Viviana Betti

Visually Induced Analgesia: Seeing the Body Reduces Pain

Given previous reports of strong interactions between vision and somatic senses, we investigated whether vision of the body modulates pain perception. Participants looked into a mirror aligned with their body midline at either the reflection of their own left hand (creating the illusion that they were looking directly at their own right hand) or the reflection of a neutral object. We induced pain using an infrared laser and recorded nociceptive laser-evoked potentials (LEPs). We also collected subjective ratings of pain intensity and unpleasantness. Vision of the body produced clear analgesic effects on both subjective ratings of pain and the N2/P2 complex of LEPs. Similar results were found during direct vision of the hand, without the mirror. Furthermore, these effects were specific to vision of ones own hand and were absent when viewing another persons hand. These results demonstrate a novel analgesic effect of non-informative vision of the body.

Dynamic reorganization of human resting-state networks during visuospatial attention

Significance The brain is never at rest, and patterns of ongoing correlated activity have been found to resemble patterns during active behavior. A fundamental problem in neuroscience concerns the relationship between spontaneous and task-driven activity. During a demanding task that requires selective attention to sensory stimuli, correlated patterns of spontaneous (rest) activity are generally preserved. However, specific changes in synchronization occur within and between networks that correlate with behavioral performance. These results indicate that attention modifies spontaneous activity patterns in support of task performance. Fundamental problems in neuroscience today are understanding how patterns of ongoing spontaneous activity are modified by task performance and whether/how these intrinsic patterns influence task-evoked activation and behavior. We examined these questions by comparing instantaneous functional connectivity (IFC) and directed functional connectivity (DFC) changes in two networks that are strongly correlated and segregated at rest: the visual (VIS) network and the dorsal attention network (DAN). We measured how IFC and DFC during a visuospatial attention task, which requires dynamic selective rerouting of visual information across hemispheres, changed with respect to rest. During the attention task, the two networks remained relatively segregated, and their general pattern of within-network correlation was maintained. However, attention induced a decrease of correlation in the VIS network and an increase of the DAN→VIS IFC and DFC, especially in a top-down direction. In contrast, within the DAN, IFC was not modified by attention, whereas DFC was enhanced. Importantly, IFC modulations were behaviorally relevant. We conclude that a stable backbone of within-network functional connectivity topography remains in place when transitioning between resting wakefulness and attention selection. However, relative decrease of correlation of ongoing “idling” activity in visual cortex and synchronization between frontoparietal and visual cortex were behaviorally relevant, indicating that modulations of resting activity patterns are important for task performance. Higher order resting connectivity in the DAN was relatively unaffected during attention, potentially indicating a role for simultaneous ongoing activity as a “prior” for attention selection.

Interspecies activity correlations reveal functional correspondence between monkey and human brain areas

Evolution-driven functional changes in the primate brain are typically assessed by aligning monkey and human activation maps using cortical surface expansion models. These models use putative homologous areas as registration landmarks, assuming they are functionally correspondent. For cases in which functional changes have occurred in an area, this assumption prohibits to reveal whether other areas may have assumed lost functions. Here we describe a method to examine functional correspondences across species. Without making spatial assumptions, we assessed similarities in sensory-driven functional magnetic resonance imaging responses between monkey (Macaca mulatta) and human brain areas by temporal correlation. Using natural vision data, we revealed regions for which functional processing has shifted to topologically divergent locations during evolution. We conclude that substantial evolution-driven functional reorganizations have occurred, not always consistent with cortical expansion processes. This framework for evaluating changes in functional architecture is crucial to building more accurate evolutionary models.

Hypnotic modulation of pain perception and of brain activity triggered by nociceptive laser stimuli.

INTRODUCTION Neuroimaging studies indicate that hypnotic suggestions of increased and decreased pain intensity and unpleasantness may modulate somatosensory and cingulate cortex activity, respectively. METHODS Using a within subject design and a strict subject selection procedure, we tested in High (Highs) and Low (Lows) hypnotically suggestible individuals whether hypnotic suggestions of sensory and affective hypoalgesia or hyperalgesia differentially affected subjective ratings of laser-induced pain and nociceptive-related brain activity in the time- and time-frequency domain. RESULTS Hypnotic modulation of pain intensity and unpleasantness affected subjective ratings of laser-induced pain only in Highs. Such modulation was more specific for unpleasantness manipulation and more evident for suggestions of hyperalgesia. Importantly, Highs and Lows showed increase and decrease of P2a and P2b wave amplitudes and gamma band power, respectively. CONCLUSIONS Hypnotic suggestions exerted a top-down modulatory effect on both evoked and induced-cortical brain responses triggered by selective nociceptive laser inputs. Furthermore, correlation analyses indicated that gamma power modulation and suggestions of hyperalgesia may reflect the process of allocating control resources to salient and threatening sensory-affective dimensions of pain.

Parallel spinal pathways generate the middle-latency N1 and the late P2 components of the laser evoked potentials

OBJECTIVE To investigate the possible presence of multiple spino-thalamic pathways with different conduction velocities (CVs) in the human spinal cord. METHODS Laser evoked potentials (LEPs) were recorded in 10 healthy subjects after stimulation of the dorsal midline at four vertebral level: C5, T2, T6, and T10. This method allowed us to minimize the influence of the conduction in the peripheral fibers and to calculate the spinal CV in two different ways: (1) the reciprocal of the slope of the regression line was obtained from the latencies of the different LEP components, and (2) the distance between C5 and T10 was divided by the latency difference of the responses at the two sites. In particular, we considered the middle-latency N1 potential (latencies of around 135, 150, 157, and 171 ms after stimulation at C5, T2, T6, and T10 levels, respectively), which is generated in the second somatosensory (SII) area, and the late P2 response (latencies of around 336, 344, 346, and 362 ms after stimulation at C5, T2, T6, and T10 levels, respectively), which is generated in the anterior cingulate cortex (ACC). RESULTS The calculated CV of the spinal fibers generating the N1 potential (around 9 m/s) was significantly different (P<0.05) from the one of the pathway producing the P2 response (around 13 m/s). CONCLUSIONS Our results suggest that the N1 and the P2 LEP components are generated by two parallel spinal pathways. SIGNIFICANCE Both the N1 and P2 potentials should be recorded in the clinical routine since a dissociated abnormality of either response may be found in lesions of the nociceptive system not only in the brain, but also at spinal cord level.

Dynamic construction of the neural networks underpinning empathy for pain.

When people witness or imagine the pain of another person, their nervous system may react as if they were feeling that pain themselves. Early neuroscientific evidence indicates that the firsthand and vicarious experiences of pain share largely overlapping neural structures, which typically correspond to the lateral and medial brain regions that encode the sensory and the affective qualities of pain. Such neural circuitry is highly malleable and allows people to flexibly adjust the empathic behavior depending on social and personal factors. Recent views posit, however, that the brain can be conceptualized as a complex system, in which behavior emerges from the interaction between functionally connected brain regions, organized into large-scale networks. Beyond the classical modular view of the brain, here we suggest that empathic behavior may be understood through a dynamic network-based approach where the cortical circuits associated with the experience of pain flexibly change in order to code self- and other-related emotions and to intrinsically map our mentality to empathetically react to others.

Effective connectivity inferred from fMRI transition dynamics during movie viewing points to a balanced reconfiguration of cortical interactions

ABSTRACT Our behavior entails a flexible and context‐sensitive interplay between brain areas to integrate information according to goal‐directed requirements. However, the neural mechanisms governing the entrainment of functionally specialized brain areas remain poorly understood. In particular, the question arises whether observed changes in the regional activity for different cognitive conditions are explained by modifications of the inputs to the brain or its connectivity? We observe that transitions of fMRI activity between areas convey information about the tasks performed by 19 subjects, watching a movie versus a black screen (rest). We use a model‐based framework that explains this spatiotemporal functional connectivity pattern by the local variability for 66 cortical regions and the network effective connectivity between them. We find that, among the estimated model parameters, movie viewing affects to a larger extent the local activity, which we interpret as extrinsic changes related to the increased stimulus load. However, detailed changes in the effective connectivity preserve a balance in the propagating activity and select specific pathways such that high‐level brain regions integrate visual and auditory information, in particular boosting the communication between the two brain hemispheres. These findings speak to a dynamic coordination underlying the functional integration in the brain.

Distinct modes of functional connectivity induced by movie-watching

&NA; A fundamental question in systems neuroscience is how endogenous neuronal activity self‐organizes during particular brain states. Recent neuroimaging studies have demonstrated systematic relationships between resting‐state and task‐induced functional connectivity (FC). In particular, continuous task studies, such as movie watching, speak to alterations in coupling among cortical regions and enhanced fluctuations in FC compared to the resting‐state. This suggests that FC may reflect systematic and large‐scale reorganization of functionally integrated responses while subjects are watching movies. In this study, we characterized fluctuations in FC during resting‐state and movie‐watching conditions. We found that the FC patterns induced systematically by movie‐watching can be explained with a single principal component. These condition‐specific FC fluctuations overlapped with inter‐subject synchronization patterns in occipital and temporal brain regions. However, unlike inter‐subject synchronization, condition‐specific FC patterns were characterized by increased correlations within frontal brain regions and reduced correlations between frontal‐parietal brain regions. We investigated these condition‐specific functional variations as a shorter time scale, using time‐resolved FC. The time‐resolved FC showed condition‐specificity over time; notably when subjects watched both the same and different movies. To explain self‐organisation of global FC through the alterations in local dynamics, we used a large‐scale computational model. We found that condition‐specific reorganization of FC could be explained by local changes that engendered changes in FC among higher‐order association regions, mainly in frontal and parietal cortices. HighlightsThe variations of functional connectivity during movie‐watching condition are explained by a single principal component.The topography of condition‐specific principal component is similar to inter‐subject synchronization in occipital and temporal brain regions, but it exhibits distinct patterns expressed in frontal brain regions.Time‐resolved functional connectivity shows that the condition‐specific functional states are continuous across time.A whole‐brain computational model shows that the changes in local dynamical properties in higher‐order association regions can explain the condition‐specific changes in FC.

Distinct Functional Connectivity Mode during Viewing Natural Scenes Revealed by Principal Component Analysis

A fundamental question in systems neuroscience is how endogenous neuronal activity self-organizes during particular brain states. Recent neuroimaging studies have revealed systematic relationships between resting-state and task-induced functional connectivity (FC). In particular, continuous task studies, such as movie watching, speak to alterations in coupling among cortical regions and enhanced fluctuations in FC compared to resting-state. This suggests that FC may reflect systematic and large-scale reorganization of functionally integrated responses while subjects are watching movies. In this study, we characterized fluctuations in FC during resting-state and movie-watching conditions. We found that the FC patterns induced systematically by movie-watching can be explained with a single principal component. These condition-specific FC fluctuations overlapped with inter-subject synchronization patterns in occipital and temporal brain regions. However, unlike inter-subject synchronization, condition-specific FC patterns contained increased correlations within frontal brain regions and reduced correlations between frontal-parietal brain regions. We investigated the condition-specific functional variations as a shorter time scale, using time-resolved FC. The time-resolved FC showed condition-specificity over time, notably when subjects were also watching the same and different movie scenes. To explain the self-organisation of whole-brain FC through the alterations in local dynamics, we used a large-scale computational model. We found that the condition-specific reorganization of FC could be explained by local changes that engendered changes in FC among higher-order association regions, mainly in frontal parietal cortices.A fundamental question in systems neuroscience is how spontaneous activity at rest is reorganized during task performance. Recent studies suggest a strong relationship between resting and task FC. Furthermore, the relationship between resting and task FC has been shown to reflect individual differences. Particularly, various studies have demonstrated that the FC has higher reliability and provides enhanced detection of individual differences while viewing natural scenes. Although the large-scale organization of FC during rest and movie-viewing conditions have been well studied in relation to individual variations, the re-organization of FC during viewing natural scenes have not been studied in depth. In this study, we used principal component analysis on FC during rest and movie-viewing condition to characterize the dimensionality of FC patterns across conditions and subjects. We found that the variations in FC patterns related to viewing natural scenes can be explained by a single component, which enables identification of the task over subjects with 100% accuracy. We showed that the FC mode associated to viewing natural scenes better reflects individual variations. Furthermore, we investigated the signatures of movie-viewing-specific functional modes in dynamic FC based on phase-locking values between brain regions. We found that the movie-specific functional mode is persistent across time; suggesting the emergence of a stable processing mode. To explain the reorganization of whole-brain FC through the changes in local dynamics, we appeal to a large-scale computational model. This modelling suggested that the reorganization of whole-brain FC is associated to the interaction between frontal-parietal and frontal-temporal activation patterns.

TOPOLOGY OF FUNCTIONAL CONNECTIVITY AND HUB DYNAMICS IN THE BETA BAND AS TEMPORAL PRIOR FOR NATURAL VISION IN THE HUMAN BRAIN

Networks hubs represent points of convergence for the integration of information across many different nodes and systems. Although a great deal is known on the topology of hub regions in the human brain, little is known about their temporal dynamics. Here, we examine the static and dynamic centrality of hub regions when measured in the absence of a task (rest) or during the observation of natural or synthetic visual stimuli. We used Magnetoencephalography (MEG) in humans (both sexes) to measure static and transient regional and network-level interaction in α- and β-band limited power (BLP) in three conditions: visual fixation (rest), viewing of movie clips (natural vision), and time-scrambled versions of the same clips (scrambled vision). Compared with rest, we observed in both movie conditions a robust decrement of α-BLP connectivity. Moreover, both movie conditions caused a significant reorganization of connections in the α band, especially between networks. In contrast, β-BLP connectivity was remarkably similar between rest and natural vision. Not only the topology did not change, but the joint dynamics of hubs in a core network during natural vision was predicted by similar fluctuations in the resting state. We interpret these findings by suggesting that slow-varying fluctuations of integration occurring in higher-order regions in the β band may be a mechanism to anticipate and predict slow-varying temporal patterns of the visual environment. SIGNIFICANCE STATEMENT A fundamental question in neuroscience concerns the function of spontaneous brain connectivity. Here, we tested the hypothesis that topology of intrinsic brain connectivity and its dynamics might predict those observed during natural vision. Using MEG, we tracked the static and time-varying brain functional connectivity when observers were either fixating or watching different movie clips. The spatial distribution of connections and the dynamics of centrality of a set of regions were similar during rest and movie in the β band, but not in the α band. These results support the hypothesis that the intrinsic β-rhythm integration occurs with a similar temporal structure during natural vision, possibly providing advanced information about incoming stimuli.