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Auditory Resting-State Network Connectivity in Tinnitus: A Functional MRI Study
Audrey Maudoux, Philippe Lefebvre, Jean-Evrard Cabay, Athena Demertzi, Audrey Vanhaudenhuyse, Steven Laureys, Andrea Soddu
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0036222
Abstract: The underlying functional neuroanatomy of tinnitus remains poorly understood. Few studies have focused on functional cerebral connectivity changes in tinnitus patients. The aim of this study was to test if functional MRI “resting-state” connectivity patterns in auditory network differ between tinnitus patients and normal controls. Thirteen chronic tinnitus subjects and fifteen age-matched healthy controls were studied on a 3 tesla MRI. Connectivity was investigated using independent component analysis and an automated component selection approach taking into account the spatial and temporal properties of each component. Connectivity in extra-auditory regions such as brainstem, basal ganglia/NAc, cerebellum, parahippocampal, right prefrontal, parietal, and sensorimotor areas was found to be increased in tinnitus subjects. The right primary auditory cortex, left prefrontal, left fusiform gyrus, and bilateral occipital regions showed a decreased connectivity in tinnitus. These results show that there is a modification of cortical and subcortical functional connectivity in tinnitus encompassing attentional, mnemonic, and emotional networks. Our data corroborate the hypothesized implication of non-auditory regions in tinnitus physiopathology and suggest that various regions of the brain seem involved in the persistent awareness of the phenomenon as well as in the development of the associated distress leading to disabling chronic tinnitus.
Diagnostic accuracy of the vegetative and minimally conscious state: Clinical consensus versus standardized neurobehavioral assessment
Caroline Schnakers, Audrey Vanhaudenhuyse, Joseph Giacino, Manfredi Ventura, Melanie Boly, Steve Majerus, Gustave Moonen, Steven Laureys
BMC Neurology , 2009, DOI: 10.1186/1471-2377-9-35
Abstract: We prospectively followed 103 patients (55 ± 19 years) with mixed etiologies and compared the clinical consensus diagnosis provided by the physician on the basis of the medical staff's daily observations to diagnoses derived from CRS-R assessments performed by research staff. All patients were assigned a diagnosis of 'VS', 'MCS' or 'uncertain diagnosis.'Of the 44 patients diagnosed with VS based on the clinical consensus of the medical team, 18 (41%) were found to be in MCS following standardized assessment with the CRS-R. In the 41 patients with a consensus diagnosis of MCS, 4 (10%) had emerged from MCS, according to the CRS-R. We also found that the majority of patients assigned an uncertain diagnosis by clinical consensus (89%) were in MCS based on CRS-R findings.Despite the importance of diagnostic accuracy, the rate of misdiagnosis of VS has not substantially changed in the past 15 years. Standardized neurobehavioral assessment is a more sensitive means of establishing differential diagnosis in patients with disorders of consciousness when compared to diagnoses determined by clinical consensus.Differentiating the vegetative (VS) from minimally conscious state (MCS) is often one of the most challenging tasks facing clinicians involved in the care of patients with disorders of consciousness (DOC). Whereas VS is characterized by the return of arousal without signs of awareness [1], MCS is defined by the presence of inconsistent but reproducible goal-directed behaviors (e.g. response to command, verbalizations, visual pursuit, etc.) [2]. Behavioral assessment remains the "gold standard" for detecting signs of consciousness and, hence, for determining diagnosis [3]. However, behavioral assessment is complicated by the presence of motor impairment, tracheotomy, fluctuating arousal level or ambiguous and rapidly habituating responses [4]. Previous studies have shown that 37 to 43% of patients diagnosed with VS demonstrated signs of awareness [5,6]. Misdiagnosis can le
Brain Connectivity in Pathological and Pharmacological Coma
Quentin Noirhomme,Andrea Soddu,Rémy Lehembre,Audrey Vanhaudenhuyse,Pierre Boveroux,Mélanie Boly,Steven Laureys
Frontiers in Systems Neuroscience , 2010, DOI: 10.3389/fnsys.2010.00160
Abstract: Recent studies in patients with disorders of consciousness (DOC) tend to support the view that awareness is not related to activity in a single brain region but to thalamo-cortical connectivity in the frontoparietal network. Functional neuroimaging studies have shown preserved albeit disconnected low-level cortical activation in response to external stimulation in patients in a “vegetative state” or unresponsive wakefulness syndrome. While activation of these “primary” sensory cortices does not necessarily reflect conscious awareness, activation in higher-order associative cortices in minimally conscious state patients seems to herald some residual perceptual awareness. PET studies have identified a metabolic dysfunction in a widespread frontoparietal “global neuronal workspace” in DOC patients including the midline default mode network (“intrinsic” system) and the lateral frontoparietal cortices or “extrinsic system.” Recent studies have investigated the relation of awareness to the functional connectivity within intrinsic and extrinsic networks, and with the thalami in both pathological and pharmacological coma. In brain damaged patients, connectivity in all default network areas was found to be non-linearly correlated with the degree of clinical consciousness impairment, ranging from healthy controls and locked-in syndrome to minimally conscious, vegetative, coma, and brain dead patients. Anesthesia-induced loss of consciousness was also shown to correlate with a global decrease in cortico-cortical and thalamo-cortical connectivity in both intrinsic and extrinsic networks, but not in auditory, or visual networks. In anesthesia, unconsciousness was also associated with a loss of cross-modal interactions between networks. These results suggest that conscious awareness critically depends on the functional integrity of thalamo-cortical and cortico-cortical frontoparietal connectivity within and between “intrinsic” and “extrinsic” brain networks.
Characteristics of Near-Death Experiences Memories as Compared to Real and Imagined Events Memories
Marie Thonnard, Vanessa Charland-Verville, Serge Brédart, Hedwige Dehon, Didier Ledoux, Steven Laureys, Audrey Vanhaudenhuyse
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0057620
Abstract: Since the dawn of time, Near-Death Experiences (NDEs) have intrigued and, nowadays, are still not fully explained. Since reports of NDEs are proposed to be imagined events, and since memories of imagined events have, on average, fewer phenomenological characteristics than real events memories, we here compared phenomenological characteristics of NDEs reports with memories of imagined and real events. We included three groups of coma survivors (8 patients with NDE as defined by the Greyson NDE scale, 6 patients without NDE but with memories of their coma, 7 patients without memories of their coma) and a group of 18 age-matched healthy volunteers. Five types of memories were assessed using Memory Characteristics Questionnaire (MCQ – Johnson et al., 1988): target memories (NDE for NDE memory group, coma memory for coma memory group, and first childhood memory for no memory and control groups), old and recent real event memories and old and recent imagined event memories. Since NDEs are known to have high emotional content, participants were requested to choose the most emotionally salient memories for both real and imagined recent and old event memories. Results showed that, in NDE memories group, NDE memories have more characteristics than memories of imagined and real events (p<0.02). NDE memories contain more self-referential and emotional information and have better clarity than memories of coma (all ps<0.02). The present study showed that NDE memories contained more characteristics than real event memories and coma memories. Thus, this suggests that they cannot be considered as imagined event memories. On the contrary, their physiological origins could lead them to be really perceived although not lived in the reality. Further work is needed to better understand this phenomenon.
Visual fixation in the vegetative state: an observational case series PET study
Marie-Aurélie Bruno, Audrey Vanhaudenhuyse, Caroline Schnakers, Mélanie Boly, Olivia Gosseries, Athena Demertzi, Steve Majerus, Gustave Moonen, Roland Hustinx, Steven Laureys
BMC Neurology , 2010, DOI: 10.1186/1471-2377-10-35
Abstract: We here studied cerebral metabolism in ten patients with chronic post-anoxic encephalopathy and 39 age-matched healthy controls. Five patients were in a vegetative state (without fixation) and five presented visual fixation but otherwise showed all criteria typical of the vegetative state. Patients were matched for age, etiology and time since insult and were followed by repeated Coma Recovery Scale-Revised (CRS-R) assessments for at least 1 year. Sustained visual fixation was considered as present when the eyes refixated a moving target for more than 2 seconds as defined by CRS-R criteria.Patients without fixation showed metabolic dysfunction in a widespread fronto-parietal cortical network (with only sparing of the brainstem and cerebellum) which was not different from the brain function seen in patients with visual fixation. Cortico-cortical functional connectivity with visual cortex showed no difference between both patient groups. Recovery rates did not differ between patients without or with fixation (none of the patients showed good outcome).Our findings suggest that sustained visual fixation in (non-traumatic) disorders of consciousness does not necessarily reflect consciousness and higher order cortical brain function.It is still a matter of debate whether visual fixation indicates "automatic" subcortical processing (i.e., is compatible with the diagnosis of the vegetative state; VS [1,2]) or whether it is a cognitively mediated behavior that heralds consciousness and higher order cortical processing (i.e., sufficient for the diagnosis of the minimallyconscious state; MCS [3]). According to the Multi Society Task Force on PVS in "rare cases, patients who have no other evidence of consciousness over a period of months to years have some degree of briefly sustained visual fixation, which is believed to be mediated through brainstem structures"[1]. Similarly, UK guidelines state that "visual fixation of a target" is a "compatible but atypical feature" of the V
Dynamic Change of Global and Local Information Processing in Propofol-Induced Loss and Recovery of Consciousness
Martin M. Monti ,Evan S. Lutkenhoff,Mikail Rubinov,Pierre Boveroux,Audrey Vanhaudenhuyse,Olivia Gosseries,Marie-Aurélie Bruno,Quentin Noirhomme,Mélanie Boly,Steven Laureys
PLOS Computational Biology , 2013, DOI: 10.1371/journal.pcbi.1003271
Abstract: Whether unique to humans or not, consciousness is a central aspect of our experience of the world. The neural fingerprint of this experience, however, remains one of the least understood aspects of the human brain. In this paper we employ graph-theoretic measures and support vector machine classification to assess, in 12 healthy volunteers, the dynamic reconfiguration of functional connectivity during wakefulness, propofol-induced sedation and loss of consciousness, and the recovery of wakefulness. Our main findings, based on resting-state fMRI, are three-fold. First, we find that propofol-induced anesthesia does not bear differently on long-range versus short-range connections. Second, our multi-stage design dissociated an initial phase of thalamo-cortical and cortico-cortical hyperconnectivity, present during sedation, from a phase of cortico-cortical hypoconnectivity, apparent during loss of consciousness. Finally, we show that while clustering is increased during loss of consciousness, as recently suggested, it also remains significantly elevated during wakefulness recovery. Conversely, the characteristic path length of brain networks (i.e., the average functional distance between any two regions of the brain) appears significantly increased only during loss of consciousness, marking a decrease of global information-processing efficiency uniquely associated with unconsciousness. These findings suggest that propofol-induced loss of consciousness is mainly tied to cortico-cortical and not thalamo-cortical mechanisms, and that decreased efficiency of information flow is the main feature differentiating the conscious from the unconscious brain.
Changes in Effective Connectivity by Propofol Sedation
Francisco Gómez, Christophe Phillips, Andrea Soddu, Melanie Boly, Pierre Boveroux, Audrey Vanhaudenhuyse, Marie-Aurélie Bruno, Olivia Gosseries, Vincent Bonhomme, Steven Laureys, Quentin Noirhomme
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0071370
Abstract: Mechanisms of propofol-induced loss of consciousness remain poorly understood. Recent fMRI studies have shown decreases in functional connectivity during unconsciousness induced by this anesthetic agent. Functional connectivity does not provide information of directional changes in the dynamics observed during unconsciousness. The aim of the present study was to investigate, in healthy humans during an auditory task, the changes in effective connectivity resulting from propofol induced loss of consciousness. We used Dynamic Causal Modeling for fMRI (fMRI-DCM) to assess how causal connectivity is influenced by the anesthetic agent in the auditory system. Our results suggest that the dynamic observed in the auditory system during unconsciousness induced by propofol, can result in a mixture of two effects: a local inhibitory connectivity increase and a decrease in the effective connectivity in sensory cortices.
Posterior Cingulate Cortex-Related Co-Activation Patterns: A Resting State fMRI Study in Propofol-Induced Loss of Consciousness
Enrico Amico, Francisco Gomez, Carol Di Perri, Audrey Vanhaudenhuyse, Damien Lesenfants, Pierre Boveroux, Vincent Bonhomme, Jean-Fran?ois Brichant, Daniele Marinazzo, Steven Laureys
PLOS ONE , 2014, DOI: 10.1371/journal.pone.0100012
Abstract: Background Recent studies have been shown that functional connectivity of cerebral areas is not a static phenomenon, but exhibits spontaneous fluctuations over time. There is evidence that fluctuating connectivity is an intrinsic phenomenon of brain dynamics that persists during anesthesia. Lately, point process analysis applied on functional data has revealed that much of the information regarding brain connectivity is contained in a fraction of critical time points of a resting state dataset. In the present study we want to extend this methodology for the investigation of resting state fMRI spatial pattern changes during propofol-induced modulation of consciousness, with the aim of extracting new insights on brain networks consciousness-dependent fluctuations. Methods Resting-state fMRI volumes on 18 healthy subjects were acquired in four clinical states during propofol injection: wakefulness, sedation, unconsciousness, and recovery. The dataset was reduced to a spatio-temporal point process by selecting time points in the Posterior Cingulate Cortex (PCC) at which the signal is higher than a given threshold (i.e., BOLD intensity above 1 standard deviation). Spatial clustering on the PCC time frames extracted was then performed (number of clusters = 8), to obtain 8 different PCC co-activation patterns (CAPs) for each level of consciousness. Results The current analysis shows that the core of the PCC-CAPs throughout consciousness modulation seems to be preserved. Nonetheless, this methodology enables to differentiate region-specific propofol-induced reductions in PCC-CAPs, some of them already present in the functional connectivity literature (e.g., disconnections of the prefrontal cortex, thalamus, auditory cortex), some others new (e.g., reduced co-activation in motor cortex and visual area). Conclusion In conclusion, our results indicate that the employed methodology can help in improving and refining the characterization of local functional changes in the brain associated to propofol-induced modulation of consciousness.
Cerebral functional connectivity periodically (de)synchronizes with anatomical constraints
Rapha?l Liégeois,Erik Ziegler,Pierre Geurts,Francisco Gomez,Mohamed Ali Bahri,Christophe Phillips,Andrea Soddu,Audrey Vanhaudenhuyse,Steven Laureys,Rodolphe Sepulchre
Quantitative Biology , 2014,
Abstract: This paper studies the link between resting-state functional connectivity (FC), measured by the correlations of the fMRI BOLD time courses, and structural connectivity (SC), estimated through fiber tractography. Instead of a static analysis based on the correlation between SC and the FC averaged over the entire fMRI time series, we propose a dynamic analysis, based on the time evolution of the correlation between SC and a suitably windowed FC. Assessing the statistical significance of the time series against random phase permutations, our data show a pronounced peak of significance for time window widths around 20-30 TR (40-60 sec). Using the appropriate window width, we show that FC patterns oscillate between phases of high modularity, primarily shaped by anatomy, and phases of low modularity, primarily shaped by inter-network connectivity. Building upon recent results in dynamic FC, this emphasizes the potential role of SC as a transitory architecture between different highly connected resting state FC patterns. Finally, we show that networks implied in consciousness-related processes, such as the default mode network (DMN), contribute more to these brain-level fluctuations compared to other networks, such as the motor or somatosensory networks. This suggests that the fluctuations between FC and SC are capturing mind-wandering effects.
Reduction in Inter-Hemispheric Connectivity in Disorders of Consciousness
Smadar Ovadia-Caro, Yuval Nir, Andrea Soddu, Michal Ramot, Guido Hesselmann, Audrey Vanhaudenhuyse, Ilan Dinstein, Jean-Flory L. Tshibanda, Melanie Boly, Michal Harel, Steven Laureys, Rafael Malach
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0037238
Abstract: Clinical diagnosis of disorders of consciousness (DOC) caused by brain injury poses great challenges since patients are often behaviorally unresponsive. A promising new approach towards objective DOC diagnosis may be offered by the analysis of ultra-slow (<0.1 Hz) spontaneous brain activity fluctuations measured with functional magnetic resonance imaging (fMRI) during the resting-state. Previous work has shown reduced functional connectivity within the “default network”, a subset of regions known to be deactivated during engaging tasks, which correlated with the degree of consciousness impairment. However, it remains unclear whether the breakdown of connectivity is restricted to the “default network”, and to what degree changes in functional connectivity can be observed at the single subject level. Here, we analyzed resting-state inter-hemispheric connectivity in three homotopic regions of interest, which could reliably be identified based on distinct anatomical landmarks, and were part of the “Extrinsic” (externally oriented, task positive) network (pre- and postcentral gyrus, and intraparietal sulcus). Resting-state fMRI data were acquired for a group of 11 healthy subjects and 8 DOC patients. At the group level, our results indicate decreased inter-hemispheric functional connectivity in subjects with impaired awareness as compared to subjects with intact awareness. Individual connectivity scores significantly correlated with the degree of consciousness. Furthermore, a single-case statistic indicated a significant deviation from the healthy sample in 5/8 patients. Importantly, of the three patients whose connectivity indices were comparable to the healthy sample, one was diagnosed as locked-in. Taken together, our results further highlight the clinical potential of resting-state connectivity analysis and might guide the way towards a connectivity measure complementing existing DOC diagnosis.
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