Periodic Reporting for period 1 - cICMs (Causal Roles of Intrinsic Coupling Modes: an Integrated Multiscale Framework for Cognitive Network Dynamics)
Période du rapport: 2023-07-01 au 2025-12-31
Cognitive and sensorimotor processes are based on the activation of highly distributed networks in the brain involving numerous interacting modules and brain regions. It is widely assumed that neuronal network interaction, at multiple spatiotemporal scales, is one of the crucial determinants of cognition and behavior, and that it is the ability for flexible configuration of functional coupling that underlies the information processing capabilities of the brain and the complexity of its dynamics.
Indeed, functional coupling is a hallmark of brain networks, and there is a wealth of studies that have observed a relation between functional connectivity patterns and cognition or sensorimotor processing. However, despite the advances they have provided, the vast majority of studies available on this topic are still correlative in nature, revealing only associations between dynamic neural coupling and network functions.
The vast majority of functional connectivity patterns observed in the brain are intrinsically generated, i.e. they are not imposed by entrainment to external stimuli but emerge from network connectivity and brain-internal factors. We term these patterns intrinsic coupling modes (ICMs). ICMs can be studied with a broad variety of methods, ranging from single-cell and local field potential (LFP) recordings to electroencephalography (EEG) and magnetoencephalography (MEG).
ICMs occur on a broad range of spatial and temporal scales, involving two distinct types of dynamics. One type of ICMs involves oscillatory signals with band-limited dynamics, can be quantified by measures of phase coupling and typically occurs at frequencies between about 1 Hz and 150 Hz. The second type of ICMs corresponds to coupled fluctuations on slower time scales and can be uncovered by correlation of signal envelopes. We designate these as phase ICMs and envelope ICMs, respectively.
The cICMs project aims to obtain causal evidence on the functional roles of ICMs. We use multi-site interventions to manipulate phase and envelope coupling and test the impact on stimulus processing and behavior. We investigate ICMs during tasks in order to test differences between both types of ICMs regarding their relation to cognitive processing. Furthermore, we aim to unravel potential interactions between phase and envelope ICMs. Importantly, we aim to develop a coherent framework for multiscale coupling dynamics. Modeling and information-theoretic analyses of the experimental data serve to integrate the results across scales and species and, thus, to derive a unified framework for multiscale coupling dynamics.
The central hypothesis of this project is that both types of ICMs have causal relevance for cognitive processing and behavior. Phase ICMs have been proposed to enable communication between neuronal populations in a spatiotemporally precise manner and to serve for flexible routing of signals. Envelope ICMs, in contrast, may couple excitability fluctuations between neuronal populations and, thus, regulate their recruitment into the same cognitive process or task. What is currently lacking is a research program that puts these different coupling modes in a unifying perspective. The overarching goal of this project is to provide such an integrated view.
Indeed, functional coupling is a hallmark of brain networks, and there is a wealth of studies that have observed a relation between functional connectivity patterns and cognition or sensorimotor processing. However, despite the advances they have provided, the vast majority of studies available on this topic are still correlative in nature, revealing only associations between dynamic neural coupling and network functions.
The vast majority of functional connectivity patterns observed in the brain are intrinsically generated, i.e. they are not imposed by entrainment to external stimuli but emerge from network connectivity and brain-internal factors. We term these patterns intrinsic coupling modes (ICMs). ICMs can be studied with a broad variety of methods, ranging from single-cell and local field potential (LFP) recordings to electroencephalography (EEG) and magnetoencephalography (MEG).
ICMs occur on a broad range of spatial and temporal scales, involving two distinct types of dynamics. One type of ICMs involves oscillatory signals with band-limited dynamics, can be quantified by measures of phase coupling and typically occurs at frequencies between about 1 Hz and 150 Hz. The second type of ICMs corresponds to coupled fluctuations on slower time scales and can be uncovered by correlation of signal envelopes. We designate these as phase ICMs and envelope ICMs, respectively.
The cICMs project aims to obtain causal evidence on the functional roles of ICMs. We use multi-site interventions to manipulate phase and envelope coupling and test the impact on stimulus processing and behavior. We investigate ICMs during tasks in order to test differences between both types of ICMs regarding their relation to cognitive processing. Furthermore, we aim to unravel potential interactions between phase and envelope ICMs. Importantly, we aim to develop a coherent framework for multiscale coupling dynamics. Modeling and information-theoretic analyses of the experimental data serve to integrate the results across scales and species and, thus, to derive a unified framework for multiscale coupling dynamics.
The central hypothesis of this project is that both types of ICMs have causal relevance for cognitive processing and behavior. Phase ICMs have been proposed to enable communication between neuronal populations in a spatiotemporally precise manner and to serve for flexible routing of signals. Envelope ICMs, in contrast, may couple excitability fluctuations between neuronal populations and, thus, regulate their recruitment into the same cognitive process or task. What is currently lacking is a research program that puts these different coupling modes in a unifying perspective. The overarching goal of this project is to provide such an integrated view.
To achieve the project objectives, we apply a translational approach which combines EEG and MEG recordings in humans with invasive recordings in ferrets. The human MEG data provide insights into ICMs underlying cognitive processes, which are then manipulated by noninvasive electrical neurostimulation. Ferrets provide a highly suited animal model which allows high-resolution recordings and targeted optogenetic manipulation of ICMs. We combine our experimental investigations with multiscale modeling and information-theoretic analyses of the relation of ICMs to behavior.
The workplan of the cICMs project encompasses four workpackages (WP) that address the project objectives. WP1 tests predictions regarding the functional roles of different ICMs at the macroscale in the human brain. WP2 comprises studies on ICMs at the meso- and microscale in anesthetized and behaving ferrets. WP3 aims to provide causal evidence through interventions using optogenetic approaches as well as electrical brain stimulation, which allow us to probe mechanisms and functional relevance of ICMs. WP4 aims to provide novel methods for data analysis in the experimental WPs and to integrate experimental results by modeling and information-theoretic analyses, in order to eventually provide a coherent framework for multiscale interaction dynamics.
Our work in the first two years of the project can be summarized as follows. Our studies of ICMs in the human brain (WP1) provide clear evidence for a relation of amplitude coupling to attentional processing. Studies in the ferret (WP2) demonstrate task-related changes of phase ICMs. Furthermore, we could demonstrate causal interactions between envelope and phase ICMs, in particular in low frequency ranges. We used transcranial alternating current stimulation (tACS) to modulate ICMs in the human brain (WP3). We could show that amplitude-modulated tACS can be employed to alter envelope ICMs in resting-state activity. In ferrets, we obtained evidence for specific effects of frequency- and amplitude-modulated optogenetic stimulation on phase and envelope ICMs in sensory and parietal cortical regions (WP3). As part of the work in WP4, we advanced methods for investigation of coupling modes in EEG/MEG data, and we applied Partial Information Decomposition to quantify redundant and synergistic components in the information carried by neural signals in ferret data. Furthermore, we elaborated on the notion of multi-timescale neural dynamics in a conceptual publication.
The workplan of the cICMs project encompasses four workpackages (WP) that address the project objectives. WP1 tests predictions regarding the functional roles of different ICMs at the macroscale in the human brain. WP2 comprises studies on ICMs at the meso- and microscale in anesthetized and behaving ferrets. WP3 aims to provide causal evidence through interventions using optogenetic approaches as well as electrical brain stimulation, which allow us to probe mechanisms and functional relevance of ICMs. WP4 aims to provide novel methods for data analysis in the experimental WPs and to integrate experimental results by modeling and information-theoretic analyses, in order to eventually provide a coherent framework for multiscale interaction dynamics.
Our work in the first two years of the project can be summarized as follows. Our studies of ICMs in the human brain (WP1) provide clear evidence for a relation of amplitude coupling to attentional processing. Studies in the ferret (WP2) demonstrate task-related changes of phase ICMs. Furthermore, we could demonstrate causal interactions between envelope and phase ICMs, in particular in low frequency ranges. We used transcranial alternating current stimulation (tACS) to modulate ICMs in the human brain (WP3). We could show that amplitude-modulated tACS can be employed to alter envelope ICMs in resting-state activity. In ferrets, we obtained evidence for specific effects of frequency- and amplitude-modulated optogenetic stimulation on phase and envelope ICMs in sensory and parietal cortical regions (WP3). As part of the work in WP4, we advanced methods for investigation of coupling modes in EEG/MEG data, and we applied Partial Information Decomposition to quantify redundant and synergistic components in the information carried by neural signals in ferret data. Furthermore, we elaborated on the notion of multi-timescale neural dynamics in a conceptual publication.
The cICMs project will close a critical gap in network neuroscience by providing causal evidence on coupling modes. Critical evidence will be provided on whether ICMs are just epiphenomena of the structural connectivity, or whether they indeed have a causal role for information processing and behavior.
Furthermore, this project will lead to a recasting of the concepts of functional and effective connectivity, which are central notions of network neuroscience, by providing a comprehensive account of coupling modes across different spatiotemporal scales.
Research in this project also has translational implications. The approach used here is likely to have implications for a wide range of neurological and psychiatric disorders that involve network malfunctions. Multiscale analysis of ICMs may lead to the development of novel network-based markers for monitoring clinical outcomes and for evaluating therapeutic interventions.
Furthermore, this project will lead to a recasting of the concepts of functional and effective connectivity, which are central notions of network neuroscience, by providing a comprehensive account of coupling modes across different spatiotemporal scales.
Research in this project also has translational implications. The approach used here is likely to have implications for a wide range of neurological and psychiatric disorders that involve network malfunctions. Multiscale analysis of ICMs may lead to the development of novel network-based markers for monitoring clinical outcomes and for evaluating therapeutic interventions.