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. 2017 Jul 26;37(30):7188-7197.
doi: 10.1523/JNEUROSCI.2896-16.2017. Epub 2017 Jun 26.

Saturation in Phosphene Size with Increasing Current Levels Delivered to Human Visual Cortex

William H Bosking  1 , Ping Sun  2 , Muge Ozker  3 , Xiaomei Pei  2 , Brett L Foster  2   4 , Michael S Beauchamp  2   4 , Daniel Yoshor  2   4
Affiliations

Saturation in Phosphene Size with Increasing Current Levels Delivered to Human Visual Cortex

William H Bosking et al. J Neurosci. .

Abstract

Electrically stimulating early visual cortex results in a visual percept known as a phosphene. Although phosphenes can be evoked by a wide range of electrode sizes and current amplitudes, they are invariably described as small. To better understand this observation, we electrically stimulated 93 electrodes implanted in the visual cortex of 13 human subjects who reported phosphene size while stimulation current was varied. Phosphene size increased as the stimulation current was initially raised above threshold, but then rapidly reached saturation. Phosphene size also depended on the location of the stimulated site, with size increasing with distance from the foveal representation. We developed a model relating phosphene size to the amount of activated cortex and its location within the retinotopic map. First, a sigmoidal curve was used to predict the amount of activated cortex at a given current. Second, the amount of active cortex was converted to degrees of visual angle by multiplying by the inverse cortical magnification factor for that retinotopic location. This simple model accurately predicted phosphene size for a broad range of stimulation currents and cortical locations. The unexpected saturation in phosphene sizes suggests that the functional architecture of cerebral cortex may impose fundamental restrictions on the spread of artificially evoked activity and this may be an important consideration in the design of cortical prosthetic devices.SIGNIFICANCE STATEMENT Understanding the neural basis for phosphenes, the visual percepts created by electrical stimulation of visual cortex, is fundamental to the development of a visual cortical prosthetic. Our experiments in human subjects implanted with electrodes over visual cortex show that it is the activity of a large population of cells spread out across several millimeters of tissue that supports the perception of a phosphene. In addition, we describe an important feature of the production of phosphenes by electrical stimulation: phosphene size saturates at a relatively low current level. This finding implies that, with current methods, visual prosthetics will have a limited dynamic range available to control the production of spatial forms and that more advanced stimulation methods may be required.

Keywords: direct cortical stimulation; electrical brain stimulation; electrical stimulation; magnification factor; phosphene; visual cortex.

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Conflict of interest statement

The authors declare no competing financial interests.

Figures

Figure 1.
Figure 1.
Methods for electrical stimulation of visual cortex. A, Custom electrode strips used in our subjects. The research electrodes used for electrical stimulation were 0.5 mm in diameter and were arranged in a 4 × 6 mm rectangle surrounding each of the first four clinical recording electrodes on the strip. B, Posterior–medial view of the occipital portion of the left hemisphere of one brain showing the typical placement of one of the hybrid strips. The strip wraps around the occipital pole and extends into the interhemispheric fissure. C, Method for mapping phosphenes. Subjects fixated a cross on a touchscreen monitor while electrical stimulation was delivered and then drew the outline of the phosphene they perceived using a stylus. D, Timing of the phosphene drawing task. An auditory tone was delivered to warn the subject of the upcoming trial and to remind them to fixate the cross in the center of the screen. Then, a second auditory tone was played and the electrical stimulus train began. After the stimulus train, the subject was free to draw the outline of the phosphene they perceived and this continued for a variable amount of time. E, Structure of the electrical stimulus train. The pulse frequency was 200 Hz and the overall duration of the stimulus train was 200 ms. F, Pulse waveform used. Biphasic pulses (−/+) were used with 0.1 ms duration per phase. G–I, Location of electrodes (red symbols) used for electrical stimulation from all subjects aligned to Talaraich coordinates and displayed on a standard brain. G, Left hemisphere electrodes that were located on the medial wall of the occipital cortex. H, Right hemisphere electrodes located on the medial wall of occipital cortex. I, Left and right hemisphere electrodes located on the occipital pole and lateral occipital cortex.
Figure 2.
Figure 2.
Phosphene location versus RF location. A, Phosphene eccentricity versus RF eccentricity. Square symbols show the actual data; black line indicates linear regression [Pearson r = 0.90, p < 0.001, 95% confidence interval (CI) = 0.84 to 0.93; Spearman r = 0.86, p < 0.001, 95% CI = 0.77 to 0.92]. B, Phosphene polar angle versus RF polar angle. Square symbols show the actual data; black line indicates linear regression (Pearson r = 0.98, p < 0.001, 95% CI = 0.96 to 0.99; Spearman r = 0.86, p < 0.001, 95% CI = 0.74 to 0.93).
Figure 3.
Figure 3.
Phosphene size versus electrical current amplitude. A, Phosphene size tested for six different electrical currents using one electrode (red circle, inset) located near the occipital pole in one subject. L, Lateral; S, superior; A, anterior. Square symbols show the actual data; black line shows a sigmoidal function fit to the data (Pearson correlation r = 0.98, p < 0.001). B, Phosphene size tested for four different currents using one electrode located in the interhemispheric fissure in a different subject (Pearson correlation r = 0.99, p = 0.01). C, Phosphene size tested for four different currents using one electrode located near the occipital pole in a third subject (Pearson correlation r = 0.98, p = 0.02). D, Normalized phosphene size versus current curves for all electrodes that had a low threshold for producing phosphenes and for which multiple currents were tested. E, Slope, or rate of change in the phosphene size versus current curves, examined for all adjacent pairs of samples on the curves shown in D. For each pair, the slope is calculated as change in phosphene size (in normalized units from D) divided by the change in current (mA) and the data point is shown at the average current for the pair. Data points are shaded to show three different regions: low currents (I < 1.5 mA; dark shading), medium currents (I = 1.5–1.75 mA; medium shading), and high currents (I > 1.75; light shading). F, Average slope of phosphene size versus current curve for low (dark-shaded bar), medium (medium-shaded bar), and high (light-shaded bar) currents determined by averaging the three data groups shown in E.
Figure 4.
Figure 4.
Phosphene size versus eccentricity. A, Phosphene size versus eccentricity plotted using data from 6 electrodes in one subject (current = 2 mA). Black line indicates linear regression [Pearson r = 0.89, p = 0.017, 95% confidence interval (CI) = −0.38 to 0.98; Spearman r = 0.83, p = 0.058, 95% CI = 0.0 to 1.0]. Data points are colored to indicate the location of the corresponding electrode on the occipital cortex (inset). Dashed line indicates location of calcarine fissure. B, Phosphene sizes measured for 7 different electrodes in a second subject (current = 1 mA; Pearson r = 0.87, p = 0.01, 95% CI = 0.66 to 0.97; Spearman r = 1, p < 0.001, 95% CI = 1.0 to 1.0). C, Phosphene sizes measured for 8 different electrodes in a third subject (current ∼ = 1 mA; Pearson r = 0.98, p < 0.001, 95% CI = 0.31 to 1.0; Spearman r = 0.83, p = 0.015, 95% CI = 0.54 to 1.0). D, Group data for phosphene size versus eccentricity. Data were pooled from all electrodes for which we sampled with a current near 1 mA (n = 42 electrodes; 0.8–1.2 mA). Black line indicates linear regression (Pearson r = 0.89, p < 0.001, 95% CI = 0.76 to 0.94; Spearman r = 0.80, p < 0.001, 95% CI = 0.57 to 0.92).
Figure 5.
Figure 5.
Model for determining phosphene size. Our model predicts phosphene size by combining an estimate of spread of activity in visual cortex with an estimate of inverse cortical magnification factor. A, Sigmoidal function used to predict the diameter of visual cortex activated based on the electrical current delivered. B, Linear function used to determine magnification factor based on eccentricity (Horton and Hoyt, 1991). C, Schematic indicating the predicted spread of activity in visual cortex when a sample electrode is stimulated with six current levels. The predicted phosphene size (blue filled circles) was compared with the actual phosphene outlines for the same currents (red dashed ellipses). D, Performance of model. Predicted phosphene size versus actual phosphene size for data from all current levels using all electrodes tested in all subjects (n = 153 observations from 93 electrodes in 13 subjects). The black line indicates the linear regression [Pearson r = 0.94, p < 0.001, 95% confidence interval (CI) = 0.91 to 0.96; Spearman r = 0.90, p < 0.001, 95% CI = 0.86 to 0.94].
Figure 6.
Figure 6.
Relationship between predicted cortical activity and behavior. A, Schematic showing the map of visual space on a flattened human V1 (Horton and Hoyt, 1991). The circles indicate the area of cortex that we predict would be active in our experiments when subjects are stimulated at three different points in the map of visual space with a near threshold current (0.8 mA; 2 mm diameter activation; red circle = 1°, blue circle = 7.5°, green circle = 20°) and at two higher currents (1 mA-3.5 mm diameter activation; 2 mA-5.3 mm diameter activation, open circles). Note that the predicted diameter of activation in V1 is the same at the three eccentricities shown, but the magnification factor changes substantially. Also note that the predicted diameter of activated cortex is the same for any current >2 mA. B, Phosphene location and size predicted for electrical stimulation at each of the sites shown in A. Phosphenes increase in size with both eccentricity and current. C, Predicted cortical activation during nonhuman primate execution of saccades after electrical stimulation (based on Tehovnik et al., 2005a; Tehovnik and Slocum, 2007b). The schematic indicates the map of visual space on a flattened macaque V1. For simplicity, the macaque map is a scaled replica of the map of visual space shown for human V1. The colored circles indicate the ∼750 μm diameter activation area that is predicted using 100 μA and Equation 4 with K = 675. Again, the predicted activation diameter in V1 is the same at the two eccentricities shown, but the magnification factor changes. The inset to the right of the full map of V1 shows an expanded view of the region between 2.5° and 5° eccentricities for one sector of the map. D, Size of saccade delay fields based on the cortical activation at the two eccentricities shown in A. The delay field predicted for stimulation of the site at 4° eccentricity is larger due to the larger inverse magnification factor at this site.
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