Hemodynamic and Electroencephalographic Responses to Illusory Figures: Recording of the Evoked Potentials during Functional MRI

doi:10.1006/nimg.2001.0948

NeuroImage

Volume 14, Issue 6, December 2001, Pages 1327-1336

https://doi.org/10.1006/nimg.2001.0948 Get rights and content

Abstract

The feasibility of recording event-related potentials (ERP) during functional MRI (fMRI) scanning using higher level cognitive stimuli was studied. Using responses to illusory figures in a visual oddball task, evoked potentials were obtained with their expected configurations and latencies. A rapid stimulation scheme using randomly varied trial lengths was employed, and class-wise characteristics of the hemodynamic response were obtained by a nonlinear analysis of the fMRI time series. Implications and limitations of conducting combined ERP–fMRI experiments using higher level cognitive stimuli are discussed. EEG/fMRI results revealed a sequential activation of striate and extrastriate occipital cortex along the ventral path of object processing for Kanizsa figures. Interestingly, Kanizsa figures activated the human motion area MT. Targets resulted in activations of frontal and parietal cortex which were not activated for standard stimuli.

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The underlying mechanisms of the event-related potential (ERP) generation are still under debate. One popular model considers the ERP as a superposition of phase-resets of ongoing endogenous oscillations of different frequencies. Brain oscillations have been shown to be modulated by transcranial alternating current stimulation (tACS). Thus, it seems feasible, that an ERP could be altered by modulating the contributing oscillations using tACS. One possible approach would be to target a frequency-matched stimulation signal to a specific ERP-component. One possible target for such an approach is the P3, which appears as delta/theta oscillations in the frequency-domain. Thus, an ERP-aligned stimulation in the delta/theta-range might be suitable to force synchronization in the stimulated frequency band and thus increase the amplitude of the P3 component. Building on an existing paradigm, in the present study 21 healthy participants received individualized ERP-aligned delta tACS and control stimulation while performing a visual task. The visual stimulation was matched to the continuous tACS in order to align the tACS peak with the P3 peak. Both the P3 amplitude and the evoked delta power were significantly increased after ERP-aligned tACS but not after control stimulation. The investigated behavioral parameter showed no stimulation dependent effect. Our results may provide new insights into the debate on the contribution of phase-reset mechanisms to the generation of ERPs and offer new opportunities for clinical trials.
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Neuroimaging evidence suggests that areas of the higher-order visual cortex, including the lateral occipital complex (LOC), are engaged in the perception of illusory contours; however, these findings remain unsubstantiated by human lesion data. Therefore, we assessed the presentation time necessary to perceive two types of illusory contours formed by Kanizsa figures or aligned line ends in patients with Parkinson's disease (PD). Additionally, we used ¹⁸F-fluorodeoxyglucose positron emission tomography (FDG-PET) to measure regional cerebral glucose metabolism in PD patients. Although there were no significant differences in the stimulus durations required for perception of illusory contours formed by aligned line ends between PD patients and controls, PD patients required significantly longer stimulus durations for the perception of Kanizsa illusory figures. Difficulty in perceiving Kanizsa illusory figures was correlated with hypometabolism in the higher-order visual cortical areas, including the posterior inferior temporal gyrus. These findings indicate an association between dysfunction in the posterior inferior temporal gyrus, a region corresponding to a portion of the LOC, and impaired perception of Kanizsa illusory figures in PD patients.
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Citation Excerpt :
Thus, potential GA residuals (incompletely removed GA) can have a deleterious effect on PA suppression (Niazy et al., 2005). Interleaved EEG-fMRI acquisitions have been proposed to allow high-quality EEG recording in the intervals without fMRI gradient coil switching (Beldzik et al., 2019; Bonmassar et al., 1999, 2001; Goldman et al., 2000, 2002; Kruggel et al., 2000, 2001; Scheeringa et al., 2011, 2016; Uji et al., 2018). Consequently, the shorter the time required for the spatial encoding of the brain volume in the fMRI time series, the more time for EEG without GA.
Electroencephalography (EEG) concurrently collected with functional magnetic resonance imaging (fMRI) is heavily distorted by the repetitive gradient coil switching during the fMRI acquisition. The performance of the typical template-based gradient artifact suppression method can be suboptimal because the artifact changes over time. Gradient artifact residuals also impede the subsequent suppression of ballistocardiography artifacts.
Here we propose recording continuous EEG with temporally sparse fast fMRI (fast fMRI-EEG) to minimize the EEG artifacts caused by MRI gradient coil switching without significantly compromising the field-of-view and spatiotemporal resolution of fMRI. Using simultaneous multi-slice inverse imaging to achieve whole-brain fMRI with isotropic 5-mm resolution in 0.1 s, and performing these acquisitions once every 2 s, we have 95% of the duty cycle available to record EEG with substantially less gradient artifact. We found that the standard deviation of EEG signals over the entire acquisition period in fast fMRI-EEG was reduced to 54% of that in conventional concurrent echo-planar imaging (EPI) and EEG recordings (EPI-EEG) across participants. When measuring 15-Hz steady-state visual evoked potentials (SSVEPs), the baseline-normalized oscillatory neural response in fast fMRI-EEG was 2.5-fold of that in EPI-EEG. The functional MRI responses associated with the SSVEP delineated by EPI and fast fMRI were similar in the spatial distribution, the elicited waveform, and detection power. Sparsely interleaved fast fMRI-EEG provides high-quality EEG without substantially compromising the quality of fMRI in evoked response measurements, and has the potential utility for applications where the onset of the target stimulus cannot be precisely determined, such as epilepsy.
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To investigate if changes in brain network function and connectivity contribute to the abnormalities in visual event related potentials (ERP) in relapsing-remitting multiple sclerosis (RRMS), and explore their relation to a decrease in cognitive performance.
We evaluated 72 patients with RRMS and 89 healthy control subjects in a cross-sectional study. Visual ERP were generated using illusory and non-illusory stimuli and recorded using 21 EEG scalp electrodes. The measured activity was modelled using Dynamic Causal Modelling. The model network consisted of 4 symmetric nodes including the primary visual cortex (V1/V2) and the Lateral Occipital Complex. Patients and controls were tested with a neuropsychological test battery consisting of 18 cognitive tests covering six cognitive domains.
We found reduced cortical connectivity in bottom-up and interhemispheric connections to the right lateral occipital complex in patients (p < 0.001). Furthermore, interhemispherical connections were related to cognitive dysfunction in several domains (attention, executive function, visual perception and organization, processing speed and global cognition) for patients (p < 0.05). No relation was seen between cortical network connectivity and cognitive function in the healthy control subjects.
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In electrophysiological experiments on visual pattern discrimination, decision difficulty was manipulated either via the physical characteristics of the test stimuli, or by changing the instruction given to the observer. Visual stimuli were rectangular matrices each composed of 100 Gabor patches having different orientations. Matrices differed in the number of Gabor patches with vertical, or horizontal, orientation. The observers’ task was either to discriminate the dominant orientation or to detect collinear elements in the matrix. Relating task difficulty to performance, in the first experimental paradigm (detection of orientation) we obtained the conventional S-like psychometric function but in the second (detection of collinearity) the psychometric function showed a complicated U-curve. Matching between electrophysiological and psychophysical data and image statistical functions allowed us to establish the relative timing of the cortical processes underlying perception and decision making in relation to textural features. In the first 170 ms after stimulus onset coding of the low-level properties of the image takes place. In the time interval 170–400 ms, ERP amplitude correlated only with complex image properties, but not with task difficulty. The first effects arising from decision difficulty were observable at 400 ms after stimulus onset, and therefore this is probably the earliest electrophysiological signature of the decision making processes, in the given experimental paradigm.

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Regular ArticleHemodynamic and Electroencephalographic Responses to Illusory Figures: Recording of the Evoked Potentials during Functional MRI

Abstract

NeuroImage

NeuroImage

NeuroImage

Clin. Neurophysiol.

Clin. Neurophysiol.

Int. J. Psychophysiol.

Brain Res.

NeuroImage

NeuroImage

Visual evoked potential (VEP) measures by simultaneous 64-channel EEG and 3T fMRI

NeuroReport

Detection of transient and distributed cortical activation during averaged single trials of a cognitive task using functional magnetic resonance imaging

Proc. Natl. Acad. Sci. USA

Event-related fMRI and the hemodynamic response

Hum. Brain Mapp.

Randomized event-related experimental designs allow for extremely rapid presentation rates using functional MRI

NeuroReport

EEG during MR imaging: Differentiation of movement artifact from paroxysmal cortical activity

Neurology

FMRI study of face perception and memory using random stimulus sequences

J. Neurophysiol.

Apparent brightness enhancement in the Kanizsa square with and without illusory contour formation

Perception

Assessing the significance of focal activations using their spatial extent

Hum. Brain Mapp.

Movement-related effects in fMRI time series

Magn. Reson. Med.

Sources of attention-sensitive visual event-related potentials

Brain Topogr.

Intersubject variability of functional areas in the human visual cortex

Hum. Brain Mapp.

Combined spatial and temporal imaging of spatial selective attention in humans

Nature

Gestalt perception modulates early visual processing

NeuroReport

Regular Article
Hemodynamic and Electroencephalographic Responses to Illusory Figures: Recording of the Evoked Potentials during Functional MRI