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Tallon-Baudry, C.

Publications and source records attributed to Tallon-Baudry, C..

9 recordsLinked to original sources

Perceptual reaction times are coupled to the gastric electrical rhythm

Withdrawal statementThe authors have withdrawn this manuscript following the identification of a methodological bias that affects the validity of the results. In particular, a bias in the statistical approach for the group-level control analysis led to an underestimation of the false positive rate. The studys conclusions are no longer valid. Therefore, the authors do not wish this work to be cited as reference. If you have any questions, please contact the corresponding author.

neuroscience↗

Interoception vs. Exteroception: Cardiac interoception competes with tactile perception, yet also facilitates self-relevance encoding

Internal bodily signals, notably the heartbeat, influence our perception of the external world - but the nature of this influence remains unclear. Different frameworks, originating in opposing views of the function of interoception, have developed largely in parallel. One line of evidence (Internal/External Competition) indicates that interoceptive and exteroceptive inputs compete for neural resources. Another line (Self-related Facilitation) shows a link between interoceptive and self-related processing, which might include computing the self-relevance of exteroceptive inputs. We contrasted these accounts within a single experimental task for which they yielded distinct predictions. We measured heartbeat-evoked potentials (HEPs, a measure of cardiac interoception) with EEG, and manipulated the self-relevance of an audio-tactile stimulus by placing the audio source either inside or outside the peripersonal space immediately around the body. On one hand, pre-stimulus HEP amplitudes over somatosensory cortex were linked to slower reaction times, and affected audio-tactile stimulus-evoked responses in the same area, indicating competition for shared neural resources. On the other hand, pre-stimulus HEPs over integrative sensorimotor and default-mode network regions facilitated stimulus self-relevance encoding, both in reaction times and audio-tactile evoked responses. Importantly, Competition and Facilitation effects were spatially and statistically independent from each other. We therefore reconcile the two views by showing the co-existence of two independent mechanisms: one that allocates neural resources to either internal bodily signals or the external world, and another by which interoception and exteroception are combined to determine the self-relevance of external signals. Our results highlight the multi-dimensionality of HEPs, and of internal states more generally. Significance StatementDo internal bodily signals distract us from the external world (Internal/External Competition account)? Or do internal signals contribute to conscious perception, by situating the perceived external world relative to the organism (Self-related Facilitation account)? So far, both accounts - reflecting fundamentally different views of brain-body interactions - received experimental support, but have never been compared directly. We measured neural responses to heartbeats, and tested how they influenced perception in an audio-tactile reaction time task where self-relevance was manipulated. We found evidence for both accounts, reflecting independent mechanisms in distinct brain regions. Our results reconcile two hitherto independent and seemingly contradictory research programmes on the relationship between interoception and exteroception. They further highlight the multi-dimensionality of cardiac-brain interactions, and hence of internal state.

neuroscience↗

The cardiac, respiratory and gastric rhythms independently modulate corticospinal excitability

Interoception refers to the brains sensing of internal body state and encompasses various bodily systems, notably the cardiac, respiratory and gastric rhythms. Beyond their roles in physiological regulation and emotional states, each of these visceral rhythms has been shown to influence brain activity and cognition, prompting for the development of various interpretative functional frameworks. However, both experimental data and functional hypothesis leave it unclear whether and how each visceral rhythm acts simultaneously and independently on brain activity. Here we address this question by measuring in human participants how the corticospinal excitability of the motor system varies with the phase of each of the three visceral rhythms. We applied single pulse Transcranial Magnetic Stimulation (TMS) over the hand region in primary motor cortex to elicit Motor Evoked Potentials (MEP), whose amplitude reflects corticospinal excitability, and tested whether MEP amplitude depends on the phase of the simultaneously measured cardiac, respiratory and gastric rhythms. All three visceral rhythms were coupled to motor excitability with similar effect sizes at the group level. However, we found no relation between coupling strengths: participants displaying high coupling with one organ did not necessarily display high coupling to the other organs. These results indicate that independent mechanisms could underly the coupling between the cardiac, respiratory and gastric rhythm and motor excitability. We further introduce the concept of individual interoceptive profiles, and show that such interoceptive profiles obtained from objective coupling strength measures were not explained by self-reported awareness of the organ. Altogether our results call for refined specifications of the frameworks offering a functional or clinical interpretation of viscera-brain coupling taking into account both independent mechanisms and individual interoceptive profiles.

neuroscience↗

Different varieties of arousal converge on a shared cortical network

The term arousal is very often used, but classical textbooks from different domains of neuroscience and psychology offer surprisingly different views on what arousal is. The huge number of scientific articles with the term arousal ([~]50.000) highlights the importance of the concept but also explains why such a vast literature has never been systematically reviewed so far. Here, we leverage the tools of natural language processing to probe the nature of arousal in a data-driven, comprehensive manner. We show that arousal comes in seven varieties: cognitive, emotional, physiological, sexual, related to stress disorders, to sleep, or to sleep disorders. We then ask whether domain-general arousal exists, and run meta-analyses of the brain imaging literature to reveal that all varieties of arousal, except arousal in sleep disorders for lack of data, converge onto a cortical arousal network composed of the pre-supplementary motor area and the left and right dorsal anterior insula. More precisely, we find that activity in dysgranular insular area 7, the region with the highest convergence across varieties of arousal is also specific to arousal. Our results show that arousal corresponds to a construct at least partially shared across different domains of neuroscience and identify the domain-general cortical arousal network. Novel taxonomies of arousal reconciling seemingly opposing views on what arousal is should thus include domain-general arousal as a central component. Significance statementThe term arousal has been used in almost 50.000 scientific papers, but it is only loosely defined. The few attempts at defining arousal in neuroscience and psychology resulted in divergent views: arousal as a multi-dimensional construct or arousal as a global state. Is arousal an abstraction of the scientists mind reflecting a myriad of distinct processes, or is there some common neuronal feature? We used large-scale semi-automatic text mining methods and neuroimaging meta-analyses to review this vast and heterogeneous literature. Our results reveal the existence of domain-general arousal, a process shared by situations as different as a cognitive task, an emotional context, and the transition to wakefulness or sexual behavior. Domain-general arousal reconciles the concepts of general and multi-dimensional arousal.

neuroscience↗

The sensory and motor components of the cortical hierarchy are coupled to the rhythm of the stomach during rest

Bodily rhythms appear as novel scaffolding mechanisms orchestrating the spatio-temporal organization of spontaneous brain activity. Here, we follow up on the discovery of the gastric resting-state network (Rebollo et al, 2018), composed of brain regions in which the fMRI signal is phase-synchronized to the slow (0.05 Hz) electrical rhythm of the stomach. Using a larger sample size (n=63 human participants), we further characterize the anatomy and effect sizes of gastric-brain coupling across resting-state networks, a fine grained cortical parcellation, as well as along the main gradients of cortical organization. Most (67%) of the gastric network is included in the somato-motor-auditory (38%) and visual (29%) resting state networks. Gastric brain coupling also occurs in the granular insula and, to a lesser extent, in the piriform cortex. Thus, all sensory and motor cortices corresponding to both exteroceptive and interoceptive modalities are coupled to the gastric rhythm during rest. Conversely, little gastric-brain coupling occurs in cognitive networks and transmodal regions. These results suggest not only that gastric rhythm and sensory-motor processes are likely to interact, but also that gastric-brain coupling might be a mechanism of sensory and motor integration that mostly bypasses cognition, complementing the classical hierarchical organization of the human brain. Significance statementWhile there is growing interest for brain-body communication in general and brain-viscera communication in particular, little is known about how the brain interacts with the gastric rhythm, the slow electrical rhythm continuously produced in the stomach. Here, we show in human participants at rest that the gastric network, composed of brain regions synchronized with delays to the gastric rhythm, includes all motor and sensory (vision, audition, touch and interoception, olfaction) regions, but only few of the transmodal regions associated with higher-level cognition. Such results prompt for a reconsideration of the classical view of cortical organization, where the different sensory modalities are considered as relatively independent modules.

neuroscience↗

Distinct neural variables underlie subjective reports of attention

Attention is subjectively experienced as a unified cognitive effort. This unitary experience of attention contrasts with the diversity of neural and peripheral correlates of attention. While the effects of attention on stimulus-evoked responses, alpha oscillations and pupil diameter, are well-known the relationship between these indices and the subjective experience of attention, has not yet been assessed. Participants performed a sustained (10 s to 30 s) attention task in which rare (10%) targets were detected within continuous tactile stimulation (16 Hz). Trials were followed by attention ratings on an 8-point Likert scale. Steady-state evoked fields (SSEFs) in response to tactile stimulation, as measured by magnetoencephalography, provided an objective measure of sensory processing. Beamformer source analysis of somatosensory alpha power was used as a measure of cortical excitability, while pupillometry provided a peripheral index of arousal. Attention ratings correlated negatively with contralateral somatosensory alpha power, and positively with pupil diameter. The effect of pupil diameter on attention ratings extended into the following trial, reflecting a sustained aspect of attention related to vigilance. The effect of alpha power did not carry over to the next trial, and furthermore mediated the effect of pupil diameter on attention ratings. Variation in SSEF power reflected stimulus processing under the influence of alpha oscillations, but were not readily expressed through subjective ratings of attention. Together, our results show that both alpha power and pupil diameter are reflected in the subjective experience of attention, albeit on different time spans, while continuous stimulus processing might not be metacognitively accessible. 1 Significance StatementAttention is subjectively experienced as a unified cognitive effort, in contrast with a diversity of neural and peripheral measures shown to correlate with attention. We present the first comprehensive study on the complex inter-relationship between the most common bio-physiological indices of attention, and their association with the subjective experience of attention. We show that the subjective experience of attention correlates negatively with cortical alpha oscillations, and positively with pupil diameter. The latter reflected a sustained aspect of attention, spanning several tens of seconds, related to vigilance. Alpha power, representing cortical control, fluctuated faster and mediated the effect of pupil diameter on attention. Tactile steady-state power reflected stimulus processing, also under the influence of alpha oscillations, but did not contribute much to subjective ratings of attention.

neuroscience↗

Fluctuations in the homeostatic neural circuitry influence consistency in choices between cultural goods

Forrest Gump or Matrix? Preference-based decisions are subjective and entail self-reflection. However, these self-related features are unaccounted for by known neural mechanisms of valuation and choice. Self-related processes have been linked to a basic interoceptive biological mechanism, the neural monitoring of heartbeats, in particular in ventromedial prefrontal cortex (vmPFC), a region also involved in value encoding. We thus hypothesized a functional coupling between the neural monitoring of heartbeats and the precision of value encoding in vmPFC. Human participants were presented with pairs of movie titles. They indicated either which movie they preferred, or performed a control objective visual discrimination that did not require self-reflection. Using magnetoencephalography, we measured heartbeat-evoked responses (HERs) before option presentation, and confirmed that HERs in vmPFC were larger when preparing to the subjective, self-related task. We retrieved the expected cortical value network during choice with time-resolved statistical modeling. Crucially, we show that larger HERs before option presentation are followed by stronger value encoding during choice in vmPFC. This effect is independent of the overall vmPFC baseline activity. The neural interaction between HERs and value encoding predicted preference-based choice consistency over time, accounting for both inter-individual differences and trial-to-trial fluctuations within individuals. Neither cardiac activity nor arousal fluctuations could account for any of the effects. HERs did not interact with the encoding of perceptual evidence in the discrimination task. Our results show that the self-reflection underlying preference-based decisions involves the integration of HERs to subjective value encoding in vmPFC, and that this integration contributes to preference stability. Significance statementDeciding whether you prefer Forrest Gump or Matrix is based on subjective values, which only you, the decision-maker, can estimate and compare, by asking yourself. Yet, how self-reflection is biologically implemented and its contribution to subjective valuation are not known. We show that in ventromedial prefrontal cortex, the neural response to heartbeats, an interoceptive self-related process, influences the cortical representation of subjective value. The neural interaction between the cortical monitoring of heartbeats and value encoding predicts choice consistency, i.e. whether you consistently prefer Forrest Gump over Matrix over time. Our results pave the way for the quantification of self-related process in decision making and may shed new light on the relationship between maladaptive decisions and impaired interoception.

neuroscience↗

Neural responses to heartbeats as a mechanism for distinguishing self from other during imagination

Imagination is an internally-generated process, where one can make oneself or other people appear as protagonists of a scene. How does the brain tag the protagonist of an imagined scene, as being oneself or someone else? Crucially, neither external stimuli nor motor feedback are available during imagination to disentangle imagining oneself from imagining someone else. Here, we test the hypothesis that an internal mechanism based on the neural monitoring of heartbeats could distinguish between self and other. 23 participants imagined themselves (from a first-person perspective) or a friend (from a third-person perspective) in various scenarios, while their brain activity was recorded with magnetoencephalography and their cardiac activity was simultaneously monitored. We measured heartbeat-evoked responses, i.e. transients of neural activity occurring in response to each heartbeat, during imagination. The amplitude of heartbeat-evoked responses differed between imagining oneself and imagining a friend, in the precuneus, mid and posterior cingulate regions bilaterally. Effect size was modulated by the general daydreaming frequency of participants but not by their interoceptive abilities. These results could not be accounted for by other characteristics of imagination (e.g., the ability to adopt the perspective, valence or arousal), nor by cardiac parameters (e.g., heart rate) or arousal levels. Heartbeat-evoked responses thus appear as a neural marker distinguishing self from other during imagination.\n\nHighlights- Heartbeat-evoked responses differentiate self from other during imagination.\n\n- These effects were located in the precuneus and mid- to posterior cingulate.\n\n- The neural monitoring of the body could be a mechanism for self/other distinction.

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Stomach-brain synchrony binds neural representations of the body in a novel, delayed-connectivity resting-state network

Resting-state networks offer a unique window into the brains functional architecture, but their characterization remains limited to instantaneous connectivity thus far. Here, we describe a novel resting-state network based on the delayed connectivity between the brain and the slow electrical rhythm (0.05 Hz) generated in the stomach. The gastric network cuts across classical resting-state networks with little overlap with autonomic regulation areas. This network is composed of regions with convergent functional properties involved in mapping bodily space through touch, action or vision, as well as mapping external space in bodily coordinates. The network is characterized by a precise temporal sequence of activations within a gastric cycle, beginning with somato-motor cortices and ending with the extrastriate body area and dorsal precuneus. Our results demonstrate that canonical resting-state networks based on instantaneous connectivity represent only one of the possible partitions of the brain into coherent networks based on temporal dynamics.

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