cortex. Activations for the two modalities differ only little, with non-verbal presentation of the stimuli having a greater impact on empathy processing in children, showing more similarities to adult processing than the verbal one. This might be caused by the fact that non-verbal processing develops earlier in life and is more familiar.
PMCID: PMC3110480  PMID: 21687450
OFC; cognitive empathy; affective empathy; children; fNIRS; verbal; non-verbal
Social neuroscience  2013;8(4):291-304.
The developmental origin of sex differences in adult brain function is poorly understood. Elucidating neural mechanisms underlying comparable cognitive functionality in both children and adults is required to address this gap. Humor appreciation represents a particularly relevant target for such developmental research because explanatory theories apply across the life span and underlying neurocircuitry shows sex differences in adults. As a positive mood state, humor is also of interest due to sex differences in rates of depression, a disorder afflicting twice as many women as men. In this study, we employed fMRI to investigate brain responses to funny versus positive (and neutral) video clips in 22 children ages 6 to 13 years, including 8 sibling pairs. Our data revealed increased activity to funny clips in bilateral temporo-occipital cortex, midbrain, and amygdala in girls. Conversely, we found heightened activation to positive clips in bilateral inferior parietal lobule, fusiform gyrus, inferior frontal gyrus, amygdala, and ventromedial prefrontal cortex in boys. Many of these effects persisted when looking at sibling-pairs only. We interpret such findings as reflecting the presence of early sex divergence in reward saliency / expectation and stimulus relevance attribution. These findings are discussed in the context of evolutionary and developmental theories of humor function.
PMCID: PMC3717405  PMID: 23672302
Humor Appreciation; Sex Differences; Reward; Children; fMRI
19.  Gesture in the developing brain 
Developmental science  2011;15(2):165-180.
Speakers convey meaning not only through words, but also through gestures. Although children are exposed to co-speech gestures from birth, we do not know how the developing brain comes to connect meaning conveyed in gesture with speech. We used functional magnetic resonance imaging (fMRI) to address this question and scanned 8- to 11-year-old children and adults listening to stories accompanied by hand movements, either meaningful co-speech gestures or meaningless self-adaptors. When listening to stories accompanied by both types of hand movements, both children and adults recruited inferior frontal, inferior parietal, and posterior temporal brain regions known to be involved in processing language not accompanied by hand movements. There were, however, age-related differences in activity in posterior superior temporal sulcus (STSp), inferior frontal gyrus, pars triangularis (IFGTr), and posterior middle temporal gyrus (MTGp) regions previously implicated in processing gesture. Both children and adults showed sensitivity to the meaning of hand movements in IFGTr and MTGp, but in different ways. Finally, we found that hand movement meaning modulates interactions between STSp and other posterior temporal and inferior parietal regions for adults, but not for children. These results shed light on the developing neural substrate for understanding meaning contributed by co-speech gesture.
PMCID: PMC3515080  PMID: 22356173
20.  Reading Acquisition Reorganizes the Phonological Awareness Network Only in Alphabetic Writing Systems 
Human brain mapping  2012;34(12):10.1002/hbm.22147.
It is unknown how experience with different types of orthographies influences the neural basis of oral language processing. In order to determine the effects of alphabetic and nonalphabetic writing systems, the current study examined the influence of learning to read on oral language in English and Chinese speakers. Children (8–12 years olds) and adults made rhyming judgments to pairs of spoken words during functional magnetic resonance imaging (fMRI). Developmental increases were seen only for English speakers in the left hemisphere phonological network (superior temporal gyrus (STG), inferior parietal lobule, and inferior frontal gyrus). The increase in the STG was more pronounced for words with conflicting orthography (e.g. pint-mint; jazz-has) even though access to orthography was irrelevant to the task. Moreover, higher reading skill was correlated with greater activation in the STG only for English speaking children. The effects suggest that learning to read reorganizes the phonological awareness network only for alphabetic and not logographic writing systems because of differences in the principles for mapping between orthographic and phonological representations. The reorganization of the auditory cortex may result in better phonological awareness skills in alphabetic readers.
PMCID: PMC3537870  PMID: 22815229
spoken language; rhyming; Chinese; orthography; phonology; development; cross-linguistic; English
21.  Frontostriatal maturation predicts cognitive control failure to appetitive cues in adolescents 
Journal of cognitive neuroscience  2010;23(9):2123-2134.
Adolescent risk-taking is a public health issue that increases the odds of poor lifetime outcomes. One factor thought to influence adolescents' propensity for risk-taking is an enhanced sensitivity to appetitive cues, relative to an immature capacity to exert sufficient cognitive control. We tested this hypothesis by characterizing interactions among ventral striatal, dorsal striatal and prefrontal cortical regions with varying appetitive load using functional magnetic resonance imaging (fMRI) scanning. Child, teen, and adult participants performed a go nogo task with appetitive (happy faces) and neutral cues (calm faces). Impulse control to neutral cues showed linear improvement with age, whereas teens showed a nonlinear reduction in impulse control to appetitive cues. This performance decrement in teens was paralleled by enhanced activity in the ventral striatum. Prefrontal cortical recruitment correlated with overall accuracy and showed a linear response with age for nogo versus go trials. Connectivity analyses identified a ventral frontostriatal circuit including the inferior frontal gyrus and dorsal striatum during nogo versus go trials. Examining recruitment developmentally showed that teens had greater between-subjects ventral-dorsal striatal coactivation relative to children and adults for happy nogo versus go trials. These findings implicate exaggerated ventral striatal representation of appetitive cues in adolescents relative to an intermediary cognitive control response. Connectivity and coactivity data suggest these systems communicate at the level of the dorsal striatum differentially across development. Biased responding in this system is one possible mechanism underlying heightened risk-taking during adolescence.
PMCID: PMC3131482  PMID: 20809855
22.  An fMRI study of sentence-embedded lexical-semantic decision in children and adults 
Brain and language  2010;114(2):90-100.
Lexical-semantic knowledge is a core language component that undergoes prolonged development throughout childhood and is therefore highly amenable to developmental studies. Most previous lexical-semantic functional MRI (fMRI) studies have been limited to single-word or word-pair tasks, outside a sentence context. Our objective was to investigate the development of lexical-semantic language networks in typically developing children using a more ecological sentence-embedded semantic task that permitted performance monitoring while minimizing head movement by avoiding overt speech. Sixteen adults and 23 children completed two fMRI runs of an auditory lexical-semantic decision task with a button-press response, using reverse speech as control condition. Children and adults showed similar activation in bilateral temporal and left inferior frontal regions. Greater activation in adults than in children was seen in left inferior parietal, premotor, and inferior frontal regions, and in bilateral supplementary motor area (SMA). Specifically for semantically incongruous sentences, adults also showed greater activation than children in left inferior frontal cortex, possibly related to enhanced top-down control. Age-dependent activation increases in motor-related regions were shown to be unrelated to overt motor responses, but could be associated with covert speech accompanying semantic decision. Unlike previous studies, age-dependent differences were not detected in posterior sensory cortices (such as extrastriate cortex), nor in middle temporal gyrus.
PMCID: PMC3630793  PMID: 20627366
23.  Imitating expressions: emotion-specific neural substrates in facial mimicry 
Intentionally adopting a discrete emotional facial expression can modulate the subjective feelings corresponding to that emotion; however, the underlying neural mechanism is poorly understood. We therefore used functional brain imaging (functional magnetic resonance imaging) to examine brain activity during intentional mimicry of emotional and non-emotional facial expressions and relate regional responses to the magnitude of expression-induced facial movement. Eighteen healthy subjects were scanned while imitating video clips depicting three emotional (sad, angry, happy), and two ‘ingestive’ (chewing and licking) facial expressions. Simultaneously, facial movement was monitored from displacement of fiducial markers (highly reflective dots) on each subject’s face. Imitating emotional expressions enhanced activity within right inferior prefrontal cortex. This pattern was absent during passive viewing conditions. Moreover, the magnitude of facial movement during emotion-imitation predicted responses within right insula and motor/premotor cortices. Enhanced activity in ventromedial prefrontal cortex and frontal pole was observed during imitation of anger, in ventromedial prefrontal and rostral anterior cingulate during imitation of sadness and in striatal, amygdala and occipitotemporal during imitation of happiness. Our findings suggest a central role for right inferior frontal gyrus in the intentional imitation of emotional expressions. Further, by entering metrics for facial muscular change into analysis of brain imaging data, we highlight shared and discrete neural substrates supporting affective, action and social consequences of somatomotor emotional expression.
PMCID: PMC1820946  PMID: 17356686
emotion; functional magnetic resonance imaging (fMRI); facial expression; imitation
24.  Imitating expressions: emotion-specific neural substrates in facial mimicry 
Intentionally adopting a discrete emotional facial expression can modulate the subjective feelings corresponding to that emotion; however, the underlying neural mechanism is poorly understood. We therefore used functional brain imaging (functional magnetic resonance imaging) to examine brain activity during intentional mimicry of emotional and non-emotional facial expressions and relate regional responses to the magnitude of expression-induced facial movement. Eighteen healthy subjects were scanned while imitating video clips depicting three emotional (sad, angry, happy), and two ‘ingestive’ (chewing and licking) facial expressions. Simultaneously, facial movement was monitored from displacement of fiducial markers (highly reflective dots) on each subject's face. Imitating emotional expressions enhanced activity within right inferior prefrontal cortex. This pattern was absent during passive viewing conditions. Moreover, the magnitude of facial movement during emotion-imitation predicted responses within right insula and motor/premotor cortices. Enhanced activity in ventromedial prefrontal cortex and frontal pole was observed during imitation of anger, in ventromedial prefrontal and rostral anterior cingulate during imitation of sadness and in striatal, amygdala and occipitotemporal during imitation of happiness. Our findings suggest a central role for right inferior frontal gyrus in the intentional imitation of emotional expressions. Further, by entering metrics for facial muscular change into analysis of brain imaging data, we highlight shared and discrete neural substrates supporting affective, action and social consequences of somatomotor emotional expression.
PMCID: PMC1820946  PMID: 17356686
emotion; functional magnetic resonance imaging (fMRI); facial expression; imitation
25.  Language and Brain Volumes in Children with Epilepsy 
Epilepsy & behavior : E&B  2010;17(3):402-407.
This study compared the relationship of language skill with fronto-temporal volumes in 69 medically treated epilepsy subjects and 34 healthy children, aged 6.1-16.6 years. It also determined if the patients with linguistic deficits had abnormal volumes and atypical associations between volumes and language skills in these brain regions. The children underwent language testing and magnetic resonance imaging scans at 1.5 Tesla. Brain tissue was segmented and fronto-temporal volumes were computed. Higher mean language scores were significantly associated with larger inferior frontal gyrus, temporal lobe, and posterior superior temporal gyrus gray matter volumes in the epilepsy group and in the children with epilepsy with average language scores. Increased total brain and dorsolateral prefrontal gray and white matter volumes, however, were associated with higher language scores in the healthy controls. Within the epilepsy group, linguistic deficits were related to smaller anterior superior temporal gyrus gray matter volumes and a negative association between language scores and dorsolateral prefrontal gray matter volumes. These findings demonstrate abnormal development of language related brain regions, and imply differential reorganization of brain regions subserving language in children with epilepsy with normal linguistic skills and in those with impaired language.
PMCID: PMC2892796  PMID: 20149755
Language; epilepsy; development; MRI; frontal lobe; temporal lobe

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