ABSTRACT
Visceral signals are constantly processed by our central nervous system, enable homeostatic regulation, and influence perception, emotion, and cognition. While visceral processes at the cortical level have been extensively studied using non-invasive imaging techniques, very few studies have investigated how this information is processed at the single neuron level, both in humans and animals. Subcortical regions, relaying signals from peripheral interoceptors to cortical structures, are particularly understudied and how visceral information is processed in thalamic and subthalamic structures remains largely unknown. Here, we took advantage of intraoperative microelectrode recordings in patients undergoing surgery for deep brain stimulation (DBS) to investigate the activity of single neurons related to cardiac and respiratory functions in three subcortical regions: ventral intermedius nucleus (Vim) and ventral caudalis nucleus (Vc) of the thalamus, and subthalamic nucleus (STN). We report that the activity of a large portion of the recorded neurons (about 70%) was modulated by either the heartbeat, the cardiac inter-beat interval, or the respiration. These cardiac and respiratory response patterns varied largely across neurons both in terms of timing and their kind of modulation. A substantial proportion of these visceral neurons (30%) was responsive to more than one of the tested signals, underlining specialization and integration of cardiac and respiratory signals in STN and thalamic neurons. By extensively describing single unit activity related to cardiorespiratory function in thalamic and subthalamic neurons, our results highlight the major role of these subcortical regions in the processing of visceral signals.
Subject(s)
Deep Brain Stimulation , Subthalamic Nucleus , Animals , Humans , Thalamus/physiology , Neurons/physiology , MicroelectrodesABSTRACT
Episodic autobiographical memories are characterized by a spatial context and an affective component. But how do affective and spatial aspects interact? Does affect modulate the way we encode the spatial context of events? We investigated how one element of affect, namely aesthetic liking, modulates memory for location, in three online experiments (n = 124, 79, and 80). Participants visited a professionally curated virtual art exhibition. They then relocated previously viewed artworks on the museum map and reported how much they liked them. Across all experiments, liking an artwork was associated with increased ability to recall the wall on which it was hung. The effect was not explained by viewing time and appeared to modulate recognition speed. The liking-wall memory effect remained when participants attended to abstractness, rather than liking, and when testing occurred 24 h after the museum visit. Liking also modulated memory for the room where a work of art was hung, but this effect primarily involved reduced room memory for disliked artworks. Further, the liking-wall memory effect remained after controlling for effects of room memory. Recalling the wall requires recalling one's facing direction, so our findings suggest that positive aesthetic experiences enhance first-person spatial representations. More generally, a first-person component of positive affect transfers to wider spatial representation and facilitates the encoding of locations in a subject-centered reference frame. Affect and spatial representations are therefore important, and linked, elements of sentience and subjectivity. Memories of aesthetic experiences are also spatial memories of how we encountered a work of art. This linkage may have implications for museum design.
Subject(s)
Memory, Episodic , Emotions , Esthetics , Humans , Mental Recall , MuseumsABSTRACT
Stimulation and functional imaging studies have revealed the existence of a large network of cortical regions involved in the regulation of heart rate. However, very little is known about the link between cortical neural firing and cardiac-cycle duration (CCD). Here, we analyze single-unit and multiunit data obtained in humans at rest, and show that firing rate covaries with CCD in 16.7% of the sample (25 of 150). The link between firing rate and CCD was most prevalent in the anterior medial temporal lobe (entorhinal and perirhinal cortices, anterior hippocampus, and amygdala), where 36% (18 of 50) of the units show the effect, and to a lesser extent in the mid-to-anterior cingulate cortex (11.1%, 5 of 45). The variance in firing rate explained by CCD ranged from 0.5 to 11%. Several lines of analysis indicate that neural firing influences CCD, rather than the other way around, and that neural firing affects CCD through vagally mediated mechanisms in most cases. These results show that part of the spontaneous fluctuations in firing rate can be attributed to the cortical control of the cardiac cycle. The fine tuning of the regulation of CCD represents a novel physiological factor accounting for spontaneous variance in firing rate. It remains to be determined whether the "noise" introduced in firing rate by the regulation of CCD is detrimental or beneficial to the cognitive information processing carried out in the parahippocampal and cingulate regions.SIGNIFICANCE STATEMENT Fluctuations in heart rate are known to be under the control of cortical structures, but spontaneous fluctuations in cortical firing rate, or "noise," have seldom been related to heart rate. Here, we analyze unit activity in humans at rest and show that spontaneous fluctuations in neural firing in the medial temporal lobe, as well as in the mid-to-anterior cingulate cortex, influence heart rate. This phenomenon was particularly pronounced in the entorhinal and perirhinal cortices, where it could be observed in one of three neurons. Our results show that part of spontaneous firing rate variability in regions best known for their cognitive role in spatial navigation and memory corresponds to precise physiological regulations.
Subject(s)
Action Potentials/physiology , Gyrus Cinguli/physiology , Heart Rate/physiology , Neurons/physiology , Parahippocampal Gyrus/physiology , Rest/physiology , Adult , Drug Resistant Epilepsy/diagnosis , Drug Resistant Epilepsy/physiopathology , Electrocardiography/methods , Female , Gyrus Cinguli/cytology , Humans , Male , Parahippocampal Gyrus/cytologyABSTRACT
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, during imagination, neither external stimuli nor motor feedback are available 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 and posterior cingulate regions bilaterally. Effect size was modulated by the daydreaming frequency scores 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 (e.g. arousal ratings, pupil diameter). Heartbeat-evoked responses thus appear as a neural marker distinguishing self from other during imagination.
Subject(s)
Brain/physiology , Heart Rate/physiology , Imagination/physiology , Self Concept , Adult , Female , Humans , MaleABSTRACT
UNLABELLED: The default network (DN) has been consistently associated with self-related cognition, but also to bodily state monitoring and autonomic regulation. We hypothesized that these two seemingly disparate functional roles of the DN are functionally coupled, in line with theories proposing that selfhood is grounded in the neural monitoring of internal organs, such as the heart. We measured with magnetoencephalograhy neural responses evoked by heartbeats while human participants freely mind-wandered. When interrupted by a visual stimulus at random intervals, participants scored the self-relatedness of the interrupted thought. They evaluated their involvement as the first-person perspective subject or agent in the thought ("I"), and on another scale to what degree they were thinking about themselves ("Me"). During the interrupted thought, neural responses to heartbeats in two regions of the DN, the ventral precuneus and the ventromedial prefrontal cortex, covaried, respectively, with the "I" and the "Me" dimensions of the self, even at the single-trial level. No covariation between self-relatedness and peripheral autonomic measures (heart rate, heart rate variability, pupil diameter, electrodermal activity, respiration rate, and phase) or alpha power was observed. Our results reveal a direct link between selfhood and neural responses to heartbeats in the DN and thus directly support theories grounding selfhood in the neural monitoring of visceral inputs. More generally, the tight functional coupling between self-related processing and cardiac monitoring observed here implies that, even in the absence of measured changes in peripheral bodily measures, physiological and cognitive functions have to be considered jointly in the DN. SIGNIFICANCE STATEMENT: The default network (DN) has been consistently associated with self-processing but also with autonomic regulation. We hypothesized that these two functions could be functionally coupled in the DN, inspired by theories according to which selfhood is grounded in the neural monitoring of internal organs. Using magnetoencephalography, we show that heartbeat-evoked responses (HERs) in the DN covary with the self-relatedness of ongoing spontaneous thoughts. HER amplitude in the ventral precuneus covaried with the "I" self-dimension, whereas HER amplitude in the ventromedial prefrontal cortex encoded the "Me" self-dimension. Our experimental results directly support theories rooting selfhood in the neural monitoring of internal organs. We propose a novel functional framework for the DN, where self-processing is coupled with physiological monitoring.
Subject(s)
Attention/physiology , Autonomic Nervous System/physiology , Heart Rate/physiology , Nerve Net/physiology , Prefrontal Cortex/physiology , Thinking/physiology , Adult , Cognition/physiology , Feedback, Physiological/physiology , Female , Humans , MaleABSTRACT
A fundamental feature of the temporal organization of neural activity is phase-amplitude coupling between brain rhythms at different frequencies, where the amplitude of a higher frequency varies according to the phase of a lower frequency. Here, we show that this rule extends to brain-organ interactions. We measured both the infra-slow (~0.05Hz) rhythm intrinsically generated by the stomach - the gastric basal rhythm - using electrogastrography, and spontaneous brain dynamics with magnetoencephalography during resting-state with eyes open. We found significant phase-amplitude coupling between the infra-slow gastric phase and the amplitude of the cortical alpha rhythm (10-11Hz), with gastric phase accounting for 8% of the variance of alpha rhythm amplitude fluctuations. Gastric-alpha coupling was localized to the right anterior insula, and bilaterally to occipito-parietal regions. Transfer entropy, a measure of directionality of information transfer, indicates that gastric-alpha coupling is due to an ascending influence from the stomach to both the right anterior insula and occipito-parietal regions. Our results show that phase-amplitude coupling so far only observed within the brain extends to brain-viscera interactions. They further reveal that the temporal structure of spontaneous brain activity depends not only on neuron and network properties endogenous to the brain, but also on the slow electrical rhythm generated by the stomach.
Subject(s)
Alpha Rhythm , Brain/physiology , Stomach/physiology , Adult , Female , Humans , Magnetoencephalography , Male , Neural Pathways/physiology , Stomach/innervation , Young AdultABSTRACT
The interplay between the brain and interoceptive signals is key in maintaining internal balance and orchestrating neural dynamics, encompassing influences on perceptual and self-awareness. Central to this interplay is the differentiation between the external world, others and the self, a cornerstone in the construction of bodily self-awareness. This review synthesizes physiological and behavioral evidence illustrating how interoceptive signals can mediate or influence bodily self-awareness, by encompassing interactions with various sensory modalities. To deepen our understanding of the basis of bodily self-awareness, we propose a network physiology perspective. This approach explores complex neural computations across multiple nodes, shifting the focus from localized areas to large-scale neural networks. It examines how these networks operate in parallel with and adapt to changes in visceral activities. Within this framework, we propose to investigate physiological factors that disrupt bodily self-awareness, emphasizing the impact of interoceptive pathway disruptions, offering insights across several clinical contexts. This integrative perspective not only can enhance the accuracy of mental health assessments but also paves the way for targeted interventions.
ABSTRACT
Why should a scientist whose aim is to unravel the neural mechanisms of perception consider brain-body interactions seriously? Brain-body interactions have traditionally been associated with emotion, effort, or stress, but not with the "cold" processes of perception and attention. Here, we review recent experimental evidence suggesting a different picture: the neural monitoring of bodily state, and in particular the neural monitoring of the heart, affects visual perception. The impact of spontaneous fluctuations of neural responses to heartbeats on visual detection is as large as the impact of explicit manipulations of spatial attention in perceptual tasks. However, we propose that the neural monitoring of visceral inputs plays a specific role in conscious perception, distinct from the role of attention. The neural monitoring of organs such as the heart or the gut would generate a subject-centered reference frame, from which the first-person perspective inherent to conscious perception can develop. In this view, conscious perception results from the integration of visual content with first-person perspective.
Subject(s)
Attention/physiology , Brain/physiology , Consciousness/physiology , Visual Perception/physiology , Brain Mapping , Humans , Perception/physiologyABSTRACT
The self has been proposed to be rooted in the neural monitoring of internal bodily signals and might thus involve interoceptive areas, notably the right anterior insula (rAI). However, studies on the self consistently showed the involvement of midline default network (DN) nodes, without referring to visceral monitoring. Here, we investigate this apparent discrepancy. We previously showed that neural responses to heartbeats in the DN encode two different self-dimensions, the agentive 'I' and the introspective 'Me', in a whole-brain analysis of magnetoencephalography (MEG) data. Here, we confirm and anatomically refine this result with intracranial recordings (intracranial electroencephalography, iEEG). In two patients, we show a parametric modulation of neural responses to heartbeats by the self-relatedness of thoughts, at the single trial level. A region-of-interest analysis of the insula reveals that MEG responses to heartbeats in the rAI encode the 'I' self-dimension. The effect in rAI was weaker than in the DN and was replicated in iEEG data in one patient out of two. We propose that a common mechanism, the neural monitoring of cardiac signals, underlies the self in both the DN and rAI. This might reconcile studies on the self highlighting the DN, with studies on interoception focusing on the insula.This article is part of the themed issue 'Interoception beyond homeostasis: affect, cognition and mental health'.
Subject(s)
Cerebral Cortex/physiology , Cognition , Heart Rate , Interoception , Nerve Net , Adult , Electrocorticography , Feedback, Physiological , Female , Humans , Male , Young AdultABSTRACT
Is our perceptual experience of a stimulus entirely determined during the early buildup of the sensory representation, within 100 to 150 ms following stimulation? Or can later influences, such as sensory reactivation, still determine whether we become conscious of a stimulus? Late visual reactivation can be experimentally induced by postcueing attention after visual stimulus offset. In a contrary approach from previous work on postcued attention and visual short-term memory, which used multiple item displays, we tested the influence of postcued attention on perception, using a single visual stimulus (Gabor patch) at threshold contrast. We showed that attracting attention to the stimulus location 100 to 400 ms after presentation still drastically improved the viewers' objective capacity to detect its presence and to discriminate its orientation, along with drastic increase in subjective visibility. This retroperception effect demonstrates that postcued attention can retrospectively trigger the conscious perception of a stimulus that would otherwise have escaped consciousness. It was known that poststimulus events could either suppress consciousness, as in masking, or alter conscious content, as in the flash-lag illusion. Our results show that conscious perception can also be triggered by an external event several hundred ms after stimulus offset, underlining unsuspected temporal flexibility in conscious perception.