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Photic stimulation of rods, cones and intrinsically photosensitive melanopsin-containing retinal ganglion cells (ipRGCs) mediates non-visual light responses, including entrainment of circadian rhythms and pupillary light reflex. Unlike visual responses to photic stimulation, the cerebral correlates of non-visual light responses in humans remains elusive. In this study, we used functional magnetic resonance imaging (fMRI) in 14 healthy young participants, to localize cerebral regions which are differentially activated by metameric light that gave rise to different levels of melanopic excitation. Mean blood oxygen-level dependent (BOLD) responses disclosed bilateral activation of the frontal eye fields during exposure to light geared towards melanopsin. Furthermore, multivariate pattern analyses showed distinct bilateral pattern activity in the inferior temporal gyri and the caudate nuclei. Taken together, our findings suggest that melanopsin-based photoreception activates a cerebral network including frontal regions, classically involved in attention and ocular motor responses.
Photoparoxysmal response (PPR) is an electroencephalographic (EEG) trait characterized by the occurrence of epileptiform discharges in response to visual stimulation. Studying this trait helps to learn about mechanisms of epileptogenicity. While simultaneous recordings of EEG and functional MRI (EEG-fMRI) in patients with spontaneous generalised spike-wave discharges (GSW) have revealed activation of the thalamus and deactivation in frontoparietal areas, EEG-fMRI studies on evoked GSW such as PPR are lacking. In this EEG-fMRI study, 30 subjects with reported generalised PPR underwent intermittent photic stimulation (IPS) in a 3 T MR scanner. PPR was elicited in 6 subjects, four diagnosed with idiopathic generalised epilepsy and two with tension-type headache. Because PPR is preceded by synchronization of cortical gamma oscillations, blood oxygenation level-dependent (BOLD) signal changes were analysed at the onset of the PPR (standard regressor) and 3 s before the onset of PPR (early regressor) in one model. In all subjects, IPS led to a significant activation of the visual cortex. Based on the early regressor, PPR associated activation was found in the parietal cortex adjacent to the intraparietal sulcus in five and in the premotor cortex in all 6 subjects. The standard regressor revealed deactivation in early activated areas in all subjects and thalamic activation in one subject. In contrast to spontaneous GSW, these results suggest that PPR is a cortical phenomenon with an involvement of the parietal and frontal cortices. Pronounced haemodynamic changes seen with the early regressor could mirror gamma activity that is known to precede PPR.
Current therapies for depression consist primarily of pharmacological agents, including antidepressants, and/or psychiatric counseling, such as psychotherapy. However, light therapy has recently begun to be considered as an effective tool for the treatment of the neuropsychiatric behaviors and symptoms of a variety of brain disorders or diseases, including depression. One methodology employed in light therapy involves flickering photic stimulation within a specific frequency range. The present study investigated whether flickering and flashing photic stimulation with light emitting diodes (LEDs) could improve depression-like behaviors in a corticosterone (CORT)-induced mouse model of depression. Additionally, the effects of the flickering and flashing lights on depressive behavior were compared with those of fluoxetine. Rhythmical flickering photic stimulation at alpha frequencies from 9-11 Hz clearly improved performance on behavioral tasks assessing anxiety, locomotor activity, social interaction, and despair. In contrast, fluoxetine treatment did not strongly improve behavioral performance during the same period compared with flickering photic stimulation. The present findings demonstrated that LED-derived flickering photic stimulation more rapidly improved behavioral outcomes in a CORT-induced mouse model of depression compared with fluoxetine. Thus, the present study suggests that rhythmical photic stimulation at alpha frequencies may aid in the improvement of the quality of life of patients with depression.
Electroencephalography (EEG) as a biomarker of neuromodulation by High Definition transcranial Direct Current Stimulation (HD-tDCS) offers promise as both techniques are deployable and can be integrated into a single head-gear. The present research addresses experimental design for separating focal EEG effect of HD-tDCS in the '4-cathode × 1-anode' (4 × 1) montage over the left motor area (C3). We assessed change in offline EEG at the homologous central (C3, C4), and occipital (O1, O2) locations. Interhemispheric asymmetry was accessed for background EEG at standard frequency bands; and for the intermittent photic stimulation (IPS). EEG was compared post- vs pre-intervention in three HD-tDCS arms: Active (2 mA), Sham (ramp up/down at the start and end), and No-Stimulation (device was not powered), each intervention lasting 20 min. The asymmetric background EEG changes were only in the central areas with right-side amplitude spectra prevalence, most pronounced in the no-stimulation arm, where they depended on comparison time-points and were consistent with markers of transition between drowsiness and vigilance - bilateral decrease in the delta and asymmetric central increase in the alpha and beta1 bands. For the active arm, similar but less pronounced changes occurred in the alpha band. In contrast, responses to IPS developed similar asymmetric amplitude increase at four harmonics of the IPS of 3 Hz only in the active arm, against a background of a brain-wide symmetric increase in both active and sham arms. Our protocols and analyses suggest methodological caveats for how EEG of tDCS studies could be conducted to isolate putative brain polarization outcomes.
Individuals with mild cognitive impairment (MCI) are at high risk of developing Alzheimer's disease (AD). Repetitive photic stimulation (PS) is commonly used in routine electroencephalogram (EEG) examinations for rapid assessment of perceptual functioning. This study aimed to evaluate neural oscillatory responses and nonlinear brain dynamics under the effects of PS in patients with mild AD, moderate AD, severe AD, and MCI, as well as healthy elderly controls (HC). EEG power ratios during PS were estimated as an index of oscillatory responses. Multiscale sample entropy (MSE) was estimated as an index of brain dynamics before, during, and after PS. During PS, EEG harmonic responses were lower and MSE values were higher in the AD subgroups than in HC and MCI groups. PS-induced changes in EEG complexity were less pronounced in the AD subgroups than in HC and MCI groups. Brain dynamics revealed a "transitional change" between MCI and Mild AD. Our findings suggest a deficiency in brain adaptability in AD patients, which hinders their ability to adapt to repetitive perceptual stimulation. This study highlights the importance of combining spectral and nonlinear dynamical analysis when seeking to unravel perceptual functioning and brain adaptability in the various stages of neurodegenerative diseases.
Proton magnetic resonance spectroscopy ((1)H-MRS) has been used in a number of studies to assess noninvasively the temporal changes of lactate (Lac) in the activated human brain. Migraine neurobiology involves lack of cortical habituation to repetitive stimuli and a mitochondrial component has been put forward. Our group has recently demonstrated a reduction in the high-energy phosphates adenosine triphosphate (ATP) and phosphocreatine (PCr) in the occipital lobe of migraine without aura (MwoA) patients, at least in a subgroup, in a phosphorus MRS ((31)P-MRS) study. In previous studies, basal Lac levels or photic stimulation (PS)-induced Lac levels were found to be increased in patients with migraine with aura (MwA) and migraine patients with visual symptoms and paraesthesia, paresia and/or dysphasia, respectively. The aim of this study was to perform functional (1)H-MRS at 3 T in 20 MwoA patients and 20 control subjects. Repetitive visual stimulation was applied using MR-compatible goggles with 8 Hz checkerboard stimulation during 12 min. We did not observe any significant differences in signal integrals, ratios and absolute metabolite concentrations, including Lac, between MwoA patients and controls before PS. Lac also did not increase significantly during and following PS, both for MwoA patients and controls. Subtle Lac changes, smaller than the sensitivity threshold (i.e. estimated at 0.1-0.2 μmol/g at 3 T), cannot be detected by MRS. Our study does, however, argue against a significant switch to non-aerobic glucose metabolism during long-lasting PS of the visual cortex in MwoA patients.
The 5-HT mixed agonist/antagonist 1-(2-methoxyphenyl)4-[4-(phthalimido)butyl]-piperazine hydrobromide (NAN-190) has been shown to greatly potentiate photic phase shifts in hamsters. The mechanism of this potentiation has yet to be determined. NAN-190 is believed to act primarily through the 5-HT(1A) receptor, but also binds to several other receptors, making it uncertain as to which receptor underlies its potentiation of photic phase shifts. Also uncertain are the intracellular changes in the suprachiasmatic nucleus (SCN) which are associated with such enhanced phase shifting. Here we examine the role of the 5-HT(1A) receptor as well as the physiological underpinnings, in terms of both gene expression and biochemical activation, in the behavioral responses to photic stimuli following pretreatment with NAN-190. Administration of NAN-190 to wildtype mice significantly potentiated late subjective night photic phase shifts, while mice lacking the 5-HT(1A) receptor (knockouts) exhibited an attenuated behavioral response to light when pretreated with NAN-190. In wildtype mice, the protein product of the immediate-early gene c-fos, induced following photic stimulation, was found to be significantly decreased with NAN-190 pretreatment. Similarly, the levels of phosphorylated CREB protein, involved in a biochemical pathway leading to gene transcription, were also attenuated by NAN-190 in the wildtype mice. However, activation of the extracellular signal-regulated kinase I/II (ERK) pathway in wildtype mice, following the light pulse, was not affected by NAN-190 pretreatment, nor was the expression of the circadian clock components Period1 and Period2. These findings suggest that the 5-HT(1A) receptor plays a critical role in the potentiation effect observed with NAN-190, and that NAN-190 may potentiate photic phase shifts at least partly by down-regulating the activity of some (but not all) genes and biochemical pathways involved in coupling the light signal to the output of the circadian clock.
Transcranial focused ultrasound (FUS) is making progress as a new non-invasive mode of regional brain stimulation. Current evidence of FUS-mediated neurostimulation for humans has been limited to the observation of subjective sensory manifestations and electrophysiological responses, thus warranting the identification of stimulated brain regions. Here, we report FUS sonication of the primary visual cortex (V1) in humans, resulting in elicited activation not only from the sonicated brain area, but also from the network of regions involved in visual and higher-order cognitive processes (as revealed by simultaneous acquisition of blood-oxygenation-level-dependent functional magnetic resonance imaging). Accompanying phosphene perception was also reported. The electroencephalo graphic (EEG) responses showed distinct peaks associated with the stimulation. None of the participants showed any adverse effects from the sonication based on neuroimaging and neurological examinations. Retrospective numerical simulation of the acoustic profile showed the presence of individual variability in terms of the location and intensity of the acoustic focus. With exquisite spatial selectivity and capability for depth penetration, FUS may confer a unique utility in providing non-invasive stimulation of region-specific brain circuits for neuroscientific and therapeutic applications.
Classically, studies adopting non-invasive transcranial electrical stimulation have placed greater importance on the position of the primary "stimulating" electrode than the secondary "reference" electrode. However, recent current density modeling suggests that ascribing a neutral role to the reference electrode may prove an inappropriate oversimplification.
Input from the light/dark (LD) cycle constitutes the primary synchronizing stimulus for the suprachiasmatic nucleus (SCN) circadian clock. However, the SCN can also be synchronized by non-photic inputs. Here, we hypothesized that the vestibular system, which detects head motion and orientation relative to gravity, may provide sensory inputs to synchronize circadian rhythmicity. We investigated the resynchronization of core temperature (Tc) circadian rhythm to a six-hour phase advance of the LD cycle (LD + 6) using hypergravity (2 G) as a vestibular stimulation in control and bilateral vestibular loss (BVL) rats. Three conditions were tested: an LD + 6 exposure alone, a series of seven 2 G pulses without LD + 6, and a series of seven one-hour 2 G pulses (once a day) following LD + 6. First, following LD + 6, sham rats exposed to 2 G pulses resynchronized earlier than BVL rats (p = 0.01), and earlier than sham rats exposed to LD + 6 alone (p = 0.002). Each 2 G pulse caused an acute drop of Tc in sham rats (-2.8 ± 0.3 °C; p < 0.001), while BVL rats remained unaffected. This confirms that the vestibular system influences chronobiological regulation and supports the hypothesis that vestibular input, like physical activity, should be considered as a potent time cue for biological rhythm synchronization, acting in synergy with the visual system.
Despite negative blood oxygenation level dependent (BOLD) responses to visual stimuli have recently gained considerable interest, the explanation for their underlying neuronal and vascular mechanisms is still controversial. In the present study, a multimodal experimental approach is presented to shed light on the negative BOLD phenomenon in the human brain. In particular, information from functional magnetic resonance imaging (fMRI) and near infrared spectroscopy (NIRS) was integrated to confirm and gain insight into the phenomenon of negative BOLD responses (NBRs) to unpatterned intermittent photic stimulation (IPS) in healthy subjects. Eight healthy subjects participated in the study. Consistent findings emerged from the activation analysis of fMRI and NIRS data and the comparison of BOLD and hemoglobin responses at the single channel level showed that NBRs are related to a decrease in oxyhemoglobin (HbO) combined with a lower increase in deoxyhemoglobin (HHb), corresponding to a decrease in total hemoglobin (THb) and estimated cerebral blood volume (CBV). The HbO and HHb variations were significant in at least one channel in six subjects out of eight (p<0.05). The NIRS technique allowed obtaining valuable information on the vascular determinants of the NBRs, since the discrimination between HbO, HHb and THb information provided a more comprehensive view of the negative BOLD phenomenon. The within and between subject heterogeneous BOLD-Hb temporal relations pave the way to further investigations into the neurovascular properties of NBRs.
The CB1 cannabinoid receptors have been found in the rodent suprachiasmatic nucleus, and their activation suppresses the light-induced phase shift in locomotor rhythmicity of mice and hamsters. Here, we show that the CB1 receptor agonist CP55940 significantly attenuates the light-induced phase delay in rats as well. Furthermore, it blocks the light induction of c-Fos and light-induced downregulation of pERK1/2 in the SCN, and the CB1 antagonist AM251 prevents the photic induction of pERK1/2 and reduces pGSK3β after photic stimulation. Our data suggest that the modulation of the cannabinoid receptor activity may affect the photic entrainment via the setting of the SCN sensitivity to light.
The circadian clock, located in the suprachiasmatic nucleus (SCN), receives a major afferent from the median raphe nucleus (MRN). In the Syrian hamster, only about 50% of the cells giving rise to this afferent contain serotonin. There is mixed evidence as to whether the serotonergic portion of this projection is involved in non-photic phase shifting of circadian locomotor rhythms. In order to better characterize the non-serotonergic projections, we conducted retrograde tract tracing using the beta subunit of cholera toxin combined with multi-label immunohistochemistry. Similar to previous findings, almost half of the retrogradely labeled cells contained serotonin. Additionally, approximately 30% of the retrogradely labeled cells contained vesicular glutamate transporter 3 (VGLUT3), but not serotonin. Surprisingly, some dorsal raphe cholera toxin labeling was also noted, particularly in animals with central-SCN injections. To determine if the non-serotonergic projections were important for non-photic phase shifts elicited by MRN stimulation, the MRN was electrically stimulated in animals pretreated with SCN injection of either the serotonin neurotoxin 5,7-dihydroxytryptamine or vehicle control. Intact animals phase advanced to midday electrical stimulation of the raphe while lesioned animals did not. Together, these results show that although some of the non-serotonergic raphe projections to the SCN contain VGLUT3, it is the serotonergic raphe innervation of the SCN that is critical for non-photic phase shifting elicited by MRN stimulation.
Human photosensitive epilepsy models have been used as proof of principle (POP) trials for epilepsy. Photosensitive patients are exposed to intermittent photic stimulation and the reduction in sensitivity to the number of standard visual stimulation frequencies is used as an endpoint. The aim of this research was to quantify the predictive capabilities of photosensitive POP trials, through a survey of current literature.
Although the suprachiasmatic nuclei (SCN) have been intensively analyzed, they contain a population of cells that has not yet been characterized. In this study, we examined the distribution of cells immunoreactive (ir) for calbindin-D28K (CaBP), calretinin (CR), parvalbumin, vasopressin-associated neurophysin (NP), substance P (SP), vasoactive intestinal peptide (VIP), and light-induced Fos-like protein. Previously unidentified cells in the core of the hamster SCN contained CaBP. Photic stimulation during the night induced Fos expression in about 75% of the CaBP-positive SCN cells, and about 50% of the Fos-positive cells in the core region expressed CaBP. These findings provide new information in the search for the cellular localization of pacemaker cells in the SCN, as photic input entrains the circadian system, and cells that receive photic input must be either part of the clock itself, or an upstream component of the clock.
Juvenile myoclonic epilepsy (JME) is typified by the occurrence of myoclonic seizures after awakening, though another common trait is myoclonic seizures triggered by photic stimulation. We aimed to investigate the functional connectivity (FC) of nuclei in the ascending reticular activating system (ARAS), thalamus and visual cortex in JME with and without photosensitivity.
Over the past decades, numerous studies have linked cortical gamma oscillations (∼30-100 Hz) to neurocomputational mechanisms. Their functional relevance, however, is still passionately debated. Here, we asked whether endogenous gamma oscillations in the human brain can be entrained by a rhythmic photic drive >50 Hz. Such a noninvasive modulation of endogenous brain rhythms would allow conclusions about their causal involvement in neurocognition. To this end, we systematically investigated oscillatory responses to a rapid sinusoidal flicker in the absence and presence of endogenous gamma oscillations using magnetoencephalography (MEG) in combination with a high-frequency projector. The photic drive produced a robust response over visual cortex to stimulation frequencies of up to 80 Hz. Strong, endogenous gamma oscillations were induced using moving grating stimuli as repeatedly done in previous research. When superimposing the flicker and the gratings, there was no evidence for phase or frequency entrainment of the endogenous gamma oscillations by the photic drive. Unexpectedly, we did not observe an amplification of the flicker response around participants' individual gamma frequencies (IGFs); rather, the magnitude of the response decreased monotonically with increasing frequency. Source reconstruction suggests that the flicker response and the gamma oscillations were produced by separate, coexistent generators in visual cortex. The presented findings challenge the notion that cortical gamma oscillations can be entrained by rhythmic visual stimulation. Instead, the mechanism generating endogenous gamma oscillations seems to be resilient to external perturbation.SIGNIFICANCE STATEMENT We aimed to investigate to what extent ongoing, high-frequency oscillations in the gamma-band (30-100 Hz) in the human brain can be entrained by a visual flicker. Gamma oscillations have long been suggested to coordinate neuronal firing and enable interregional communication. Our results demonstrate that rhythmic visual stimulation cannot hijack the dynamics of ongoing gamma oscillations; rather, the flicker response and the endogenous gamma oscillations coexist in different visual areas. Therefore, while a visual flicker evokes a strong neuronal response even at high frequencies in the gamma-band, it does not entrain endogenous gamma oscillations in visual cortex. This has important implications for interpreting studies investigating the causal and neuroprotective effects of rhythmic sensory stimulation in the gamma-band.
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