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Swallowing monitoring Intracranial electroencephalogram (EEG) was recorded during participants’ swallowing. The swallowing was monitored by an RGB camera of Kinect v2 (Microsoft), an electroglottograph (EGG), and the microphone of a laryngograph (A). Across-trials averaged impedance waveforms of an EGG (B) and a throat microphone (sound) (C) from Participant 1 (P1) are shown. For analysis, the onset of swallowing was defined as the peak time of an impedance waveform. We could detect when participants opened their mouths and when water bolus was injected into the mouth by the RGB camera of Kinect v2.
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Swallowing is attributed to the orchestration of motor-output and sensory-input. We hypothesized that swallowing can illustrate differences between motor and sensory neural processing. Eight epileptic participants fitted with intracranial electrodes over the orofacial cortex were asked to swallow a water bolus. Mouth-opening and swallowing were tre...
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Citations
... Similarly, the beta band exhibited a significant effect, suggesting a distinct impact of the Erigo device on this frequency range. The heightened beta power post-intervention could be indicative of increased alertness or engagement, corroborating the notion that motor stimulation contributes to changes in cortical excitability and arousal level [34]. These findings support the hypothesis that the Erigo device, with its motor rehabilitation and sensory stimulation capabilities, contributes to distinct alterations in brainwave patterns associated with neural plasticity. ...
... It was an authors' opinion that LCF is less sensible to detect changes in comatose patients. The literature on hemispheric specificity in response to motor interventions varies, with some studies emphasizing lateralized effects and others highlighting non-lateralized changes in brain activity [9,10,34]. This stability might suggest that the device's effects are more prominent in higher-frequency oscillations, reflecting specific cognitive processes related to attention and alertness, rather than broader changes in neural synchronization. ...
In disorders of consciousness, verticalization is considered an effective type of treatment to improve motor and cognitive recovery. Our purpose is to investigate neurophysiological effects of robotic verticalization training (RVT) in patients with minimally conscious state (MCS). Thirty subjects affected by MCS due to traumatic or vascular brain injury, attending the intensive Neurorehabilitation Unit of the IRCCS Neurolesi (Messina, Italy), were included in this retrospective study. They were equally divided into two groups: the control group (CG) received traditional verticalization with a static bed and the experimental group (EG) received advanced robotic verticalization using the Erigo device. Each patient was evaluated using both clinical scales, including Levels of Cognitive Functioning (LCF) and Functional Independence Measure (FIM), and quantitative EEG pre (T0) and post each treatment (T1). The treatment lasted for eight consecutive weeks, and sessions were held three times a week, in addition to standard neurorehabilitation. In addition to a notable improvement in clinical parameters, such as functional (FIM) (p < 0.01) and cognitive (LCF) (p < 0.01) outcomes, our findings showed a significant modification in alpha and beta bands post-intervention, underscoring the promising effect of the Erigo device to influence neural plasticity and indicating a noteworthy difference between pre-post intervention. This was not observed in the CG. The observed changes in alpha and beta bands underscore the potential of the Erigo device to induce neural plasticity. The device’s custom features and programming, tailored to individual patient needs, may contribute to its unique impact on brain responses.
... MEG captures the magnetic fields generated by synchronized neuronal currents [32]. ECoG detects the cortical potential generated by neural oscillatory activities and has disclosed the role of the cerebral cortex in both the motor and sensory components of voluntary swallowing [41,42]. TMS enables direct activation of cortical neurons and was used to investigate the integrity of the corticospinal and corticobulbar tracts [43]. ...
Swallowing is a sophisticated process involving the precise and timely coordination of the central and peripheral nervous systems, along with the musculatures of the oral cavity, pharynx, and airway. The role of the infratentorial neural structure, including the swallowing central pattern generator and cranial nerve nuclei, has been described in greater detail compared with both the cortical and subcortical neural structures. Nonetheless, accumulated data from analysis of swallowing performance in patients with different neurological diseases and conditions, along with results from neurophysiological studies of normal swallowing have gradually enhanced understanding of the role of cortical and subcortical neural structures in swallowing, potentially leading to the development of treatment modalities for patients suffering from dysphagia. This review article summarizes findings about the role of both cortical and subcortical neural structures in swallowing based on results from neurophysiological studies and studies of various neurological diseases. In sum, cortical regions are mainly in charge of initiation and coordination of swallowing after receiving afferent information, while subcortical structures including basal ganglia and thalamus are responsible for movement control and regulation during swallowing through the cortico-basal ganglia-thalamo-cortical loop. This article also presents how cortical and subcortical neural structures interact with each other to generate the swallowing response. In addition, we provided the updated evidence about the clinical applications and efficacy of neuromodulation techniques, including both non-invasive brain stimulation and deep brain stimulation on dysphagia.
... The symptoms of anxiety and depression in the case group were more severe than the control group ( According to the Bucco-Facial-Apraxia assessment, we found most of WD patients with dystonia were unable to perform some functional movements such as pursing or puckering of the lips. Lateral precentral gyrus and prefrontal cortex are associating with orofacial motor action (Hashimoto et al., 2021;Loh et al., 2020). Damage of the premotor cortex, parietal association cortex or supplementary motor cortex may produce higher-order deficits and apraxia (Attallah et al., 2020). ...
Objective
To study the clinical features and power spectral entropy (PSE) of electroencephalography signals in Wilson's disease (WD) patients with dystonia.
Methods
Several scale evaluations were performed to assess the clinical features of WD patients. Demographic information and electroencephalography signals were obtained in all subjects.
Results
34 WD patients with dystonia were recruited in the case group and 24 patients without dystonia were recruited in the control group. 20 healthy individuals were included in the healthy control group. The mean body mass index (BMI) in the case group was significantly lower than that in the controls (p < .05). The case group had significantly higher SAS, SDS, and Bucco‐Facial‐Apraxia Assessment scores (p < .05). Total BADS scores in the case group were lower than those in the control group (p < .01). Note that 94.11% of the case group presented with dysarthria and 70.59% of them suffered from dysphagia. Dysphagia was mainly related to the oral preparatory stage and oral stage. Mean power spectral entropy (PSE) values in the case group were significantly different (p < .05) from those in the control group and the healthy group across the different tasks.
Conclusions
The patients with dystonia were usually accompanied with low BMI, anxiety, depression, apraxia, executive dysfunction, dysarthria and dysphagia. The cortical activities of the WD patients with dystonia seemed to be more chaotic during the eyes‐closed and reading tasks but lower during the swallowing stages than those in the control group.
... It has low spatial (10-20 mm) and temporal (seconds) resolutions, but it is more portable compared to fMRI, allowing flexibility in studying various swallowing protocols [67]. Recently, researchers have explored the use of EEG and ECoG in detecting swallowing-related cortical activations and reported encouraging findings [71][72][73]. EEG measures brain electrical activity through scalp electrodes. Similar to MEG, although EEG has poor spatial resolution, it offers excellent temporal resolution (1-5 milliseconds), making it a suitable candidate for measuring timing-related neural activity [74]. ...
... Other studies have reported a shift in activation sites within the cortex [82,86,92,100] or from predominantly cortical to predominantly subcortical structures [72,145]. Using MEG, Furlong et al., [92] found that activation shifted from caudolateral sensorimotor cortex during swallowing preparation towards more superior sensorimotor cortex during swallowing execution and related tongue movement. ...
... A recent electrocorticogram (ECoG) study by Hashimoto et al., [146] found that high gamma (HG) band activity in the orofacial cortex increased before swallowing and peaked at the junction between voluntary and involuntary stages of swallowing, implying that the driving force of swallowing may have switched from the cerebral cortex to the brainstem during the transition. Furthermore, this group of researchers also investigated the relationship between high-frequency and low-frequency cortical oscillations using phaseamplitude coupling (PAC) methods [72]. They found that during motor tasks (mouth opening and swallowing), HG activities were coupled with alpha band (10-16 Hz) before motor-related HG power increase, whereas for the sensory task (water injection into the mouth), HG activity was coupled with theta band (5-9 Hz) during sensoryrelated HG power increase. ...
This review aims to update the current knowledge on the cerebral control of swallowing. We review data from both animal and human studies spanning across the fields of neuroanatomy, neurophysiology and neuroimaging to evaluate advancements in our understanding in the brain's role in swallowing. Studies have collectively shown that swallowing is mediated by multiple distinct cortical and subcortical regions and that lesions to these regions can result in dysphagia. These regions are functionally connected in separate groups within and between the two hemispheres. While hemispheric dominance for swallowing has been reported in most human studies, the laterality is inconsistent across individuals. Moreover, there is a shift in activation location and laterality between swallowing preparation and execution, although such activation changes are less well-defined than that for limb motor control. Finally, we discussed recent neurostimulation treatments that may be beneficial for dysphagia after brain injury through promoting the reorganization of the swallowing neural network.
... PAC analysis measures the degree of synchronization between phases with low-frequency oscillations and high-frequency amplitudes (Cohen, 2008). PAC can be physiological (Hashimoto et al., 2021d, Yanagisawa et al., 2012 or pathological. Studies related to pathological PAC have demonstrated that ictal HFA amplitude is coupled with d (Nariai et al., 2011) or h (Ibrahim et al., 2014) bands. ...
... The HFA power is strongly correlated with the neural firing rate (Ray et al., 2008), and, in animal studies, neural spiking was found to be locked to the trough of a oscillations (Haegens et al., 2011). In a previous study of physiological PAC, high gamma amplitude during high PAC values peaked around the trough of a oscillations (Hashimoto et al., 2021d, Yanagisawa et al., 2012. Moreover, in a study of pathological PAC related to epilepsy, the HFA amplitude during high PAC was time-locked to the trough of lower-frequency oscillations (Ibrahim et al., 2014). ...
... PAC has been observed in both physiological and pathological neural processing. The former includes hand movement (Yanagisawa et al., 2012), swallowing (Hashimoto et al., 2021d) and somatosensory processing (Lakatos et al., 2008), and the latter includes epileptic seizures (Hashimoto et al., 2020, 2021c, Iimura et al., 2018, and Parkinson's disease (de Hemptinne et al., 2015). It was reported that ictal HFA amplitudes are coupled with d (Iimura et al., 2018, Nariai et al., 2011), h (Hashimoto et al., 2021c, Ibrahim et al., 2014, and a (Ibrahim et al., 2014) phases, while b-HFA coupling has been reported as a useful marker for seizure detection (Edakawa et al., 2016). ...
Objective
To clarify variations in the relationship between high-frequency activities (HFAs) and low–frequency bands from the tonic to the clonic phase in focal to bilateral tonic-clonic seizures (FBTCS), using phase-amplitude coupling.
Methods
This retrospective study enrolled six patients with drug-resistant focal epilepsy who underwent intracranial electrode placement at Osaka University Hospital (July 2018–July 2019). We recorded 11 FBTCS. The synchronization index (SI) and receiver–operating characteristic (ROC) analysis were used to analyze the coupling between HFA amplitude (80–250 Hz) and lower frequencies phase.
Results
In the tonic phase, the θ (4–8 Hz)-HFA coupling peaked, and the HFA power occurred at baseline (0 μV) of θ oscillations. In contrast, in the clonic phase, the δ (2–4 Hz)-HFA coupling peaked, and the HFA power occurred at the trough of δ oscillations. ROC analysis indicated that the δ-HFA SI discriminated well the clonic from the tonic phase.
Conclusions
The main low-frequency band modulating the HFA shifted from the θ band in the tonic phase to the δ band in the clonic phase.
Significance
Neurophysiological key frequency bands were implied to be the θ band and δ band in tonic and clonic seizures, respectively, which improves our understanding of FBTCS.
... PAC analysis measures the degree of synchronization between phases with low-frequency oscillations and high-frequency amplitudes (Cohen, 2008). PAC can be physiological (Hashimoto et al., 2021c, Yanagisawa et al., 2012 or pathological. Studies related to pathological PAC have demonstrated that ictal HFA amplitude is coupled with δ (Nariai et al., 2011) or θ (Ibrahim et al., 2014) bands. ...
... PAC has been observed in both physiological and pathological neural processing. The former includes hand movement (Yanagisawa et al., 2012), swallowing (Hashimoto et al., 2021c) and somatosensory processing (Lakatos et al., 2008), . CC-BY-NC-ND 4.0 International license made available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. ...
... The HFA power is strongly correlated with the neural firing rate (Ray et al., 2008), and, in animal studies, neural spiking was found to be locked to the trough of α oscillations (Haegens et al., 2011). In a previous study of physiological PAC, high gamma amplitude during high PAC values peaked around the trough of α oscillations (Hashimoto et al., 2021c, Yanagisawa et al., 2012. Moreover, in a study of pathological PAC related to epilepsy, the HFA amplitude during high PAC was time-locked to the trough of lower-frequency oscillations (Ibrahim et al., 2014). ...
Objective
To clarify variations in the relationship between high-frequency activities (HFAs) and low-frequency bands from the tonic to the clonic phase in focal to bilateral tonic-clonic seizures (FBTCS), using phase-amplitude coupling.
Methods
This retrospective study enrolled six patients with drug-resistant focal epilepsy who underwent intracranial electrode placement for presurgical invasive electroencephalography at Osaka University Hospital (July 2018–July 2019). We used intracranial electrodes to record seizures in focal epilepsy (11 FBTCS). The magnitude of synchronization index (SIm) and receiver-operating characteristic (ROC) analysis were used to analyze the coupling between HFA amplitude (80–250 Hz) and lower frequencies phase.
Results
The θ (4–8 Hz)-HFA SIm peaked in the tonic phase, whereas the δ (2–4 Hz)-HFA SIm peaked in the clonic phase. ROC analysis indicated that the δ-HFA SIm discriminated well the clonic from the tonic phase.
Conclusions
The main low-frequency band modulating the HFA shifted from the θ band in the tonic phase to the δ band in the clonic phase.
Significance
In FBTCS, low-frequency band coupling with HFA amplitude varies temporally. Especially, the δ band is specific to the clonic phase. These results suggest dynamically neurophysiological changes in the thalamus or basal ganglia throughout FBTCS.
Highlights
The θ band (4–8 Hz) was mainly coupled with high-frequency activity (HFA) in the tonic phase of focal to bilateral tonic-clonic seizures (FBTCS).
The δ band (2–4 Hz) was mainly coupled with HFA in the clonic phase of FBTCS.
The magnitude of the synchronization index related to δ-HFA phase-amplitude coupling discriminated well the clonic from the tonic phase.
... Moreover, coupling θ waves with HFOs has been reported to well discriminate normal brain regions from the seizure onset zone (SOZ) 24 . These pathological PACs are usually accompanied by ictal HFA, whereas physiological PACs that are involved in motor-related HFAs (i.e., high γ band) appear before HFA increases 25,26 . Physiological PAC precedes physiological HFA; however, whether a preceding seizure-related PAC can be observed before ictal HFA appears is unknown. ...
... In this study, ISA-HFA PAC increased before the increase in HFA occurred, and this profile that PAC precedes HFA increasing is also reported in previous studies related to motor-related physiological PAC 25,26 . A hold-andrelease model was proposed, which indicated that physiological coupling restricted the HFA and attenuation of the coupling releases the HFA. ...
Infraslow activity (ISA) and high-frequency activity (HFA) are key biomarkers for studying epileptic seizures. We aimed to elucidate the relationship between ISA and HFA around seizure onset. We enrolled seven patients with drug-resistant focal epilepsy who underwent intracranial electrode placement. We comparatively analyzed the ISA, HFA, and ISA-HFA phase-amplitude coupling (PAC) in the seizure onset zone (SOZ) or non-SOZ (nSOZ) in the interictal, preictal, and ictal states. We recorded 15 seizures. HFA and ISA were larger in the ictal states than in the interictal or preictal state. During seizures, the HFA and ISA of the SOZ were larger and occurred earlier than those of nSOZ. In the preictal state, the ISA-HFA PAC of the SOZ was larger than that of the interictal state, and it began increasing at approximately 87 s before the seizure onset. The receiver-operating characteristic curve revealed that the ISA-HFA PAC of the SOZ showed the highest discrimination performance in the preictal and interictal states, with an area under the curve of 0.926. This study demonstrated the novel insight that ISA-HFA PAC increases before the onset of seizures. Our findings indicate that ISA-HFA PAC could be a useful biomarker for discriminating between the preictal and interictal states.
... Moreover, studies using PET and fMRI showed that swallowing recruits multiple cerebral regions, predominantly in sensorimotor areas of the brain [28,29]. Most recently, Hashimoto et al. demonstrated for the first time the brain oscillation changes between voluntary and involuntary swallowing with electrocorticogram (ECoG) [30]. They found that the swallowing driving force switched from the cortex to brain stem at the transition from oral to pharyngeal phase of swallowing, providing evidence of the dynamics within the neural network of swallowing. ...
Dysphagia is a common and devastating complication following brain damage. Over the last 2 decades, dysphagia treatments have shifted from compensatory to rehabilitative strategies that facilitate neuroplasticity, which is the reorganization of neural networks that is essential for functional recovery. Moreover, there is growing interest in the application of cortical and peripheral neurostimulation to promote such neuroplasticity. Despite some preliminary positive findings, the variability in responsiveness toward these treatments remains substantial. The purpose of this review is to summarize findings on the effects of neurostimulation in promoting neuroplasticity for dysphagia rehabilitation and highlight the need to develop more effective treatment strategies. We then discuss the role of metaplasticity, a homeostatic mechanism of the brain to regulate plasticity changes, in helping to drive neurorehabilitation. Finally, a hypothesis on how metaplasticity could be applied in dysphagia rehabilitation to enhance treatment outcomes is proposed.
... Ictal HFA amplitudes coupled with δ 17,18 , θ 19,20 , and α 19 phases, and β-HFA coupling are useful markers for seizure detection 21 . These pathological PACs are usually accompanied by ictal HFA, whereas physiological PACs that are involved in motor-related HFAs (high γ band) appear before the HFA increases 22,23 . Physiological PAC may induce a delay in physiological HFA; however, it is not known whether a preceding seizure-related PAC can induce a delay in ictal HFA or not. ...
... During the seizure-dependent HFA increase, the PAC using a lower frequency (except for ISA) simultaneously increases 19,20,24 . However, in this study, PAC with ISA increased before the increase in HFA, which was concordant with the profile of physiological PAC 22,23 . Moreover, the PAC before SO was positively correlated with the later HFA; therefore, ISA-HFA PAC might play an essential role in inducing an HFA burst during or just before seizures. ...
IMPORTANCE
This research describes a method to accurately predict the onset of epileptic seizures; this will help treat patients timely, prevent future seizures, and improve outcomes.
OBJECTIVE
We aimed to assess whether the phase-amplitude coupling (PAC) between infraslow activities (ISA) and high-frequency activities (HFA) increases before seizure onset.
DESIGN AND SETTING
This retrospective, single-center case series included patients admitted to the neurosurgery department at Osaka University Hospital in Suita, Osaka, from July 2018 to July 2019.
PARTICIPANTS
We enrolled seven patients with drug-resistant focal epilepsy who underwent intracranial electrode placement as part of a presurgical invasive electroencephalography study.
MAIN OUTCOMES AND MEASURES
We comparatively analyzed the ISA, HFA, and ISA-HFA PAC in the seizure onset zone (SOZ) or non-SOZ (nSOZ) in the interictal, preictal, and ictal states.
RESULTS
We recorded 15 seizures in seven patients [1 female (14%); mean (SD) age = 26 (12) years; age range, 15-47 years]. HFA and ISA were larger in the ictal states than in the interictal and preictal states. During seizures, the HFA and ISA of the SOZ were larger and earlier than those of nSOZ. In the preictal states, the ISA-HFA PAC was larger than that of the interictal states, and it began increasing at 93 seconds before the seizure onset (95% confidence interval: −116 – −71 s). There were no differences in the values and time of ISA-HFA PAC between both zones. Our phase-based analysis revealed differences between the SOZ- and nSOZ-PAC. In SOZ, the HFA amplitudes were tuned at the trough of the ISA oscillations, and in nSOZ, the HFA amplitudes were tuned at the peak of these oscillations. The receiver-operating characteristic curve showed that the ISA-HFA PAC of the SOZ showed the highest discrimination performance in the preictal and interictal states, with an area under the curve (AUC) of 0.926. However, ISA-HFA PAC was not suitable to differentiate between SOZ and nSOZ (interictal AUC = 0.555, preictal AUC = 0.691, and ictal AUC = 0.646).
CONCLUSION AND RELEVANCE
This study demonstrated the novel insight that ISA-HFA PAC increases before the onset of seizures, regardless of the seizure onset zone. Our findings indicate that ISA-HFA PAC is a potential biomarker for predicting the onset of seizures and may be valuable to physicians who routinely treat epileptic patients.
Key Points
Question
Is phase-amplitude coupling (PAC) between infraslow activities (ISA) and high-frequency activities (HFA) a useful biomarker for seizure prediction?
Findings
In this case series study on 15 focal-onset seizures in seven epileptic patients who underwent intracranial electrode placement, we found that a PAC of the ISA phase and HFA amplitude achieved significantly higher values in preictal states than in the interictal states, and ISA-HFA PAC of the seizure onset zone (SOZ) began increasing at 93 seconds before seizure onset (SO), while both HFA and ISA increased after SO. The receiver-operating characteristic curve showed that the ISA-HFA PAC of the SOZ showed the highest discrimination performance in the preictal and interictal states, with an area under the curve of 0.926.
Meaning
This study demonstrates that ISA-HFA PAC can differentiate between the preictal and interictal states of a seizure, indicating that it is a potential marker for seizure prediction.
Neurotechnology refers to the use of devices and techniques to sense the brain activity and stimulate the brain. Techniques for brain sensing include non-invasive techniques such as electroencephalography (EEG), functional Magnetic Resonance Imaging (fMRI), functional Near-Infrared Spectroscopy (fNIRS), Magnetoencephalography (MEG), and Positron Emission Tomography (PET), and invasive techniques involving direct implantation of devices in the brain. Techniques for brain stimulation include neurofeedback from brain activity sensed from EEG, fMRI, or fNIRS to reinforce brain functions, Transcranial Magnetic Stimulation, Deep Brain Stimulation (DBS), and Vagus Nerve Stimulation.
A brain machine interface (BMI) is a device that translates neuronal information into commands capable of controlling a computer or robotic arm. BMI has advanced remarkably, with the development of such products as power-assisted robot suits for limb-paralyzed patients, devices for DBS for Parkinson’s disease, and cochlear implants for hearing-impaired patients.
In the field of otorhinolaryngology, sensory organs transmit auditory, equilibrium, olfactory, and gustatory information to the brain, whereas motor organs responsible for phonation, articulation and swallowing, receive direct commands from the brain through the cranial nerves. Application of neurotechnology to these organs could lead to breakthrough medicine with a promising future in the field of otorhinolaryngology.
