Breakdown of Cortical Effective Connectivity During Sleep.

University of Milan, Milano, Lombardy, Italy
Science (Impact Factor: 33.61). 10/2005; 309(5744):2228-32. DOI: 10.1126/science.1117256
Source: PubMed


When we fall asleep, consciousness fades yet the brain remains active. Why is this so? To investigate whether changes in cortical information transmission play a role, we used transcranial magnetic stimulation together with high-density electroencephalography and asked how the activation of one cortical area (the premotor area) is transmitted to the rest of the brain. During quiet wakefulness, an initial response (approximately 15 milliseconds) at the stimulation site was followed by a sequence of waves that moved to connected cortical areas several centimeters away. During non-rapid eye movement sleep, the initial response was stronger but was rapidly extinguished and did not propagate beyond the stimulation site. Thus, the fading of consciousness during certain stages of sleep may be related to a breakdown in cortical effective connectivity.

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Available from: Giulio Tononi,
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    • "At the integrated system level, plasticity and neuromodulation have crucial roles in altering excitability in the brain and regulating physiological states such as sleep and wake (Gorgoni et al., 2013). Such modulation of excitatory and inhibitory brain activity during different physiologic states and conditions leads to specific brain waves with dominant frequencies—e.g., higher frequency α-wave associated with higher excitability and dissynchronous cortical activation during quiet wake, and low frequency δ-wave associated with low excitability and global synchronous activation during deep sleep (Kryger et al., 1994; Massimini et al., 2005; Niedermeyer and da Silva, 2005; Siegel, 2005). In addition to dominant brain waves, physiological states are characterized by specific signatures in the temporal modulation of brain waves (Linkenkaer-Hansen et al., 2001; Poil et al., 2008) and their synchronization across different locations (White et al., 1998; Kopell et al., 2000). "
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    ABSTRACT: Neural plasticity transcends a range of spatio-temporal scales and serves as the basis of various brain activities and physiologic functions. At the microscopic level, it enables the emergence of brain waves with complex temporal dynamics. At the macroscopic level, presence and dominance of specific brain waves is associated with important brain functions. The role of neural plasticity at different levels in generating distinct brain rhythms and how brain rhythms communicate with each other across brain areas to generate physiologic states and functions remains not understood. Here we perform an empirical exploration of neural plasticity at the level of brain wave network interactions representing dynamical communications within and between different brain areas in the frequency domain. We introduce the concept of time delay stability (TDS) to quantify coordinated bursts in the activity of brain waves, and we employ a system-wide Network Physiology integrative approach to probe the network of coordinated brain wave activations and its evolution across physiologic states. We find an association between network structure and physiologic states. We uncover a hierarchical reorganization in the brain wave networks in response to changes in physiologic state, indicating new aspects of neural plasticity at the integrated level. Globally, we find that the entire brain network undergoes a pronounced transition from low connectivity in Deep Sleep and REM to high connectivity in Light Sleep and Wake. In contrast, we find that locally, different brain areas exhibit different network dynamics of brain wave interactions to achieve differentiation in function during different sleep stages. Moreover, our analyses indicate that plasticity also emerges in frequency-specific networks, which represent interactions across brain locations mediated through a specific frequency band. Comparing frequency-specific networks within the same physiologic state we find very different degree of network connectivity and link strength, while at the same time each frequency-specific network is characterized by a different signature pattern of sleep-stage stratification, reflecting a remarkable flexibility in response to change in physiologic state. These new aspects of neural plasticity demonstrate that in addition to dominant brain waves, the network of brain wave interactions is a previously unrecognized hallmark of physiologic state and function.
    Frontiers in Neural Circuits 10/2015; Front Neural Circuits(9):62. DOI:10.3389/fncir.2015.00062 · 3.60 Impact Factor
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    • "its phase transition and thus to connect two robust but seemingly unrelated findings characterizing states of reduced awareness: loss of temporal complexity (i.e. long-range temporal correlations [Tagliazucchi et al., 2013a]) and rapidly vanishing responses to direct magnetic and electric stimulation of the cortex (Massimini et al., 2005; Ferrarelli et al., 2010; Casali et al., 2013; Pigorini et al., 2015). Within our framework, both arise as a result of increased stability, with endogenous as well as exogenous fluctuations failing to displace the system between different metastable states. "
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    ABSTRACT: Loss of cortical integration and changes in the dynamics of electrophysiological brain signals characterize the transition from wakefulness towards unconsciousness. The common mechanism underlying these observations remains unknown. In this study we arrive at a basic model, which explains these empirical observations based on the theory of phase transitions in complex systems. We studied the link between spatial and temporal correlations of large-scale brain activity recorded with functional magnetic resonance imaging during wakefulness, propofol-induced sedation and loss of consciousness, as well as during the subsequent recovery. We observed that during unconsciousness activity in frontal and thalamic regions exhibited a reduction of long-range temporal correlations and a departure of functional connectivity from the underlying anatomical constraints. These changes in dynamics and anatomy-function coupling were correlated across participants, suggesting that temporal complexity and an efficient exploration of anatomical connectivity are inter-related phenomena. A model of a system exhibiting a phase transition reproduced our findings, as well as the diminished sensitivity of the cortex to external perturbations during unconsciousness. This theoretical framework unifies different empirical observations about brain activity during unconsciousness and predicts that the principles we identified are universal and independent of the causes behind loss of awareness.
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    • "The activity states observed in the CXC network have analogs in real brains. The slow oscillations and global coupling seen at low AAS input levels in the CXC network are similar to the strong delta oscillations and very low dynamical complexity observed during deep (non-REM) sleep (Massimini et al., 2005; Murphy et al., 2009). "
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    Frontiers in Systems Neuroscience 08/2015; 9. DOI:10.3389/fnsys.2015.00119
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