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Toni, I.

Publications and source records attributed to Toni, I..

9 recordsLinked to original sources

Between-movie variability severely limits generalizability of "naturalistic" neuroimaging

Movie-watching fMRI has become increasingly popular in neuroscience. Movie-fMRI data are commonly analyzed using inter-subject correlation (ISC), which quantifies the similarity of neural time series across individuals. Differences in ISC during movie viewing have been associated with psychological traits and clinical diagnoses. However, most studies investigating group differences in ISC or ISC-behavior associations have drawn conclusions from a single movie. Because ISC is inherently stimulus-driven, effects observed for one movie may not generalize to another. Yet, the extent to which ISC patterns and ISC-behavior associations depend on the specific movie being viewed has received limited systematic attention. Here, we analyzed three independent datasets comprising 318 subjects and 36 movies in total to quantify between-movie variability in ISC and assess its consequences for ISC-behavior associations. Across datasets, ISC varied between movies throughout the cortex. This variability was spatially heterogeneous: regions with stronger ISC showed greater between-movie variability. Movie-specific inter-subject representational similarity analysis revealed distinct spatial distributions of ISC-behavior associations, with limited overlap between movies. This pattern was observed for two distinct behavioral constructs. These findings suggest that ISC-behavior associations can be strongly movie-specific.

neuroscience↗

Improving approach-avoidance control in social anxiety by targeting phase-amplitude coupling between prefrontal and sensorimotor cortex

Social avoidance is a hallmark of social anxiety disorder. Difficulties in controlling avoidance behavior are the core maintaining factor of this impairing condition, hampering the efficacy of existing therapies. This preregistered study tested a physiologically-grounded non-invasive enhancement of control over social approach and avoidance behavior in socially anxious individuals. Their prefrontal and sensorimotor areas received dual-site phase-coupled electrical stimulation, to enhance endogenous inter-regional theta-gamma phase-amplitude coupling, a mechanism known to support emotion control in non-anxious individuals. We measured behavioral and fMRI-BOLD responses during in-phase, anti-phase, and sham stimulations, while participants performed a social approach-avoidance task, involving either automatic or controlled emotional actions. In-phase stimulation selectively enhanced control over approach-avoidance actions, and modulated neural responses in the same prefrontal region where stimulation-reactivity increased as a function of trait anxiety. These findings illustrate how human neurophysiological connectivity can be leveraged to improve control over social avoidance, opening the way for mechanistically grounded clinical interventions of persistent avoidance in anxiety disorders. SIGNIFICANCE STATEMENTControlling automatic approach-avoid behavior is essential for human social interactions. This ability is impaired in social anxiety, but we know how neurotypical brains use endogenous rhythmic coupling for social emotion control. In a preregistered study, we used noninvasive electrical brain stimulation to enhance endogenous rhythmic coupling between prefrontal theta- and sensorimotor gamma-band rhythms, while highly socially anxious individuals solved an emotional control challenge. In-phase stimulation selectively enhanced emotional action control and modulated neural activity in a prefrontal cortex region where brain stimulation reactivity increased as a function of trait anxiety. These findings provide evidence for the generalizability and clinical potential of this interventional approach to social anxiety.

neuroscience↗

Developmental shift in testosterone influence on prefrontal emotion control

A paradox of testosterone effects is seen in adolescents vs. adults in social emotional approach-avoidance behavior. During adolescence, high testosterone levels are associated with increased anterior prefrontal (aPFC) involvement in emotion control, whereas during adulthood this neuro-endocrine relation is reversed. Rodent work shows that, during puberty, testosterone transitions from a neuro-developmental to a social-sexual activating hormone. In this study, we explored whether this functional transition is also present in human adolescents and young adults. Using a prospective longitudinal design, we investigated the role of testosterone on neural control of social emotional behavior during the transitions from middle to late adolescence and into young adulthood. Seventy-one individuals (tested at ages 14, 17, and 20 years) performed an fMRI-adapted approach-avoidance (AA) task involving automatic and controlled actions in response to social emotional stimuli. In line with predictions from animal models, the effect of testosterone on aPFC engagement decreased between middle and late adolescence, and shifted into an activational role by young adulthood - impeding neural control of emotions. This change in testosterone function was accompanied by increased testosterone-modulated amygdala reactivity. These findings qualify the testosterone-dependent maturation of the prefrontal-amygdala circuit supporting emotion control during the transition from middle adolescence into young adulthood.

neuroscience↗

Social framing effects in decision making

Human decisions are known to be strongly influenced by the manner in which options are presented, the "framing effect". Here, we ask whether decision-makers are also influenced by how advice from other knowledgeable agents are framed, a "social framing effect". For example, do students learn better from a teacher who often frames advice by emphasizing appetitive outcomes, or do they learn better from another teacher who usually emphasizes avoiding options that can be harmful to their progress? We study the computational and neural mechanisms by which framing of advice affect decision-making, social learning, and trust. We found that human participants are more likely to trust and follow an adviser who often uses an appetitive frame for advice compared with another one who often uses an aversive frame. This social framing effect is implemented through a modulation of the integrative abilities of the ventromedial prefrontal cortex. At the time of choice, this region combines information learned via personal experiences of reward with social information, but the combination differs depending on the social framing of advice. Personally-acquired information is weighted more strongly when dealing with an adviser who uses an aversive frame. The findings suggest that social advice is systematically incorporated into our decisions, while being affected by biases similar to those influencing individual value-based learning.

neuroscience↗

Improving emotional-action control by targeting long-range phase-amplitude neuronal coupling.

Control over emotional action tendencies is essential for every-day interactions. This cognitive function can fail during socially challenging situations, and is chronically attenuated in social psychopathologies such as social anxiety and aggression. Previous studies have shown that control over social-emotional action tendencies depends on phase-amplitude coupling between prefrontal theta-band (6 Hz) rhythmic activity and broadband gamma-band activity in sensorimotor areas. Here, we delivered dual-site phase-coupled brain stimulation to facilitate theta-gamma phase-amplitude coupling between frontal regions known to implement that form of control, while participants were challenged to control their automatic action tendencies in a social-emotional approach/avoidance-task. Participants had increased control over their emotional action tendencies, depending on the relative phase and dose of the intervention. Concurrently measured fMRI effects of task and stimulation, and estimated changes in effective connectivity, indicated that the intervention improved control by increasing the efficacy of anterior prefrontal inhibition over sensorimotor cortex. This enhancement of emotional action control provides causal evidence for a phase-amplitude coupling mechanism guiding action selection during emotional-action control. More generally, the finding illustrates the potential of physiologically-grounded interventions aimed at reducing neural noise in cerebral circuits where communication relies on phase-amplitude coupling.

neuroscience↗

Electrocorticographic dissociation of alpha and beta rhythmic activity in the human sensorimotor system

This study uses electrocorticography in humans to assess how alpha- and beta-band rhythms modulate excitability of the sensorimotor cortex during movement selection, as indexed through a psychophysically-controlled movement imagery task. Both rhythms displayed effector-specific modulations, tracked spectral markers of action potentials in the local neuronal population, and showed spatially systematic phase relationships (traveling waves). Yet, alpha- and beta-band rhythms differed in their anatomical and functional properties, were weakly correlated, and traveled along opposite directions across the sensorimotor cortex. Increased alpha-band power in the somatosensory cortex ipsilateral to the selected arm was associated with spatially-unspecific inhibition. Decreased beta-band power over contralateral motor cortex was associated with a focal shift from relative inhibition to excitation. These observations indicate the relevance of both inhibition and disinhibition mechanisms for precise spatiotemporal coordination of neuronal populations during movement selection. Those mechanisms are implemented through the substantially different neurophysiological properties of sensorimotor alpha- and beta-band rhythms.

neuroscience↗

Human lateral Frontal Pole contributes to control over social-emotional behaviour

Regulation of emotional behavior is essential for human social interactions. Recent work has exposed its cognitive complexity, as well as its unexpected reliance on portions of the anterior prefrontal cortex (aPFC) also involved in exploration, relational reasoning, and counterfactual choice, rather than on dorsolateral and medial prefrontal areas involved in several forms of cognitive control. This study anatomically qualifies the contribution of aPFC territories to the regulation of social-emotional actions, and explores a possible structural pathway through which emotional regulation might be implemented. We provide converging evidence from task-based fMRI, diffusion-weighted imaging, and functional connectivity fingerprints for a novel neural element in emotional regulation. Task-based fMRI in human male participants (N = 40) performing a social-emotional approach-avoidance task identified aPFC territories involved in the regulation of social-emotional actions. Connectivity fingerprints, based on diffusion-weighted imaging and resting-state connectivity, localized those task-defined frontal regions to the lateral frontal pole (FPl), an anatomically-defined portion of the aPFC that lacks a homologous counterpart in macaque brains. Probabilistic tractography indicated that 10-20% of inter-individual variation in social-emotional regulation abilities is accounted for by the strength of structural connectivity between FPl and amygdala. Evidence from an independent replication sample (N = 50; 10 females) further substantiated this result. These findings provide novel neuroanatomical evidence for incorporating FPl in models of control over human social-emotional behavior. Significance statementSuccessful regulation of emotional behaviors is a prerequisite for successful participation in human society, as is evidenced by the social isolation and loss of occupational opportunities often encountered by people suffering from emotion-regulation disorders such as social-anxiety disorder and psychopathy. Knowledge about the precise cortical regions and connections supporting this control is crucial for understanding both the nature of computations needed to successfully traverse the space of possible actions in social situations, and the potential interventions that might result in efficient treatment of social-emotional disorders. This study provides evidence for a precise cortical region (FPl) and a structural pathway (the ventral amygdalofugal bundle) through which a cognitively complex form of emotional action regulation might be implemented in the human brain.

neuroscience↗

The effects of a TMS double lesion to a cortical network

Transcranial magnetic stimulation (TMS) has contributed to our understanding of the functions of individual brain regions, but its use to examine distributed functions throughout a network has been more limited. We assess the functional consequences of a TMS pulse to the oculomotor network which was first perturbed by continuous theta-burst stimulation (cTBS), to examine the potential for additive effects from lesions to two network nodes. Twenty-three humans performed pro-(look towards) and anti-(look away) saccades after receiving cTBS to right frontal eye fields (FEF), dorsolateral prefrontal cortex (DLPFC) or somatosensory cortex (S1) (control). On a subset of trials, a TMS pulse was applied to right posterior parietal cortex (PPC). We assessed changes in saccade amplitudes, performance (percentage correct) and reaction times, as these parameters relate to computations in networks involving these nodes. We observed impairments in ipsilateral anti-saccade amplitudes following DLPFC cTBS that were enhanced by a PPC pulse, but that were not enhanced relative to the effect of the PPC pulse alone. There was no evidence for effects from the double lesion to performance or reaction times. This suggests that computations are distributed across the network, such that even a single lesion is consequential.

neuroscience↗

The context-dependent nature of the neural implementation of intentions

Many studies have identified networks in parietal and prefrontal cortex that are involved in intentional action. Yet, knowledge about what these networks exactly encoded is still scarce. In this study we look into the content of those processes. We ask whether the neural representations of intentions are context- and reason-invariant, or whether these processes depend on the context we are in, and the reasons we have for choosing an action. We use a combination of functional magnetic resonance imaging and multivariate decoding to directly assess the context- and reason-dependency of the processes underlying intentional action. We were able to decode action decisions in the same context and for the same reasons from the fMRI data, in line with previous decoding studies. Furthermore, we could decode action decisions across different reasons for choosing an action. Importantly, though, decoding decisions across different contexts was at chance level. These results suggest that for voluntary action, there is considerable context-dependency in intention representations. This suggests that established invariance in neural processes may not reflect an essential feature of a certain process, but that this stable character could be dependent on invariance in the experimental setup, in line with predictions from situated cognition theory.

neuroscience↗