Steady-State Visually Evoked Potentials Elicited by Multifrequency Pattern-Reversal Stimulation

Abstract

Purpose: It has been shown that multifrequency stimulation with multifocal electroretinography can reduce recording time without a loss in signal-to-noise ratio. Here, we studied the applicability of multifrequency stimulations for steady-state visually evoked potential (VEP) recordings.

Methods: Multifrequency VEPs were recorded monocularly from 10 healthy subjects using pattern-reversal stimuli. The reversal frequency varied between 5 and 30 Hz. Pattern-reversal checkerboard stimuli were generated using four square arrays, each containing 100 light-emitting diodes (LEDs), positioned in four quadrants. Each array had a temporal frequency that differed slightly from the nominal frequency. The long duration of the data acquisition ensured that the slightly different stimulus frequencies in the four LED arrays can be resolved and that the responses to the stimulus in each array can be distinguished (e.g., with a frequency resolution: 0.011 Hz at 12 Hz). The best response from the four recording electrode configuration, defined as the recording with the maximal signal-to-noise ratio, was used for further analysis. Algorithmic latencies were calculated from the ratio of phase data and frequencies in a range of 4 and 20 Hz.

Results: Quadrant-VEPs with simultaneous pattern-reversal stimulation yielded a significant dependency on temporal frequency and stimulus location. The frequency range leading to the maximal response amplitude was between 10 and 12 Hz. Response phases decreased approximately linearly, with increasing temporal frequency suggesting a mean algorithmic latency between 112 and 126 ms.

Conclusions: Multifrequency stimulation using LED arrays is an efficient method for recording pattern-reversal VEPs while all stimuli are presented at the same time.

Translational relevance: Simultaneously recorded VEPs as performed by the multi-frequency method can be used for objective measurements of visual field defects.

Keywords: multifocal VEP; objective visual field test; pattern reversal; signal-to-noise ratio; steady-state.

Figure 1

Stimulus arrangement of four LED arrays.

Figure 2

Spectra of steady-state VEP obtained from the four recording channels for a nominal 12-Hz pattern-reversal frequency. The measurement time was 91.5 seconds. In this time span, the number of reversals at each LED array was 1073, 1098, 1108, and 1123, respectively. Thus, the exact frequency of each LED array was 11.727 (left upper), 12.000 (right upper), 12.109 (left lower), and 12.273 Hz (right lower). For the most part, the stimulus frequencies were detected in all recording channels. The spectra deliver nine or more nonstimulus frequencies between the stimulus frequencies, which can be used to calculate the SNR.

Figure 3

Spectra obtained from a recording at one channel (electrodes above and below inion) for all frequencies tested.

Figure 4

Reliability of multifocal VEPs: (a) Bland-Altman analyses of all first and second VEP amplitudes reveal the variation between measurements in four quadrants. There was no significant relationship between difference and mean of the amplitudes. (b) Correlation coefficients of the reliability analysis for first and second measurement at four LED arrays. The dotted line indicates the significance level (with consideration of Bonferroni correction).

Figure 5

(a) SNR (±95 CI) from 10 healthy subjects plotted as a function of temporal frequency (Hertz) for all four LED arrays. (b) Filled symbols: mean amplitudes (microvolts) (±95 CI) from all subjects as a function of stimulus frequency plotted for different positions of the stimulation field. Maximal signals were recorded in the upper-right LED array. For all stimulus postions, a maximal amplitude was observed at 10 or 12 Hz. Open symbols: amplitudes calculated at two nonstimulus frequencies (noise level).

Figure 6

(a) Phase values from three subjects for different channels at one stimulus location (upper right). The figures show individual linear regression lines and indicate good reproducibility of the phase values from first and second measurement by equal symbols. Eleven percent (23/216) of the phase values were excluded because corresponding amplitudes were low at this stimulus position. An algorithmic latency value for each subject has been calculated by the slope of the regression line using the formula (in milliseconds): latency = − [(Δphase/ΔF) × 1000 ms/360°]. (b) Phase values for all quadrants at channel 1 (i.e., electrodes above and below from inion). At this electrode position, the SNR values were larger than 2 dB in 75% (538/720) of the cases. The figures also show regression lines and indicate algorithmic latencies for the total cohort.