NIH Public Access Author Manuscript Vision Res. Author manuscript; available in PMC 2013 June 01. NIH-PA Author Manuscript Published in final edited form as: Vision Res. 2012 June 1; 62: 220–227. doi:10.1016/j.visres.2012.04.011. Binocular retinal image differences influence eye-position signals for perceived visual direction Deepika Sridhar1 and Harold E. Bedell1,2 Harold E. Bedell: HBedell@Optometry.uh.edu 1College of Optometry, University of Houston. 505 J Armistead Bldg, Houston, TX 77204-2020, USA 2Center for NeuroEngineering & Cognitive Science, University of Houston, Houston, TX 77204-4005, USA Abstract NIH-PA Author Manuscript Correctly perceiving the direction of a visible object with respect to one’s self (egocentric visual direction) requires that information about the location of the image on the retina (oculocentric visual direction) be combined with signals about the position of the eyes in the head. The WellsHering laws that govern the perception of visual direction and modern restatements of these laws assume implicitly that retinal and eye-position information are independent of one another. By measuring observers’ manual pointing responses to targets in different horizontal locations, we show that retinal and eye-position information are not treated independently in the brain. In particular, decreasing the relative visibility of one eye’s retinal image reduces the strength of the eye-position signal associated with that eye. The results can be accounted for by interactions between eye-specific retinal and eye-position signals at a common neural location. Keywords Egocentric visual direction; visual suppression; eye-position; asymmetric vergence; heterophoria; pointing 1. Introduction NIH-PA Author Manuscript The direction of visual objects with respect to one’s self is known as egocentric (specifically, headcentric) visual direction (EVD). According to the Wells-Hering laws of visual direction that were proposed approximately two centuries ago (Hering, 1879/1942; Wells, 1818) perceived EVD results from a combination of the information about the location of the image on the retina and extra-retinal signals about the position of the eyes in the head: © 2012 Elsevier Ltd. All rights reserved. Corresponding author: Deepika Sridhar, College of Optometry, University of Houston, 505 J Armistead Bldg, Houston, TX 77204-2020, USA. DSridhar.2010@alumni.opt.uh.edu, Phone: +1 713 743 1993, Fax: +1 713 743 2053. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Sridhar and Bedell Page 2 NIH-PA Author Manuscript In this formulation, the perceived retinal image location is provided by local sign information, the direction with respect to the fovea that is associated with stimulation of a specific retinal location (Helmholtz, 1910/1962; Lotze, 1886; Rose, 1999), and sensed eye position. Eye-position information is obtained from extra-retinal eye-position signals, which have been shown to derive from an internal representation of the efferent commands to the eyes and from proprioceptive signals from the extraocular muscles (Bridgeman & Stark, 1991; Gauthier, Nommay & Vercher 1990; von Holst, 1954). For perceived EVD to be accurate, the eye-position signals from each eye should be weighted equally, as assumed by both Wells and Hering for observers with normal binocular vision. However, subsequent reports indicate that between-eye differences in the weighting of eye-position information occur in some observers (Simpson, 1992; Sridhar & Bedell, 2011). Therefore, in the general case, where w1 and w2 are the weights given to the left- and right-eye’s position information, respectively. NIH-PA Author Manuscript Similarly, the retinal component of perceived direction for a binocular visual target depends to some extent on the characteristics of each eye’s retinal stimulus. Specifically, the perceived direction of a disparate target is weighted more heavily toward the image with less blur (Charnwood, 1949), higher luminance (Charnwood, 1949; Francis & Harwood, 1951; Sridhar & Bedell, 2011), or more contrast (Ding & Sperling, 2007; Mansfield & Legge, 1996; Sridhar & Bedell, 2011), indicating unequal weighting of the retinal information from the two eyes. The Wells-Hering laws and modern restatements of these laws assume implicitly that the retinal and the eye-position contributions to perceived visual direction are independent of one another (Helmholtz, 1910/1962; Hering, 1879/1942; Ono, 1991; Walls, 1951; Wells, 1818). However, we reported recently that many individuals exhibit similar quantitative between-eye differences in the relative weighting of the retinal and eye-position information that contribute to perceived EVD (Sridhar & Bedell, 2011), raising the possibility that these two sources of information are not independent. NIH-PA Author Manuscript Binocular rivalry suppression is a commonly encountered perceptual phenomenon in which observers are unaware intermittently of part or all of the visual image that is presented to one eye (e.g., Bharadwaj, O’ Shea, Alais & Parker, 2008; Blake & Logothetis, 2002; Breese, 1909; Helmholtz, 1910/1962; Müller, 1842; Le Conte, 1897; Schor, 1977; Smith, Levi, Manny, Harwerth & White, 1994; Wheatstone, 1838; Wolfe, 1986). Subjects with strabismus exhibit clinical suppression when one eye is deviated, to avoid the confusion that would occur when dissimilar images fall on corresponding retinal points and diplopia when similar images fall on non-corresponding retinal points (Cooper, Feldman & Pasner, 2000; Hess, 1991; Holopigian, 1989; Schor, 1977; Serrano-Pedraza, Clarke & Reed, 2011; Sireteanu, 1982; Smith et al., 1994; Steinbach, 1981; Travers, 1940). In observers without strabismus, suppression is fostered by dissimilarity between the images in the two eyes, as occurs for example when the image in one eye is blurred as a result of anisometropia (e.g., Heath, Hines & Schwartz, 1986; Humphriss, 1982; Liu & Schor, 1994; Pianta & Kalloniatis, 1998; Schor, Landsman & Erickson, 1987; Shors, Wright & Greene, 1992; Simpson, 1991). The deviation of one eye has been reported not to influence perceived EVD in individuals with constant strabismus, who typically behave as if they are unaware of both the retinal and eye-position information from the deviated eye (Gauthier, Berard, Deransard, Semmlow & Vision Res. Author manuscript; available in PMC 2013 June 01. Sridhar and Bedell Page 3 Vercher, 1985; Mann, Hein & Diamond, 1979). These observations again raise the possibility that retinal and eye-position signals are not independent. NIH-PA Author Manuscript In the studies described here, we test the assumption of the Wells-Hering laws that independent retinal information and eye-position signals contribute to perceived EVD by estimating the weighting of the eye-position signals from each eye under conditions of unequal image visibility in the two eyes. The results demonstrate that the relative weighting of extra-retinal eye-position signals for the two eyes of normal observers depends on the relative visibility of the binocular retinal images. A parsimonious way to account for these findings is to assume that retinal and extra-retinal information interact to determine perceived EVD at a location in the brain where eye-specific signals exist. 2. General Methods NIH-PA Author Manuscript The first experiment investigated the relative weighting of the eye-position signals from the two eyes on perceived EVD when the image from one eye was suppressed foveally. To determine whether the perceptual suppression of one eye’s image is necessary for eyeposition signals to be altered, the second experiment compared the weighting of eye-position information from the two eyes when the image in each eye was of different luminance. In the third experiment, we assessed the weighting of eye-position signals when one eye was occluded, and allowed to drift to its heterophoric position, i.e., the angular misalignment of the occluded non-viewing eye with respect to the viewing eye. A fourth, control experiment assessed whether the contribution of eye-position information to perceived EVD depends on the velocity of the eye movements. At least seven adults participated in each of the experiments described here. All observers had best-corrected visual acuity of at least 20/20 in each eye and no history of abnormal binocular vision or ocular motility. Each observer voluntarily provided written informed consent in accordance with the tenets of the Declaration of Helsinki, after the experimental protocol was reviewed by the University of Houston Committee for the Protection of Human Subjects. NIH-PA Author Manuscript Perceived EVD was determined from normal observers’ open-loop pointing responses (Barbeito & Ono, 1979; Bock & Kommerell, 1986; Ono & Weber, 1981; Sridhar & Bedell, 2011; Steinbach & Smith, 1981) to a fixation cross that was presented on the black background of a 120-Hz frame-rate, gamma-corrected Clinton Monochrome Monoray monitor. The stimuli were presented at a physical distance of 50 cm. Observers viewed the monitor in a completely dark room through FE-1 ferro-electric goggles (Cambridge Research Systems) that were attached to a stand with a chin and head rest. Synchronization of the video-frames of the monitor with the ferro-electric goggles allowed for dichoptic image presentation during binocular viewing (in experiments 1, 2 and 4), and for the presentation of alternate video frames to one eye during monocular viewing (in experiment 3). The monitor is equipped with a DP 104 phosphor that decays to 0.1% of the peak value in 0.6 ms. Consequently, none of the presented images persisted from one frame to the next. For experiments 1, 2 and 4, different positions of one eye were produced by presenting that eye’s image of the cross with different horizontal separations on the monitor from the cross that was shown to the other eye (Figure 1). In these experiments, the eye that underwent a change in its final position as the result of the asymmetric vergence demand with respect to the plane of the monitor is referred to as the varying eye. The eye that undergoes no change in position as a result of the vergence demand is referred to as the non-varying eye. Vision Res. Author manuscript; available in PMC 2013 June 01. Sridhar and Bedell Page 4 3. Experiment 1: Perceived EVD during binocular suppression NIH-PA Author Manuscript Nine observers participated in the first experiment, which compared the contribution of the eye-position signal for the varying eye to the perceived EVD of a foveal target during and in the absence of foveal suppression. The suppression of the varying eye’s image was induced by blurring the image presented to that eye (Humphriss, 1982; Schor et al., 1987; Simpson, 1991), and detection thresholds were measured to determine the highest luminance at which the blurred foveal target could be presented and still be suppressed (see section 3.2., below). NIH-PA Author Manuscript The luminance detection threshold was measured for a cross (39.7 arc min long, and 5.3 arc min wide) and a 5.3 arc min square suppression check (presented approximately 21 arc min from the center of the cross) presented to one eye at the center of the monitor for an unlimited viewing time. Both the cross and the suppression check were filtered with a twodimensional Gaussian to simulate +1.25 D of blur during viewing with a 4 mm pupil (Smith, Jacobs & Chan, 1989). The blurred cross and suppression check will be referred to collectively as the blurred target (Figure 2). The detection threshold for the blurred target was determined also during binocular viewing when a clear 2.5 cd/m2 cross with no suppression check was presented concurrently to the other eye. For binocular detection thresholds, the clear cross seen by the non-varying eye was at the center of the monitor and the blurred target presented to the varying eye was positioned to stimulate 0, 8.55 deg of convergence, or 2.85 deg of divergence with respect to the plane of the monitor. In both the monocular and binocular viewing conditions, the observer adjusted the luminance of the blurred target so that the suppression check just disappeared. The order of the four viewing conditions (presentation of the blurred target to the right or left eye, for monocular and binocular viewing), and the asymmetric vergence demand during binocular viewing was randomized. Four separate detection thresholds were obtained for each monocular viewing condition and averaged. The binocular detection threshold was estimated twice for each vergence demand and averaged. The magnitude of foveal suppression was quantified as the log ratio of the average binocular to the average monocular threshold. Because the size of the target is small, we assume that the suppression measured in this experiment was limited to the fovea. 3.1. Assessment of eye-position NIH-PA Author Manuscript To ensure that the vergence responses during binocular viewing were approximately equal to the vergence demand in both the foveal-suppression and non-suppression conditions, in this and in experiments 2 and 4, fixation disparity was measured for each vergence demand using a pair of flashed dichoptic unblurred vertical Nonius lines (Ogle, Martens & Dyer, 1967), presented above and below a binocular fixation cross. During the foveal-suppression condition, the cross seen by the varying eye was blurred, and during the non-suppression condition the crosses seen by both eyes were clear. The horizontal offset of the Nonius line seen below the fixation cross by the varying eye that is perceived to be in alignment with the Nonius line seen above the fixation cross by the non-varying eye provided an estimate of the fixation disparity. 3.2. Measurement of perceived EVD The strength of the eye-position signals during the foveal suppression and non-suppression conditions was inferred from the open-loop pointing responses to targets with different asymmetric vergence demands. In the foveal-suppression condition, observers viewed the blurred target with the varying eye and a clear cross (2.5 cd/m2 luminance) with the nonvarying eye (Figure 2). The clear cross was presented at the center of the monitor or at 1.15, 2.29, or 3.44 deg to the right or left of center. The blurred target was displaced on the monitor with respect to the clear target to stimulate asymmetric vergence demands of 0, Vision Res. Author manuscript; available in PMC 2013 June 01. Sridhar and Bedell Page 5 NIH-PA Author Manuscript 2.85, 5.70, or 8.55 deg of convergence, or 2.85 deg of divergence. The luminance of the blurred target was set one standard deviation lower than the observer’s binocular detection threshold (mean = 0.24 cd/m2, see results for detection thresholds), to ensure that it was completely suppressed. In the non-suppression condition, the blurred target was replaced by a clear cross with a luminance of 2.5 cd/m2. The foveal-suppression and non-suppression conditions, the eye that viewed the blurred target during suppression, the target location and the asymmetric vergence demand were randomized from trial to trial. On each trial, the observer pressed a button to confirm that the suppression check was not visible when the clear and the blurred target were superimposed and to indicate that (s)he was ready to point to the target. The shutters of the goggles then closed in front of both eyes, and a dim horizontal scale, marked in 0.6 deg intervals and visible only to the experimenter, replaced the pointing target on the monitor. The observer pointed to the remembered location of the target using the index finger of the preferred hand and the experimenter noted the pointing response to the nearest 0.3 deg. A homogeneous white screen was presented for 3 s before the next pointing target, to control dark adaptation and to facilitate the visual recalibration of sensed eye position (Blouin, Amade, Vercher, Teasdale & Gauthier, 2002). Each set of trials consisted of 75 pointing responses. The responses from at least two sets of trials were combined for each observer. NIH-PA Author Manuscript Pointing errors were calculated as the difference between where the observer pointed on the monitor and the location of the target that was seen by the non-varying eye. The constant error was defined as the average pointing error (calculated separately for the fovealsuppression and non-suppression conditions) when there was no vergence demand with respect to the plane of the monitor. Pointing errors were corrected for each observer’s idiosyncratic constant error by subtracting the constant error from each pointing error. No statistically significant (p > 0.05) difference was observed in the corrected pointing errors to the target seen by the non-varying eye for the different locations on the monitor and the corrected pointing responses were plotted against the asymmetric vergence demand, separately for the right- and left eye-varying conditions and for the foveal-suppression and non-suppression conditions. Straight lines were fit to the corrected pointing errors to determine the strength of the eye-position signal for the varying eye in the presence and absence of foveal suppression. 3.3. Results NIH-PA Author Manuscript Average monocular and binocular detection thresholds for the blurred target were 0.17 ± 0.11 (SD) and 0.34 ± 0.13 cd/m2. The average depth of suppression was −0.34 ± 0.21 log units (across observers, range: −0.11 to −0.66 log units), in agreement with previous studies in strabismic subjects with suppression, and in non-human primates with experimentally induced strabismus (Holopigian, 1989; Wensween, Harwerth & Smith, 2001). For the observers in this experiment, the fixation disparity was small, amounting to 8.95 (±5.78 SD) and 5.26 (±4.20) arc min in the foveal-suppression and non-suppression conditions, respectively, indicating that in both conditions the asymmetric vergence response was essentially equivalent to the vergence demand. Nevertheless, the difference in fixation disparity between the two conditions reaches statistical significance (tdf=8 = 2.32; p = 0.049). Across observers, the average variability of the pointing responses in the fovealsuppression and non-suppression conditions was 1.88 ± 0.57 and 1.66 ± 0.40 deg, respectively, which do not differ significantly (repeated tdf=8 = 0.57, p = 0.58, 2-tailed). Straight lines fit to each observer’s pointing responses as a function of the asymmetric vergence demand specify the weighting afforded to the position signals for the varying eye (Figure 3). According to the Wells-Hering laws of visual direction the expected slope of the Vision Res. Author manuscript; available in PMC 2013 June 01. Sridhar and Bedell Page 6 NIH-PA Author Manuscript fitted lines is 0.5, which would indicate an equal contribution of the position signal for each eye to perceived EVD. For the 9 observers tested in this experiment, the slopes of the fitted lines were significantly shallower during the foveal-suppression condition than the nonsuppression condition, indicating a reduced weighting of the eye-position signal from the suppressed eye (mean absolute values of slope = 0.45 ± 0.08 [SD] and 0.34 ± 0.13 in the non-suppressed and suppressed conditions, respectively; repeated measures tdf=8 = 3.68, p = 0.006, 2-tailed; Figures 3a, b and 4). 4. Experiment 2: Perceived EVD for targets of unequal luminance NIH-PA Author Manuscript The second experiment determined how the relative luminance of the retinal images in the two eyes influences the strength of the eye-position signal to perceived EVD. Eight observers participated. In this experiment, the pointing targets presented to the two eyes (including the suppression check for the varying eye) were unblurred and had either the same luminance in both eyes, or the luminance of the cross and the suppression check shown to the varying eye was 4 or 8 times lower than the cross shown to the non-varying eye. The mean luminance of the two eyes’ images remained equal to 2.5 cd/m2 in all viewing conditions. The strength of the eye-position signal for each luminance condition was estimated as in section 3.2 by first calculating the corrected pointing errors and then fitting straight lines separately to the corrected pointing errors made when the right or the left eye was the varying eye. 4.1. Results As expected, the observers in this experiment reported that the suppression check presented to the varying eye always remained visible. Nevertheless, the slopes of the lines fit to the 8 observers’ pointing responses were significantly shallower when the varying eye viewed a target that was 4 or 8 times lower in luminance than the non-varying eye, compared to when both eyes viewed targets of equal luminance (Geisser-Greenhouse corrected post-hoc comparisons following significant [F df=2,14 = 6.34, p = 0.023] repeated-measures ANOVA; Fdf=1,14 = 5.55, p = 0.049 for 4 times difference in luminance; Fdf=1,14 = 12.18, p = 0.009, for 8 times difference in luminance, Figures 3c, d and 4). 5. Experiment 3: Perceived EVD during occlusion of one eye NIH-PA Author Manuscript The third experiment measured the contribution of the eye-position signal to perceived EVD during monocular viewing, i.e., in the complete absence of retinal information from one eye. Open-loop pointing responses were obtained from 10 observers when either the right or left eye viewed the target, or when both eyes viewed a target with no vergence demand with respect to the plane of the monitor. The average pointing error during binocular viewing was subtracted from the average pointing error during monocular viewing to indicate the position information that was available from the occluded eye during monocular viewing. As in experiments 1 and 2, above, accurate eye alignment during binocular viewing was verified by fixation disparity measurements. During monocular viewing, the fixation cross was visible to only one eye. Therefore, the physical offset between the flashed dichoptic Nonius lines that produced the perception of vertical alignment specified the direction and magnitude of the observer’s lateral heterophoria. 5.1. Results During monocular viewing, the average angle of hetereophoria for the 10 observers was 2.10 ± 2.17 [SD] deg (range = 0.12 to 7.18 deg) in the divergent direction. Because the position of the occluded eye was not manipulated in this experiment, Figure 5 plots one data point per observer, corresponding to the average difference between the pointing responses during Vision Res. Author manuscript; available in PMC 2013 June 01. Sridhar and Bedell Page 7 NIH-PA Author Manuscript binocular fixation of the cross and during fixation when one eye was occluded. The straight line fit to the observers’ average monocular pointing responses was constrained to have a yintercept of zero, based on the Wells-Hering prediction that no systematic pointing error should occur in the absence of hetereophoria.* The best fitting slope is 0.27 ± 0.05, which is significantly greater than a slope of zero (tdf=9 = 5.08, p = 0.006), but also is significantly less than the value of 0.5 that is predicted by the Wells-Hering laws of visual direction (tdf=9 = 4.49, p = 0.003). 6. Target visibility and eye-position information NIH-PA Author Manuscript Figure 4 compares the average slopes of the pointing vs. eye-position functions for the different conditions of relative target visibility. A comparison of the dark gray bars indicates that no significant difference exists between the slopes fit to the observers’ pointing responses in the non-suppression condition of Experiment 1 (central pair) and the equalluminance condition of experiment 2 (leftmost set of 3 bars; Welch’s two-sample tdf=14, = 0.996, p = 0.336, 2 tailed). Neither of these average slopes differ significantly from the expected value of 0.5 (for the non-suppression condition, tdf=8 = 1.89, p = 0.095; for the equal-luminance condition, tdf=7 = 0.36, p = 0.73). The average slope of the pointing vs. eye-position function fell to 0.41 when the target shown to the varying eye was 8 times lower in luminance than the target seen by the fellow eye (light gray bar in the left set of 3 bars), and to 0.35 when a dim, blurred target was presented to the varying eye and perceptually suppressed (light gray bar in the central pair of bars). In the condition when one eye was occluded, the strength of the eye-position signal was calculated as the difference in pointing during monocular vs. binocular viewing, divided by the observers’ measured heterophoria. Figure 4 (rightmost bar) shows that the contribution of the occluded eye’s position signal to perceived EVD is on average less than half of the value expected from the Well-Hering’s laws, with substantial between-observer variability. 7. Experiment 4: Perceived EVD and asymmetric vergence velocity NIH-PA Author Manuscript The velocity of the vergence eye movement that occurs following the occlusion of one eye is typically slower (Barnard & Thomson, 1995; Kim, Granger-Donetti, Vicci & Alvarez, 2010; Ludvigh, McKinnon, & Zaitzeff, 1964; Park & Shebilske, 1991; Peli & McCormack, 1983) than vergence eye movements in response to horizontal image disparity during binocular viewing (Maxwell, Tong & Schor, 2010; Semmlow, Hung & Ciuffreda, 1986). It is therefore possible that the low velocity of the eye movement that occurs following the occlusion of one eye, compared to the higher velocity of vergence during binocular viewing is responsible for the decreased eye-position-signal weight for the occluded eye in Experiment 3. To assess whether the velocity of asymmetric vergence influences estimates of perceived EVD, nine observers viewed identical unblurred crosses (without suppression checks) in the two eyes that either (1) appeared with one of several asymmetric vergence demands with respect to the monitor, or (2) appeared initially with no vergence demand, after which the target seen by the varying eye moved at a velocity of either 0.75 or 1.5 deg/s to produce the same final amplitudes of asymmetric vergence. The velocities of 0.75 and 1.5 deg/s were chosen to approximately match the range of eye velocities reported previously after the occlusion of one eye (Barnard & Thomson, 1995; Kim, Granger-Donetti, Vicci & Alvarez, 2010; Ludvigh, McKinnon, & Zaitzeff, 1964; Park & Shebilske, 1991; Peli & McCormack, 1983). *If the regression line is not constrained to pass through (0, 0), the fitted intercept is −0.420, which does not differ significantly from an intercept of zero (tdf=8= 1.92, p = 0.092). Vision Res. Author manuscript; available in PMC 2013 June 01. Sridhar and Bedell Page 8 NIH-PA Author Manuscript When the target appeared initially with an asymmetric vergence demand, the observer either pointed at the target immediately or after a delay of 9 s. This is the duration required to achieve the largest vergence demand when the targets seen by both eyes appeared initially with no vergence demand and then the target seen by the varying eye moved at a velocity of 0.75 deg/s. The different amplitudes, which are identical to those used in Experiments 1 and 2, and velocities of vergence demand and the varying eye changed randomly from trial to trial. 7.1. Results The observers’ pointing responses do not differ significantly among the different eyevelocity conditions in Experiment 4 (repeated-measures ANOVA, F3,18 = 0.127, p = 0.943, Geisser-Greenhouse corrected). This outcome indicates that the reduced eye-position signal for the occluded eye in the third experiment is unlikely to be attributable to the slow dynamics of the phoric eye-movement response. 8. Discussion NIH-PA Author Manuscript We showed previously that normal individuals frequently exhibit between-eye differences in the weighting of retinal and eye-position information and that, within individuals, the weighting of these two types of information is correlated (Sridhar & Bedell, 2011). The results presented here indicate that the relative visibility of the retinal images in the two eyes influences the weighting of the eye-position signals for perceived EVD. Previously, Blouin et al. (2002) determined that information about the perceived direction of binocular eccentric gaze is approximately 20 percent weaker in darkness or with minimal visual stimulation, compared to conditions in which the visual stimulation is more extensive. Considering the results of our second experiment, it is not clear whether the reduction of eye-position weighting that we found when a blurred, low luminance target is presented to one eye is attributable to the suppression of that eye’s visual information, to the associated reduction of target luminance (on average, by a factor of 10.6 times, compared to the luminance of the target presented to the non-suppressed eye), or both. NIH-PA Author Manuscript The application of a common weighting factor for retinal and eye-position information and the interaction between retinal information and eye-position signals would occur most parsimoniously at a common neural site. However, the characteristics of the neural signals that are required for these interactions to occur make the identification of a likely neural location difficult. For the relative visibility of the two retinal images to influence the weighting of eye-position signals, both the retinal and the eye-position signals at any candidate site should be eye-specific. Eye-specific retinal information is available primarily in neurons at lower levels of processing in the visual pathway (for example in the lateral geniculate nucleus and in cortical areas V1 and V2 (Hubel & Wiesel, 1962; Zeki, 1978a), whereas the neurons in higher visual areas carry primarily binocular information (Zeki, 1978b). On the other hand, neurons that combine eye-position and visual information are either absent or minimal in areas V1 and V2, and are increasingly common in higher visual areas, such as V3, V3A, LIP and MST (Balslev & Miall, 2008; Galletti & Battaglini, 1989; Gur & Snodderly, 1997; Nakamura & Colby, 2002; Prevosto, Graf & Ugolini, 2009; Wang, Zhang, Cohen & Goldberg, 2007). It remains unknown whether the neuronal eye-position signals in any of these higher visual areas are eye-specific, as would be required for a change in the weighting of eye-position signals to be implemented. A recent psychophysical result indicates that eye-specific visual information must be available in the higher visual areas, such as MT or MST, that process two-dimensional and three-dimensional motion information (Rokers, Czuba, Cormack & Huk, 2011). Lehky (2011) attempted to account for the availability of monocular visual information beyond the Vision Res. Author manuscript; available in PMC 2013 June 01. Sridhar and Bedell Page 9 NIH-PA Author Manuscript neural locus of binocular visual combination by demonstrating that the visual information available to the left and right eyes can in principle be recovered from the responses of binocular visual neurons that exhibit different degrees of ocular dominance. Similarly, an appropriate combination of neural signals that specify conjugate and convergence eye positions (essentially reversing the strategy envisioned by Hering (Hering, 1868/1977, also Minken, Gielen & Van Gisbergen, 1995) to generate oculomotor commands would allow the brain to recover separate eye-position signals for the left and right eyes. Implementation of these or similar neural strategies could account for our results that retinal and eye-position information are not independent of each other, as has long been assumed, by allowing for interactions to occur at a higher level of visual processing where visual and eye-position signals are available concurrently. NIH-PA Author Manuscript Our finding that the relative visibility of the retinal images affects the weighting of eyeposition signals also addresses a long-standing controversy as to whether the brain takes the position of the non-viewing eye into account during monocular viewing (Erkelens, 2000; Gauthier, Nommay & Vercher, 1990; Helmholtz, 1910/1962; Hering, 1879/1942; Morgan, 1947; Ono & Weber, 1981; Park & Shebilske, 1991; Simpson, 1992; Wells, 1818). Both Hering (1879/1942) and Helmholtz (1910/1962) believed that eye-position signals from the non-seeing eye are taken into account when either eye is occluded. However, Helmholtz predicted that eye position is taken into account more completely when the favored (or dominant) eye is occluded and Walls (1951) argued that only the position of the dominant eye is accounted for during occlusion. Most (but not all, see Walls, 1951) studies confirm that the eye-position signals from an occluded eye contribute to the perceived EVD of a target that is visible only to the unoccluded eye. In agreement with previous reports (Ono & Weber, 1981; Park & Shebilske, 1991; Simpson, 1992), our data show that the contribution of the eye-position signal from the non-viewing eye is not complete, and exhibits considerable variability among observers. For example, Ono and Weber’s (1981) data indicate a weighting of eye position for the occluded eye of 0.28 ± 0.28 in a sample of 19 observers, in contrast to an expected weighting of 0.5 based on the Wells-Hering’s laws. This difference in eye-position weighting between binocular and monocular viewing conditions is not accounted for by differences in the eye movements during binocular and monocular viewing and raises questions about the quantitative contribution of eye-muscle proprioception to signaled eye position, which has been evaluated previously only during monocular viewing (Bridgeman & Stark, 1991; Gauthier, Nommay & Vercher, 1990). Acknowledgments NIH-PA Author Manuscript We thank Drs. Saumil Patel and Scott Stevenson for helpful suggestions and Dr. Ying-sheng Hu for statistical advice. This research was supported in part by Core Center grant, P30 EY07551 from the National Eye Institute. References Balslev D, Miall RC. Eye position representation in human anterior parietal cortex. Journal of Neuroscience. 2008; 28:8968–8972. [PubMed: 18768690] Barbeito R, Ono H. Four methods of locating the egocenter: A comparison of their predictive validities and reliabilities. 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Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex. Journal of Physiology. 1978b; 277:273–290. [PubMed: 418176] NIH-PA Author Manuscript Vision Res. Author manuscript; available in PMC 2013 June 01. Sridhar and Bedell Page 13 Highlights NIH-PA Author Manuscript • Eye-position and retinal information determine perceived egocentric direction. • It is assumed that eye-position and retinal information are processed independently. • Here we show that these two sources of information interact with one another. • Monocular eye-position signals are likely to occur at higher cortical visual areas. NIH-PA Author Manuscript NIH-PA Author Manuscript Vision Res. Author manuscript; available in PMC 2013 June 01. Sridhar and Bedell Page 14 NIH-PA Author Manuscript NIH-PA Author Manuscript Figure 1. NIH-PA Author Manuscript The Wells-Hering laws of visual direction predict that the perceived egocentric visual direction (EVD) of a foveally viewed target should vary systematically with the positions of both eyes, even if only one eye views the target. The three arrows in the left panel show the predicted direction of a foveal target for three different positions of the left eye. In this example, virtual targets farther and nearer than the plane of the monitor (i.e., at the gray square and circle) are produced by shifting the location of the target that is seen by the left eye (dotted gray crosses to the left and right of the cross seen by the right eye at the center of the monitor). The thin solid and dashed lines represent the left and right eyes’ lines of sight, which correspond to three difference asymmetric vergence demands. The right panel illustrates how pointing responses are expected to change as a function of the left eye’s position. If the position of both eyes is weighted equally, then the line fit to the pointing responses is predicted to have a slope of 0.5. A shallower slope indicates that the position signal for the varying left eye is weighted less in the computation of perceived EVD than the position signal for the non-varying right eye. If the position of the right eye varies, then the expected slope of the line fit to the pointing responses is −0.5. Vision Res. Author manuscript; available in PMC 2013 June 01. Sridhar and Bedell Page 15 NIH-PA Author Manuscript Figure 2. Stimuli for Experiment 1. The images of the cross and suppression check (below and right of the cross) seen by the varying eye (left panel) were blurred. To measure monocular detection thresholds, only the blurred image was presented to one eye. To measure detection thresholds during binocular viewing, a clear cross (and no suppression check) was presented concurrently to the other eye. Similarly, during the measurement of perceived EVD, the two eyes viewed images that were presented dichoptically. NIH-PA Author Manuscript NIH-PA Author Manuscript Vision Res. Author manuscript; available in PMC 2013 June 01. NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript Sridhar and Bedell Vision Res. Author manuscript; available in PMC 2013 June 01. Page 16 Sridhar and Bedell Page 17 NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript Figure 3. Sample plots of corrected pointing errors vs. vergence demand (i.e., the position of the varying eye) for the foveal-suppression and non-suppression conditions in experiment 1 (top two panels, a and b) and for the conditions of different target luminance in the two eyes in experiment 2 (bottom two panels, c and d). Triangles and circles in the top two plots indicate the corrected pointing errors obtained when the left or the right eye position varies, respectively. The best fitting lines to the corrected pointing responses as a function of the asymmetric vergence demand are shown. The different symbols in the bottom two plots indicate pointing responses for different interocular luminance ratios, when either the left or the right eye position varies. Specifically, black unfilled, grey, and filled black circles indicate the corrected pointing errors for 1:1, 4:1 and 8: 1 luminance ratios, respectively. Bold black lines, grey lines, and dotted black lines indicate the best-fitting lines for 1:1, 4:1 Vision Res. Author manuscript; available in PMC 2013 June 01. Sridhar and Bedell Page 18 and 8:1 luminance ratios, respectively. Symbol and line conventions in panel 3d are same as those in panel 3c. NIH-PA Author Manuscript NIH-PA Author Manuscript NIH-PA Author Manuscript Vision Res. Author manuscript; available in PMC 2013 June 01. Sridhar and Bedell Page 19 NIH-PA Author Manuscript NIH-PA Author Manuscript Figure 4. NIH-PA Author Manuscript Absolute values of the slopes fit to the pointing vs. eye-position data, averaged for all observers and for changes in the position of the left and right eyes in the different experimental conditions. Slope values are interpreted to indicate the eye-position weighting for the varying eye. The leftmost 3 bars indicate averaged right- and left-eye absolute slope values when both eyes viewed targets of equal luminance (dark gray bar), and when the luminance of the target seen by one eye was lower by a factor of 4 or 8 times (stippled and light gray bars, respectively). The middle pair of bars indicates the average right- and lefteye absolute slope values in the absence of suppression (dark gray bar) and during suppression of the varying eye’s fixation target (light gray bar). The rightmost bar indicates the averaged magnitude of the eye-position signal during occlusion of the left or the right eye. The eye-position signal during occlusion was calculated for each observer as the corrected pointing error divided by the lateral heterophoria, averaged for occlusion of the left and right eyes. Error bars indicate ±1 SE of the mean. Vision Res. Author manuscript; available in PMC 2013 June 01. Sridhar and Bedell Page 20 NIH-PA Author Manuscript NIH-PA Author Manuscript Figure 5. Relationship between corrected pointing errors and lateral heterophoria. Each data point represents the average corrected pointing error during occlusion of the left and right eyes for one observer, with positive errors in the direction predicted by the Well’s-Hering laws. The continuous and the dashed lines represent the best-fit line to the data (constrained to have a y-intercept of 0) and the Wells-Hering slope prediction of 0.5. NIH-PA Author Manuscript Vision Res. Author manuscript; available in PMC 2013 June 01.