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Official websites use. Share sensitive information only on official, secure websites. Correspondence , Jennifer K. Email: steeves yorku. Visual cortical excitability, measured using phosphene thresholds, remained unchanged following both cTBS and iTBS conditions. These findings demonstrate that a single session of TBS to the visual cortex can be used without significant effects on the tonic levels of these key neurotransmitters; and add to our understanding that TBS has differential effects at visual, motor, and frontal cortices. Results demonstrate that TBS produces differential effects at the visual cortex compared to aftereffects that have been measured at motor and frontal cortices. These findings have key implications for clinical use, and for investigative vision research when making inferences on causality. Even when the rTMS effect appears specific, doubling the duration of stimulation can reverse the outcome from inhibition to excitation and vice versa Gamboa et al. This would have significant implications for both experimental and clinical use. Accordingly, the use of rTMS to modulate disorders has focused on these cortical regions, for example, stroke for reviews, see Dionisio et al. Although rTMS has been used frequently in exploratory vision research e. However, underlying neurophysiological effects of NIBS differ fundamentally across cortical and subcortical regions Castrillon et al. Clinically, TMS has great potential as a valuable therapeutic tool in several visual and ophthalmological disorders Mahayana et al. Previously, we have successfully reduced visual hallucinations that occurred as a consequence of occipital stroke using rTMS to the visual cortex Rafique et al. Both rTMS and TBS protocols to the occipital cortex have significantly improved visual acuity, stereoacuity, and contrast sensitivity measures in amblyopia Clavagnier et al. Although there is a lack of data investigating changes in metabolites following rTMS, Table 1 highlights variability in findings across studies owing to differences in stimulation parameters and the cortical region being stimulated. However, Allen et al. For TBS to be valuable in investigative research and be implemented successfully in clinical applications through neuroplasticity changes, its effects need to be studied in various brain regions in both healthy and patient populations. Examining the underlying neurophysiological mechanisms associated with TBS will further our understanding of the various protocols and their potential therapeutic benefit. In addition, it will help establish safety profiles for various protocols and populations. No history of cardiovascular or neurological disorders, no head trauma, no medications lowering seizure threshold, no sleep disorders. No history of cardiovascular, neurological, or psychiatric disorders, no head trauma, no current medications, no sleep apnoea. Participants had no known contraindications to TMS and magnetic resonance imaging MRI , no underlying medical conditions, and no history of neurological or psychological disorders Kim et al. Participants were not taking any medications at the time of participation Stell et al. Additionally, participants were asked to attempt a good night's sleep Clow et al. All participants gave informed consent, and the protocol was approved by the Office of Research Ethics at York University in accordance with the Declaration of Helsinki. Participants received monetary compensation. Participants completed different versions at each visit. Participants were instructed to remain still, keep their eyes closed throughout, and refrain from falling asleep. Imaging was performed with the room lights turned off. A single 25 mm 3 cubic voxel was placed medially at the visual cortex V1. The volume of interest VOI was placed as far back in the occipital pole's posterior region as possible and centered on the calcarine sulcus. The VOI position was verified in three planes sagittal, coronal, and transverse for accurate placement, and images in all planes were recorded and used as a reference for subsequent acquisitions for each participant. Figure 1a shows an example of the standard voxel placement in the occipital cortex. Stimulation sites black circle were positioned at the center of the MRS VOI white box for each participant individually. Phosphene threshold PT is a method of measuring visual cortex excitability through the perception of phosphenes. A phosphene is a phenomenon of light that can be produced from direct stimulation of the occipital cortex in the absence of visual stimuli. PTs can be used to determine the individual intensity for TMS administration at the visual cortex in the same way that the motor threshold is used to determine TMS intensity when applied to the motor cortex. PT, therefore, provides an individual excitability threshold for TMS administration since thresholds vary greatly across individuals Stewart et al. In a dimly lit room, wearing a blindfold with eyes closed, participants were instructed to lean forward with their forehead resting on a table while placing no pressure on their eyes. We marked four locations to form a square area to be tested: at the inion, 2 cm above the inion, 2 cm to the left of the inion, and 2 cm above the 2 cm to the left of the inion marker. If no phosphenes were evoked after 10 pulses, the coil was moved to a new position in the marked region. The cTBS protocol consisted of bursts containing three pulses at 50 Hz 20 ms between each stimulus , repeated at 5 Hz intervals i. The iTBS protocol consisted of the same bursts containing three pulses at 50 Hz, repeated at 5 Hz intervals but applied in 2 s trains repeated every 10 s for a total of s, also providing a total of pulses Huang et al. The sham TBS protocols were the same as the active conditions, except it was performed using the sham placebo coil. The sham coil is equipped with a shield that attenuates the magnetic field yet mimics auditory and stimulatory effects. The stimulation site was mapped on each participant's corresponding anatomical image in Brainsight by manually matching the anatomical landmarks to the MRS VOI images obtained at the baseline MRS acquisition. Thus, the neuronavigation system precisely maps individually targeted stimulation sites and accounts for anatomical variability across participants. The coil was held parallel to the midline with the handle pointing downwards and the coil center tangential to the head to minimize coil to cortex distance as the participants sat upright with their chin resting on a chin rest. The study was divided into two visits. MRS baseline measures were acquired upon eligibility at approximately pm, followed by PT at approximately pm. To minimize the potential diurnal variation of neuromodulators, including those involved in TMS mechanisms, the second visit was carried out approximately a week later as close to the baseline time of day as possible. Metabolites are, however, reliably stable for at least several weeks Henry et al. Participants were also asked to report any adverse effects of TBS. Figure 2 shows an overview of the experimental procedure. Diagram of the experimental procedure. Day 1 participants underwent visual and cognitive screening, followed by a baseline MRS scan, and lastly PT. The 3. The amplitude of the peak for each metabolite relates to the total number of molecules and represents the total concentration of that metabolite. GannetSegment then calculated the relative tissue volume fractions from the voxel mask and segmentation results for grey matter GM , white matter WM , and CSF. These corrections account for the effects of tissue composition, tissue water content, and water and metabolite relaxation, as well as the fact that GABA is present in higher concentrations in GM compared to WM at approximately a ratio Edden et al. This resulted in the removal of all time points for one participant as mentioned in Section 2. Statistical analyses were conducted in R statistical software v1. Data were found to violate assumptions of parametric testing. Akaike's information criterion was used to measure the goodness of a fit of an estimated model, and the appropriate covariance structure with the lowest reported criterion was used for statistical analysis. Tissue fractions within the VOI across visits were analyzed as no significant changes would indicate consistent VOI positioning across visits and groups. Box plots show the exclusive interquartile range. Extreme points represent outliers. Following TBS, one participant in the cTBS condition and one participant in the sham condition reported a minor headache, and one participant in the sham group reported craniofacial discomfort near the left eye. These effects are consistent with common and temporary reports following TMS Oberman et al. These preliminary findings suggest that unlike TBS to the motor or frontal cortices, TBS to the visual cortex can be used in investigative or clinical settings without significant implications or alterations to these neurotransmitter levels at the stimulation site. Each TMS paradigm modulates specific neural elements in different layers of the cortex. The cTBS protocol suppresses the amplitude of the I1 wave, suggesting that cTBS has its major effect on the synapse between the inputs responsible for the I1 wave and the pyramidal tract neurons, whereas 1 Hz rTMS produces a selective suppression of late I waves with no change in the I1 wave. This finding may suggest that TBS caused subtle changes in the relationship between the metabolites, one that was not sufficiently large to cause discernible changes between the conditions. Stagg et al. The authors suggest that the tight biochemical relationship between the neurotransmitters may be driven by glutamate since glutamate is a precursor to GABA. The effects of TBS are also in part mediated by glutamatergic mechanisms Huang et al. Since it is still unclear how TBS protocols precisely interact with LTP and LTD mechanisms, if TBS acts on glutamatergic mechanisms, then it may affect the overall homeostatic balance between GABA and glutamate concentrations rather than simply impacting one metabolite over the other. Donahue et al. In the presence of higher GABA concentrations, they suggest that the greater associated vascular and metabolic response occurs presumably to promote an increase in excitatory activity required to overcome the inhibition that may result from higher GABA availability. The lack of causal effects in our study may also be masked by other factors. We observed high interindividual variability across participants in the present study. The current brain state at the time of stimulation, history of synaptic activity, structural asymmetry, neurochemistry, the specific interneuron networks recruited, hormonal levels, circadian rhythms, sex, age, genetics e. Although we attempted to constrain these variables as much as possible in our participant recruitment, there are factors that we could not control for that may have led to null findings, for example, structural differences and genetics. Intraindividual variability is, however, considerably consistent over weeks Hinder et al. One aspect of the contrasting finding could be owed to differences in MRI scanner and acquisition parameters. The most notable disparities include differences in stimulation coil, inclusion criteria, threshold determination, and active versus passive viewing during MRS. We employed much stricter exclusion criteria to control for confounding variables associated with TMS and metabolites to minimize interindividual variability mentioned above that substantially impacts the response to TMS. Allen et al. We used the PT as it offers a more accurate and relevant measure of visual cortical excitability, and quantifies suprathreshold stimulation of target neurons at the visual cortex. The MT is shown to not accurately reflect visual cortical excitability Boroojerdi et al. Further, MTs are markedly lower than PTs, which would result in lower stimulation intensity in the study by Allen and colleagues. Lastly, Allen et al. Task viewing stimulates cortical activity Vanderwal et al. A significant change in PT occurs when presented with high visual demands following cTBS, but no change in PT is observed in a low visual demand condition i. Stochastic resonance, a phenomenon that exists in systems with measurement thresholds, may account for these observed differences Schwarzkopf et al. The phenomenon suggests that information is enhanced by the injection of low levels of noise that in turn lower the response threshold, whereas higher noise levels disrupt performance. Consequently, the choice of threshold, as well as the coil, likely affects any impact on metabolite levels. Such elevated baseline noise in participants with higher PTs could be increased further by TBS as per the stochastic resonance phenomenon and would lead to increased PTs. Particularly with the round coil, the induced noise would be expected to be greater as well as stimulating a greater number of neurons. Additionally, a visual acuity task i. Optimal levels of noise are necessary to push weak subthreshold signals over the threshold, thereby improving information transfer. Continued investigation into the neurophysiological effects of NIBS will allow us to refine the poorly generalized assumption that stimulation interaction with underlying brain activity, structure, and its ability to target specific neuronal pathways is homogenous across the brain. These physiological, functional, and anatomical properties as well as connectivity profiles greatly influence the diverse responses to stimulation depending on the site of stimulation. LTP and LTD in the visual cortex vary depending on the layer in the visual cortex that is stimulated since each layer depends on specific receptor and neurotransmitter activation Daw et al. Identical stimulation protocols induce a differential cascade of effects since not all brain regions respond equally Castrillon et al. It has been suggested that the effects of NIBS are determined by the extent of functional integration of a target region rather than the frequency range of the stimulation protocol Castrillon et al. Franca et al. For example, iTBS effects are strongly related to baseline network connectivity Nettekoven et al. Quite simply, we do not know enough about TMS protocols or how to maximize their associated effects. Prior to developing a clinical intervention protocol or implying causality in investigative research using TMS, mechanistic knowledge about TMS processes and its contribution to changes in brain regions and networks following stimulation needs to be better quantified in healthy populations. Initial work in healthy participants can lead to translational validation studies for therapeutic use in visual disorders such as amblyopia, visual hallucinations, and other visual impairments. Monitoring of symptoms using neurophysiological data longer term is needed to substantiate mechanisms and optimize stimulation parameters. However, Glx is considered primarily driven by the glutamate signal as glutamate is found at much greater concentrations than glutamine in the brain Stagg, As such, it is unlikely that macromolecule contamination affects interpretability. Glutamate concentrations are considered stable for at least 1 month Henry et al. Since TMS focality is not confined to the stimulation site but also regions nearby as well as inducing direct and indirect distal effects on neurophysiological and cognitive behavior, it is essential to measure stimulation effects in distal brain regions. Due to the single voxel limit of MRS, this requires further separate sessions of the highly controlled experimental design with identical stimulation protocols. The present study and our previous rTMS study Rafique et al. The general analogy that TBS produces similar effects to rTMS does not account for the discrepancy in that the number of pulses is usually unequal. Previous studies have demonstrated that doubling the duration of stimulation can produce a contrasting effect Gamboa et al. Future work is required to compare equivalent protocols in terms of pulses between conventional rTMS and TBS at the visual cortex since analogous effects may not be seen when the number of pulses is equal. Accelerated TBS is considered safe and well tolerated in clinical populations Desmyter et al. We demonstrate that cTBS and iTBS protocols at the visual cortex have different effects than those seen at the motor and frontal cortices. Modified protocols of TBS may be needed at the visual cortex to produce substantial changes in LTD and LTP mechanisms, particularly if the tool is to hold value for translation to therapeutic use in patient populations. The authors would like to thank all participants for their contributions. Stoby, K. Continuous and intermittent theta burst stimulation to the visual cortex do not alter GABA and glutamate concentrations measured by magnetic resonance spectroscopy. Brain and Behavior, 12, e As a library, NLM provides access to scientific literature. Brain Behav. Find articles by Karlene S Stoby. Find articles by Sara A Rafique. Georg Oeltzschner 2 Russell H. Find articles by Georg Oeltzschner. Find articles by Jennifer K E Steeves. Open in a new tab. Karlene S. Stoby and Sara A. Rafique should be considered joint first author. Similar articles. Add to Collections. Create a new collection. Add to an existing collection. Choose a collection Unable to load your collection due to an error Please try again. Add Cancel. Bridges et al. Iwabuchi et al. No history of neurological or psychiatric disorders, no head trauma, no current medications No substance dependence. Michael et al. No neurological or psychiatric disorders No history of substance abuse. No neurological or psychiatric disorders Gender, age, and education matched. No history of cardiovascular, neurological, or psychiatric disorders, no head trauma, no current medications, no sleep apnoea No substance abuse.
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