Visual motion priming reveals why motion perception deteriorates during mesopic vision

Abstract

Abstract

Abstract:

Abstract  We know empirically that the perception of moving objects deteriorates under mesopic vision, in which both rods and cones operate. The purpose of this study was to examine the cause of this degradation. We utilized a phenomenon called visual motion priming, in which the perceived direction of a directionally ambiguous test stimulus is influenced by the moving direction of a preceding stimulus. The spatial distances between the priming and the test stimuli were varied. At mesopic light levels, a stimulus that is presented at the central retina is presumably processed by the cone system, while a stimulus that is presented at the peripheral retina is processed by the rod system (Raphael & MacLeod, 2011). Subjects judged the perceived direction of 180° phase-shifted sine-wave grating that was followed by a smoothly drifting priming stimulus under different retinal illuminances. We found that, under mesopic conditions, the strength of motion priming was greatly reduced when the priming and test stimuli were presented separately at the center and the periphery, respectively. In contrast, motion priming was perceived in most of the trials under photopic and scotopic conditions or when both the priming and test stimuli were presented at the central retina under mesopic conditions. When the priming and test stimuli temporally overlapped, motion priming was conspicuous irrespective of the retinal illuminance. These results suggest that the incompleteness in the integration of signals that was induced by the temporal delay of rod pathways caused the degradation of motion perception under mesopic vision.

Introduction

In natural environments, ambient light levels may change by a factor of 10¹¹ between day and night (Hood & Finkelstein, 1986; Stockman & Sharpe, 2006). Because the dynamic range of the constituent neurons of the visual system is limited to approximately 10² (Wandell, 1995), the visual system deals with this by switching between two different types of photoreceptors: rods, which function at lower levels of illumination, and cones, which function at higher levels. Scotopic, mesopic, and photopic regions are defined, respectively, according to whether rods alone, rods and cones, or cones alone operate. In our daily lives, the range of scotopic and mesopic vision, in which the rod system is active, extends over a range as wide as 10⁶. An understanding of the characteristics of visual functioning under low levels of retinal illuminance is therefore very important from both scientific and practical viewpoints (Hess, 1990; Hess, Sharpe, & Nordby, 1990). 

In this study, the characteristics of visual motion perception with mesopic vision were examined. At mesopic light levels, the underlying computation is supposed to be particularly complex because input signals are processed through rod and cone pathways, which have different spatiotemporal properties (Bloomfield & Dacheux, 2001; Stockman & Sharpe, 2006). Visual perception—and presumably motion perception—is known to deteriorate with mesopic vision. For example, the number of traffic accidents has been reported to greatly increase at dusk both in the United States (Owens, Wood, & Owens, 2007) and in Japan (Yamadaya, 2010). According to a report from Japan's Metropolitan Police Department (Yamadaya, 2010), the deterioration in visual motion sensitivity that has been observed at dusk could be a possible explanation for the increase in the traffic accident rate at that time, although there has been no experimental evidence for this. Another example is related to ball games, such as tennis or baseball. It is empirically known that a baseball outfielder is more likely to lose sight of a fly ball in the twilight sky and commit errors. In tennis, it is the personal impression of one of the authors that tracking a moving ball at dusk seems to be difficult, even though the visibility of the ball is preserved at that time. 

Psychophysical experiments that have been conducted in laboratories have shown that the perception of visual motion varies with retinal illuminance. Velocity perception (Gegenfurtner, Mayser, & Sharpe, 2000; Hammett, Champion, Thompson, & Morland, 2007; Pritchard & Hammett, 2012; Vaziri-Paskham & Cavanagh, 2008), velocity discrimination thresholds (Takeuchi & De Valois, 2000), short-range motion perception (Dawson & Di Lollo, 1990), complex-motion perception (Billino, Bremmer, & Gegenfurtner, 2008), biological-motion perception (Billino et al., 2008; Grossman & Blake, 1999), perception of static-motion illusions (Hisakata & Murakami, 2008), perception of interstimulus-interval reversal (Sheliga, Chen, FitzGibbon, & Miles, 2006; Takeuchi & De Valois, 1997, 2009; Takeuchi, De Valois, & Motoyoshi, 2001), perception of two-stroke motion (Mather & Challinor, 2009), the coherent-motion threshold (Billino et al., 2008; Lankheet, van Doorn, & van de Grind, 2002; van de Grind, Koenderink, & van Doorn, 2000), and moving-texture segregation (Takeuchi, Yokosawa, & De Valois, 2004) have all been shown to vary with the retinal illuminance. 

Billino et al. (2008) found that biological-motion processing at low light levels is most relevant to an understanding of the deterioration of motion perception that occurs with mesopic vision in the real situations mentioned previously. They measured the thresholds for the detection of biological-motion perception during photopic, mesopic, and scotopic conditions and found that the detection thresholds for biological motion were exclusively increased in mesopic conditions, even though the thresholds under scotopic conditions matched those under photopic conditions. They speculated that the largest threshold increases that occur in mesopic conditions are caused by the simultaneous activity of rods and cones, which could result in degraded velocity perception. In this study, we examined visual motion perception when both cone- and rod-mediated signals were involved in order to clarify why motion perception deteriorates at mesopic light levels. For this purpose, we used a phenomenon called visual motion priming. 

Visual motion priming is a phenomenon in which the perceived direction of a directionally ambiguous stimulus is influenced by the movement direction of the preceding stimulus (Anstis & Ramachandran, 1987; Campana, Pavan, & Casco, 2008; Jiang, Luo, & Parasuraman, 2002; Jiang, Pantle, & Mark, 1998; Kanai & Verstraten, 2005; Pantle, Gallogly, & Piehler, 2000; Pavan, Campana, Guerresch, Manassi, & Casco, 2009; Piehler & Pantle, 2001; Pinkus & Pantle, 1997; Ramachandran & Anstis, 1983; Raymond, O'Donnell, & Tipper, 1998; Takeuchi, Tuladhar, & Yoshimoto, 2011). Ramachandran and Anstis (1983) reported that a preceding brief dot stimulus induces visual inertia, in which a subsequent directionally ambiguous bistable long-range stimulus is perceived to move in the same direction as the preceding one. Pinkus and Pantle (1997) used a moving sine-wave grating and showed that visual inertia occurs with a periodic pattern. A subsequently presented directionally ambiguous test pattern that was made of a 180°-shifted grating is perceived to move in the same direction as the priming grating when the presentation duration of the primer is less than approximately 300 ms. They named this phenomenon positive motion priming. Pantle et al. (2000) showed that positive motion priming is perceived when the presentation duration of the priming stimulus is shorter, while so-called negative motion priming is perceived when a subsequent test pattern is perceived to move in the opposite direction of the priming stimulus when its presentation duration is longer. In addition, Kanai and Verstraten (2005) showed that the strength of positive motion priming is reduced as the presentation duration of the priming stimulus increases, and the perceived direction of the test pattern is reversed by a priming stimulus of 640 ms. They called this negative priming phenomenon the rapid form of motion aftereffects (see, e.g., Mather, Verstraten, & Anstis, 1998). These previous studies have shown that positive priming switches to negative priming as the primer duration lengthens under photopic vision. In summary, these studies suggest the existence of a mechanism that integrates the preceding priming pattern and the test pattern in order to elicit motion perception (Pinkus & Pantle, 1997). 

In previous studies (Kanai & Verstraten, 2005; Pantle et al., 2000; Pavan et al., 2009; Piehler & Pantle, 2001; Takeuchi et al., 2011), both priming and test stimuli were presented at the same location in the visual field. Our work differs from these studies, as we separately presented the priming and test stimuli in the central and peripheral retinae. The reason for this manipulation is that the transition from cone to rod vision that accompanies decrements in retinal illuminance has been shown to not occur uniformly over the visual field. Raphael and MacLeod (2011) have estimated the relative contribution of rods and cones to luminance at various light levels and retinal eccentricities by minimum-motion photometry with annular grating patterns of different-sized radiuses ranging from 1° to 18°. Their results show that, under mesopic light levels, the cones define vision alone in the central retina, and as retinal eccentricity increases, the relative rod contribution in the peripheral retina becomes larger (see Raphael & MacLeod, 2011, figure 5). Therefore, by separately presenting priming and test stimuli in the center and periphery, we expected that we would be able to determine how the separate visual inputs to cone and rod systems are processed to induce motion priming. One possible prediction from the results of the study by Billino et al. (2008) is that the strength of motion priming will be reduced under mesopic conditions when the priming and test stimuli are separately presented in the cone-mediated central and rod-mediated peripheral visual fields, presumably because of the different spatiotemporal response characteristics of the two systems (see, e.g., Buck, 2004). 

Our method utilizing visual motion priming with spatially separated priming and test stimuli raises an interesting issue regarding visual motion-detecting mechanisms. It has been shown that different types of motion-detecting mechanisms are implemented in the visual system (see, e.g., Cavanagh & Mather, 1989; Lu & Sperling, 1995) and that the relative contributions of those motion mechanisms differ depending on the retinal eccentricity (see, e.g., Ashida, Seiffert, & Osaka, 2001; Chubb & Sperling, 1989; Edwards & Nishida, 2004; Lu & Sperling, 1999; Maruya, Mugishima, & Sato, 2003; Pantle, 1992; Smith, Hess, & Baker, 1994; Solomon & Sperling, 1994; Takeuchi & De Valois, 2009; Wang, Hess, & Baker, 1997; Zanker, 1997). Takeuchi and De Valois (2009) showed with a phenomenon called interstimulus-interval (ISI) reversal (Braddick, 1980) that the relative contribution of higher-order motion mechanisms, such as feature-tracking mechanisms (see, e.g., Cavanagh, 1992, 1994; Nishida, 2011), in the central visual field becomes larger as retinal illuminance decreases, while motion perception in the peripheral visual field continues to depend on first-order motion mechanisms (Adelson & Bergen, 1985; van Santen & Sperling, 1985; Watson & Ahumada, 1985). In addition, there has been evidence that different motion mechanisms have different sensitivities to the velocity and luminance contrast of a moving pattern (see, e.g., Hawken, Gegenfurtner, & Tang, 1994; Lu & Sperling, 1995). First-order motion mechanisms are more sensitive to higher velocities and lower contrasts than are higher-order motion mechanisms. Thus, we manipulated these stimulus parameters in order to examine the contribution of underlying motion mechanisms on motion priming that is induced by a spatially separated priming stimulus. 

We found that the strength of motion priming was greatly reduced when the priming and test stimuli were spatially separated under mesopic conditions. The reduction of motion priming was observed irrespective of the stimulus velocity and contrast. Motion priming was observed when the priming and test stimuli temporally overlapped. From these results, we concluded that the deterioration of motion perception that occurs under mesopic vision is due to a mismatch in the temporal characteristics of the cone- and rod-mediated systems that feed into the motion-sensing mechanisms. 

Experiment 1

Methods

Apparatus

The stimuli were generated by MATLAB (The MathWorks, Inc., Natick, MA) with the Psychophysics Toolbox version 3.0 extension (Brainard, 1997; Pelli, 1997) on a computer (MacPro, Apple Inc., Cupertino, CA) and displayed on a 21-in. RGB monitor (SONY GDM F520, Sony Corporation, Tokyo, Japan). The monitor had a frame rate of 120 Hz, a spatial resolution of 1024 × 768 pixels, and 12-bit gray-level resolution. The monitor output was linearized (gamma corrected) under software control. For all experiments using luminance-varying stimuli, the space-averaged chromaticity (CIE 1931) of the display had an x value of 0.31 and a y value of 0.33. Subjects observed the display while their head position was maintained by a chin- and headrest. Patterns were viewed monocularly with the right eye at a viewing distance of 57 cm. The pupil diameter and eye fixation of the right eye of each subject were recorded with a ViewPoint EyeFrame SceneCamera Systems MSE07 (Arrington Research, Inc., Scottsdale, AZ). The sampling rate of this infrared-video-based eye tracker was 60 Hz. Neutral density filters were placed just distal to the right eye in order to obtain three different average luminance levels (48 cd/m², 0.048 cd/m², and 0.0048 cd/m²). The retinal illuminances were computed from the subjects' pupil diameters that were measured under these three luminance levels. Figure 1 presents the averaged retinal illuminances for five subjects. The three retinal illuminances approximated 2.4, −0.1, and −1.1 log photopic Td (log Td). We assumed that these retinal illuminances corresponded to the photopic, mesopic, and scotopic levels, respectively, based on the results of the study by Hood and Finkelstein (1986). At mesopic light levels (0.048 cd/m²), the cones are assumed to be mainly active in the central retina, while rod activity dominates in the peripheral retina (see Raphael & MacLeod, 2011, figure 5. We should note that, in the scotopic level described here, cones would be still active for some subjects whose pupil sizes were larger (Figure 1). The room was darkened and light shielded, with no other source of illumination present. 

Figure 1

 

Three averaged retinal illuminances (2.4, −0.1, and −1.1 log Td) obtained from the pupil measurement (N = 5). These three levels correspond to photopic, mesopic, and scotopic light levels from the highest adaptation levels. The horizontal line represents retinal illuminance. The horizontal error bars represent ±1 standard deviation. The two dashed vertical lines starting at the left are drawn at the cone threshold and at the rod saturation, respectively (based on Hood and Finkelstein, 1986).

Subjects

Five subjects participated in the experiments. Two of them were the authors of this study, and the other three did not know the purpose of the experiments. All had normal or corrected-to-normal vision. All subjects gave informed consent before their inclusion in the study. 

Stimuli

Figure 2 illustrates the schematic descriptions of the stimuli in a single trial. In order to enable comparisons with previous studies of motion priming, we used a stimulus that was similar to that used by Kanai and Verstraten (2005), Pantle et al. (2000), and Takeuchi et al. (2011). An achromatic vertical sine-wave grating was displayed in a rectangular window that measured 19.8H° × 3.3V °. The edges of the stimulus were tapered by a Gaussian function with a sigma value of 2.8°. Because high-spatial-frequency grating may be scarcely detectable under low retinal illuminance (Hess et al., 1990), the spatial frequency of the stimulus was set to 0.5 c/°. The stimulus was presented on a uniform gray-colored background (CIE1931; x = 0.31, y = 0.33), which had a luminance that was the same as the space-averaged luminance of the sine-wave grating. 

Figure 2

 

Schematic descriptions of the stimuli in a single trial. (A) The condition in which the test stimulus was presented at the central visual field (VF) while the position of the priming stimulus was varied. (B) The condition in which the priming stimulus was presented in the central VF while the position of the test stimulus was varied. The spatial distance between the center of the priming stimulus and that of the test stimulus was varied from 0.0° to 10.0°. The black central cross (1.0° × 1.0°) was displayed in order to assist the subjects in maintaining fixation when the grating was presented in the periphery. Direction judgments of the ambiguous test stimulus subsequent to a priming stimulus (presentation duration of 167 ms) under different retinal illuminances were examined. The velocity and the contrast of the stimuli were varied.

The direction of motion of the priming stimulus was either to the right or to the left. Based on our previous study (Takeuchi et al., 2011) and our preliminary observations, the presentation duration of the priming stimulus was set to 167 ms, which induced strong positive priming at photopic levels. The duration at which the transition from positive to negative priming occurred was not fixed but depended highly on the velocity of the priming stimulus (see Takeuchi et al., 2011, figure 7). Positive priming was prominent when the priming stimulus was slower, while negative priming was observed when the priming stimulus was fast. The velocity of the priming stimulus was therefore varied from 2 to 4 Hz, which correspond to a variation from 4.0°/s to 8.0°/s. When the velocity of the priming stimulus was decreased to 1 Hz (2.0°/s) or increased to 5 Hz (10.0°/s) in the preliminary observations, neither positive nor negative priming was reported, and thus these velocities were not used in the main experiment. 

Similar to previous studies (Kanai & Verstraten, 2005; Pantle et al., 2000; Pinkus & Pantle, 1997; Takeuchi et al., 2011), the ambiguous test stimulus was made by shifting the phase of the grating 180°. The spatial frequency was set to 0.5 c/°, which was the same as that of the priming stimulus. In order to equate the velocities of the priming stimulus and the test stimulus, the duration of one frame of the test stimulus was determined based on the velocity of the priming stimulus. It was set to a duration that was equal to that required for the priming stimulus to shift 180°. A total of four frames were presented for the test stimulus. 

The test stimulus was presented immediately after the offset of the priming stimulus. The strength of motion priming is known to be reduced when there is an ISI between the priming and test stimuli (Kanai & Verstraten, 2005). Thus, no ISI was inserted between the priming and test stimulus, in order to make the motion priming stronger. 

We ran two experimental conditions separately. In one condition, the test stimulus was presented in the central visual field and the position of the priming stimulus was varied (Figure 2A). In the other condition, the priming stimulus was presented in the central visual field and the position of the test stimulus was varied (Figure 2B). In the preliminary observations, we collected data from both the upper and lower peripheral retinae. When we equated the effective luminance contrast with the method we describe later, we did not find any systematic differences between the data from the lower and upper retinae. Therefore, we used only the upper region in the main experiment. The spatial distance between the center of a priming stimulus and that of a test stimulus was varied from 0.0° to 10.0°. We confirmed that neither positive nor negative priming was conspicuous when the spatial distance was increased to 13° or more in the preliminary observation. At a spatial distance of 0.0°, both priming and test stimuli were presented at the center. A black fixation cross (1.0° × 1.0°) was displayed in order to assist subjects in maintaining fixation while the priming or test stimulus was presented in the periphery. We checked that the subjects continuously viewed the fixation point by tracking their eye fixations with an eye-tracking device. 

Because the contrast sensitivity of a moving pattern varies depending on the retinal illuminance (see, e.g., Conner, 1982; Hess et al., 1990; Kelly, 1971; Snowden, Hess, & Waugh, 1995; Takeuchi & De Valois, 2000), the appearance of a pattern could be different if its luminance contrast is fixed under different retinal illuminances. For example, if the luminance contrast is low, then the pattern might totally disappear under low retinal illuminance, even though it is clearly seen under high retinal illuminance. Thus, we equated the effective luminance contrast under different retinal-illuminance conditions by measuring direction-discrimination thresholds in advance, as we describe later. The Michelson contrast of the sine-wave gratings in the main experiment was set to multiples of the measured thresholds. Previous studies have suggested that a low-level motion system, such as a first-order motion system, is activated by low-contrast stimuli, while high-contrast stimuli activate both first-order and higher-order motion mechanisms (see, e.g., Takeuchi & De Valois, 1997). Thus, the luminance contrast of the priming and test stimuli was set to 2 or 8 times the direction-discrimination threshold. 

Procedure

Contrast-sensitivity measurements:

In order to equate the appearance of the stimulus in terms of multiples of the threshold contrast for the different retinal illuminances, we measured the contrast sensitivity for the direction discrimination of the moving sine-wave gratings for each velocity, each retinal illuminance, and each eccentricity. The presentation duration of the moving stimulus was 167 ms, which was the same as that of the priming stimulus that was used in the main experiment. Subjects judged the perceived motion direction of the stimulus with a two-alternative forced choice (leftward or rightward). The onset of each stimulus was marked by an auditory cue. The fixation cross was displayed in order to assist subjects in maintaining fixation while the stimulus was presented in the periphery. No feedback was given. The contrast of the stimulus was varied with a staircase algorithm that was designed to converge to a 79% correct level (Levitt, 1971). Contrast was decreased after three consecutive correct responses and increased after one wrong response. The size of the contrast increments or decrements decreased as the staircase depth increased; it was 0.4 log unit in the beginning and fell to a terminal value of 0.1 log unit. The threshold for a given staircase run was computed as the mean of the contrast of the final three out of six turning points. Similar measurements were done for each subject at each retinal illuminance, retinal eccentricity, and velocity. 

Direction judgment of the ambiguous test stimulus:

In the main experiment, the priming stimulus was displayed 500 ms after a beep, which signaled the start of each trial. The presentation duration of the priming stimulus was 167 ms. The directionally ambiguous test stimulus was presented after termination of the priming stimulus without any ISI (Figure 2). The subjects' task was to indicate the perceived direction of the test stimulus by pressing the 4 key (leftward) or 6 key (rightward) on the keyboard. The subjects were instructed to continuously view the fixation point through the trial. After the button press, a 1-s intertrial interval, in which a uniform field with space-averaged luminance was displayed, was inserted in order to reduce the effect of the former trial. 

As shown in Figure 2, we ran two experimental conditions separately. Their difference was whether the fixed presentation location was that of the test stimulus (Figure 2A) or the priming stimulus (Figure 2B). In the first condition, when the test stimulus was presented in the center of the visual field, each session consisted of 64 trials: eight trials for each of the four spatial distances between the priming and the test stimuli (0.0°, 3.3°, 6.7°, and 10.0°) and for the two directions of the priming stimulus (rightward and leftward), which were presented in random order. Three retinal illuminances (2.4, −0.1, or −1.1 log Td), three velocities (2, 3, or 4 Hz), and two contrasts (2 or 8 time the direction-discrimination threshold that was measured beforehand) were examined. In each session, retinal illuminance, velocity, and the contrast of the priming stimulus were fixed. Each subject completed two sessions for each of the retinal illuminances, velocities, and contrasts. The velocity and contrast of the stimuli were varied in random order between sessions for each subject. Subjects were initially dark-adapted for 30 min prior to the task. We always started the experiment from the darkest adapting levels. Subjects underwent at least 20 practice trials in each condition prior to the actual data acquisition. 

In the second condition, in which the priming stimulus was presented in the center of the visual field (Figure 2B), we replicated the first experimental condition (Figure 2A) except that we did not run the condition of the velocity of 3 Hz. The same subjects participated in this experiment. 

Results

Contrast-sensitivity measurements

Figure 3 shows the direction-discrimination threshold of the moving sine-wave grating for the five subjects at each velocity and retinal illuminance. The percentage-contrast threshold is plotted as a function of the spatial distance from the fixation point in degrees. The contrast threshold increased as retinal illuminance decreased. While there was a tendency for the threshold to increase as the distance from the fixation point increased at photopic light levels, such a tendency was not observed for lower retinal illuminances. 

Figure 3

 

Averaged data of the contrast thresholds that were obtained from direction-discrimination measurements of the five subjects. The contrast threshold is plotted as a function of the spatial distance of the moving stimulus from the fixation point. (A) The velocity of the stimulus was 2 Hz. (B) The velocity of the stimulus was 3 Hz. (C) The velocity of the stimulus was 4 Hz. The error bars represent ±1 standard deviation. Each curve represents the data that were collected under different retinal illuminances (2.4, −0.1, or −1.1 log Td). At a spatial distance of 0.0°, the stimulus was presented in the central visual field.

In the main experiment, we multiplied the direction-discrimination threshold value (2× or 8× thresholds) in order to equate the effective luminance contrast of the stimuli under different conditions. However, under the lowest retinal illuminance examined (−1.1 log Td), the threshold value was so high that the 8× threshold contrast exceeded 100%. Thus, the contrast of the stimulus at this condition was set to 2 times the threshold. In the other conditions, the contrast was set to 2× or 8× thresholds. 

Direction judgments in the central visual field

The number of trials in which subjects looked more than 1.5° away from the fixation point through a single trial was less than 1%. Thus, excluding the data from these trials did not change the results and conclusions. We therefore used data from all of the trials for the subsequent analysis. Figure 4 shows the results of the direction judgments of the test stimuli for the five subjects at each velocity, contrast, and retinal illuminance. The percentage response to positive motion priming was plotted as a function of the spatial distance between the priming and test stimuli in degrees. Thus, when more than 50% of the responses were positive motion priming, subjects reported that the perceived direction of the test stimulus was in the same direction as that of the priming stimulus in the majority of the trials. When fewer than 50% of the responses were scored as positive priming, subjects reported that the motion of the test stimulus was in the direction opposite to the priming stimulus (negative priming) in the majority of the trials. 

Figure 4

 

Averaged data for the five subjects of the direction judgments of the test stimuli that were presented in the central visual (Figure 2A). In each graph, the percentage response of positive priming (motion of test stimulus in the same direction as the priming stimulus) is plotted as a function of the spatial distance between the priming and test stimuli in degrees. The error bars represent ±1 standard error of the mean. Each curve represents the data that were collected under different retinal illuminances (2.4, −0.1, or −1.1 log Td). (A–C) The luminance contrast was set to 8× the direction-discrimination threshold. (D–F) The luminance contrast was set to 2× the direction-discrimination threshold. The velocity of the stimulus was 2 Hz [(A) and (D)] 3 Hz [(B) and (E)], or 4 Hz [(C) and (F)].

At the 8× threshold contrast, a two-way ANOVA showed that, at the velocity of 2 Hz (Figure 4A), the interaction between retinal illuminance and spatial distance between the priming and test stimuli was significant, F(3, 12) = 8.93, p < 0.01. At the velocity of 3 Hz (Figure 4B), the interaction between retinal illuminance and spatial distance was significant, F(3, 12) = 5.94, p < 0.05. At the velocity of 4 Hz (Figure 4C), the interaction between retinal illuminance and spatial distance was not significant, F(3, 12) = 0.29, not significant (ns). The main effects of retinal illuminance and spatial distance were significant, F(1, 4) = 23.15, p < 0.01 for the retinal illuminance, F(3, 12) = 33.50, p < 0.001 for the spatial distance. 

At the 8× threshold contrast (Figure 4A through C), when both the priming and test stimuli were presented at the same location in the central visual field (spatial distance: 0.0°), positive motion priming was observed in most of the trials under photopic conditions, which replicated the previous results that were reported by Kanai and Verstraten (2005), Pantle et al. (2000), Pavan et al. (2009), and Takeuchi et al. (2011). In addition to this, we found that positive motion priming was perceived under mesopic conditions at a similar frequency as that observed under photopic conditions. 

When the priming stimulus was presented in the periphery (spatial distance: 3.3°, 6.7°, or 10.0°), the perception of visual motion priming depended on the retinal illuminance and velocity. At the velocity of 2 Hz, positive motion priming was perceived in more than 90% of the trials, whereas neither positive nor negative priming was reported under mesopic conditions. As the velocity increased, the percentage response to negative priming increased for the photopic and mesopic conditions. At 4 Hz, negative priming was dominant under all retinal illuminances. However, we should note that negative priming was more conspicuous in the photopic conditions than in the mesopic conditions. 

At the 2× threshold contrast, a two-way ANOVA showed that, at the velocity of 2 Hz (Figure 4D), the interaction between retinal illuminance and spatial distance between the priming and test stimuli was not significant, F(6, 24) = 0.72, ns. The main effect of retinal illuminance was not significant, F(2, 8) = 1.61, ns, while that of spatial distance was significant, F(3, 12) = 36.58, p < 0.001. At the velocity of 3 Hz (Figure 4E), the interaction between retinal illuminance and spatial distance was not significant, F(6, 24) = 1.16, ns. The main effect of retinal illuminance was not significant, F(2, 8) = 1.71, ns, while that of spatial distance was significant, F(3, 12) = 26.39, p < 0.001. At the velocity of 4 Hz (Figure 4F), the interaction between retinal illuminance and spatial distance was not significant, F(6, 24) = 2.04, ns. The main effect of retinal illuminance was not significant, F(2, 8) = 0.97, ns, while that of spatial distance was significant, F(3, 12) = 25.60, p < 0.001. 

At the 2× threshold contrast (Figure 4D through F), when both the priming and test stimuli were presented in the central visual field (spatial distance: 0.0°), positive motion priming was perceived in nearly 90% of the trials, which was similar to the results at the 8× threshold contrast. When the priming stimulus was presented in the periphery (spatial distance: 3.3°, 6.7°, or 10.0°), negative priming became more conspicuous irrespective of the velocity of the priming stimulus, and no statistical difference was found among the three retinal illuminances. 

As described in the Introduction, we predicted that the strength of motion priming under mesopic conditions would be reduced when both the priming and test stimuli were separately presented in the center and periphery. We actually found a decline in the strength of the motion priming at mesopic light levels under conditions in which the positive priming was dominant at photopic levels (Figure 4A and B). Although negative priming was perceived at mesopic levels in Figure 4C through F, careful examination of the data showed that the percentage response of negative priming at mesopic levels was less than that perceived at the other two light levels. We discuss this point later in this section when we discuss Figure 7, in which the data of Figure 4 are replotted. 

Direction judgments in the peripheral visual field

We examined the effects of motion priming when the priming stimulus was presented in the center of the visual field while the spatial location of the test stimulus was varied (Figure 2B). At an 8× threshold contrast, a two-way ANOVA showed that, at a velocity of 2 Hz (Figure 5A), the interaction between retinal illuminance and spatial distance between the priming and test stimuli was significant, F(3,12) = 4.46, p < 0.05. At a velocity of 4 Hz (Figure 5B), the interaction between retinal illuminance and spatial distance was not significant, F(3, 12) = 2.51, ns. The main effects of retinal illuminance and spatial distance were significant, F(1, 4) = 9.68, p < 0.05 for the retinal illuminance, F(3, 12) = 19.21, p < 0.001 for the spatial distance. At a 2× threshold contrast, a two-way ANOVA showed that, at a velocity of 2 Hz (Figure 5C), the interaction between retinal illuminance and spatial distance was significant, F(6, 24) = 2.84, p < 0.05. At a velocity of 4 Hz (Figure 5D), the interaction between retinal illuminance and spatial distance was significant, F(6, 24) = 2.76, p < 0.05. 

Figure 5

 

Averaged data for the five subjects of direction judgments of the test stimulus in the peripheral visual field (Figure 2B). In each graph, the percentage response of positive priming (motion of the test stimulus in the same direction as the priming stimulus) is plotted as a function of the spatial distance between the priming and test stimuli in degrees. The error bars represent ±1 standard error of the mean. Each curve represents the data that were collected under different retinal illuminances (2.4, −0.1, or −1.1 log Td). Luminance contrast was set to 8× the direction-discrimination threshold [(A) and (B)] or 2× the threshold [(C) and (D)]. The velocity of the stimulus was 2 Hz [(A) and (C)] or 4 Hz [(B) and (D)].

When both priming and test stimuli were presented at the same location in the central visual field (spatial distance: 0.0°), the subjects reported positive motion priming for nearly 90% of the trials under all of the conditions. When the test stimulus was presented in the periphery (spatial distance: 3.3°, 6.7°, or 10.0°), the frequency of the perception of motion priming at mesopic levels was greatly diminished and thus the percentage response converged to 50%. As especially shown in Figure 5A and D, no motion priming was observed under mesopic conditions, while negative priming was dominant under photopic and scotopic conditions. 

In order to further examine the results in mesopic conditions, we replotted the data of Figure 5 in Figure 6, in which the percentage of positive priming was plotted as a function of retinal illuminance. The data for the conditions when the priming and test stimuli were presented at the same location in the central area (spatial distance: 0.0°) were omitted from the graphs because the strength of the priming was nearly invariant with retinal illuminance. The percentage of positive priming was closer to 50% at mesopic levels (−0.1 log Td) than at photopic (2.4 log Td) or scotopic (−1.1 log Td) levels. This tendency was shown irrespective of the velocity and contrast of the stimulus. 

Figure 6

 

Replotted data from Figure 5. The percentage of positive motion priming was plotted as a function of retinal illuminance. (A) through (D) correspond to Figure 5A−D, respectively. Error bars represent ±1 standard error of the mean. Each curve represents the data that were collected at different spatial distances between the priming and test stimuli (3.3°, 6.7°, or 10°). The data that were collected when both priming and test stimuli were presented in the central visual field (spatial distance: 0.0°) were omitted from this figure.

In addition, we replotted the data of Figure 4 in order to examine whether a similar tendency would be seen for the results of the first experiment. Figure 7A through D was made from the data of Figure 4A, C, D, and F. Thus, the experimental parameters for each graph in Figure 7 correspond to those in Figure 6. At mesopic levels, the strength of the motion priming was reduced in Figure 7, although it was not as prominent as that shown in Figure 6. These results indicate that the effects of the priming stimulus were weakened (but did not completely disappear) in most of the cases at mesopic levels when the test stimulus was presented at the center (Figure 2A). The results shown in Figure 7A appear to differ from those shown in Figure 6 and the other graphs of Figure 7. However, the difference was that either positive or negative priming was perceived at photopic levels (2.4 log Td). We speculate that these apparent differences between Figures 6 and 7 can be explained by the type of underlying motion-detection mechanisms. We will discuss these matters in the Discussion section. 

Figure 7

 

Replotted data from Figure 4. The percentage of positive motion priming was plotted as a function of retinal illuminance. (A) through (D) correspond to Figure 4A, C, D, and F, respectively. The error bars represent ±1 standard error of the mean. Each curve represents the data that were collected at different spatial distances between the priming and test stimuli (3.3°, 6.7°, or 10°). The data that were collected when both the priming and test stimuli were presented in the central visual field (spatial distance: 0.0°) were omitted from this figure.

In summary of the present findings, when the priming and test stimuli were separately presented in the center and periphery, the strength of motion priming was diminished at mesopic levels. A decrease in the strength of motion priming was observed both when the perceived direction of the test stimulus was judged to be in the center and when it was judged in the periphery, although the decrease was more prominent in the latter case. 

Discussion

Our prediction was that the strength of the motion priming would be reduced under mesopic conditions if the coactivity of rods and cones induces detrimental effects on motion integration (Billino et al., 2008). We found that, when the priming and test stimuli were separately presented in the center and periphery, the effects of the priming stimulus were greatly reduced at mesopic levels, while positive or negative priming was perceived at both photopic and scotopic levels. 

Before discussing the weakening of motion priming under mesopic conditions, which was the main subject of this study, we need to note the underlying mechanisms of motion priming. We found that the perceived direction of motion priming depended on the velocity and the contrast of the stimulus. For example, as shown in Figure 4A and C, increasing the velocity of the stimulus reversed the perceived direction of motion priming, from a positive to a negative direction. Previous studies have indicated that positive and negative priming are induced by different motion mechanisms (see, e.g., Kanai & Verstraten, 2005; Pantle et al., 2000). We will discuss this matter first. 

Motion mechanisms responsible for visual motion priming

When both the priming and test stimuli were presented in the central visual field, positive motion priming was prominent irrespective of the retinal illuminance, velocity, and contrast of the stimulus. However, when the priming and test stimuli were separately presented in the center and periphery, positive motion priming was observed under very limited conditions in which the test stimulus was presented at the center, the velocity of the priming stimulus was low, the contrast of the priming stimulus was high, and the retinal illuminance was high enough to activate the cone system (Figures 4A and 7A). In other conditions, negative priming was dominant except at mesopic light levels. This finding was consistent with the remark by Pantle et al. (2000) that negative priming is a more robust phenomenon than positive priming. Based on this suggestion, we will discuss the underlying mechanisms of negative motion priming first. 

As mentioned in the Introduction, it has been shown that the contrast sensitivity of a first-order motion system is relatively higher than that of other motion mechanisms (Dosher, Landy, & Sperling, 1989; Lu & Sperling, 1995; Nishida, 1993; Smith et al., 1994; Solomon & Sperling, 1994; Sperling, 1989; Takeuchi & De Valois, 1997). Takeuchi and De Valois (1997) found that the perceived direction of a two-frame sinusoidal grating that is separated by an ISI is predicted by a first-order motion model that was designed by Adelson and Bergen (1985) when the contrast of the stimulus is as low as the 3× direction-discrimination threshold, but the inclusion of a feature-tracking mechanism is also suggested when the contrast is as high as 8× threshold. Furthermore, the relative contribution of a first-order motion mechanism has been shown to be larger in the periphery than in the central retina (see, e.g., Smith et al., 1994; Takeuchi & De Valois, 2009). In addition, a plausible candidate for a directionally selective motion detector that is sensitive to high velocity is energy based (see, e.g., Burr & Ross, 1982; Burr, Ross, & Morrone, 1986; Lappin, Tadin, Nyquist, & Corn, 2009; Lu & Sperling, 1995). Meanwhile, we showed that negative priming was prominent when the stimulus contrast was low, the stimulus velocity was high, and the test stimulus was presented in the periphery. We suggest that a low-level motion mechanism, such as a first-order motion mechanism, was responsible for the induction of the negative priming. 

Neurophysiological studies have shown that a moving stimulus with a very short duration, such as several hundred milliseconds, is enough to change the adaptation status of directionally selective neurons that are located in V1 or MT (Lisberger & Movshon, 1999; Priebe, Churchland, & Lisberger, 2002). Psychophysical studies have indicated that the rapid adaptation of directionally selective neurons is an underlying neural mechanism of negative motion priming (Pantle et al., 2000; Pavan et al., 2009) or rapid-type motion aftereffects (Glasser, Tsui, Pack, & Tadin, 2011; Kanai & Verstraten, 2005). Duffy and Hubel (2007) recorded the responses from V1 cells in primates and showed that directional selectivity is invariant under different retinal illuminances from photopic to scotopic conditions. They argued that the spatiotemporal center-surround organization of V1 cells does not vary as retinal illuminance decreases. This is consistent with our observations of negative priming under both high and low retinal illuminances. 

If negative priming is induced by an energy-based directionally selective system, such as a first-order motion mechanism, the mechanism responsible for the positive priming would be different from the one that induces negative priming because the two priming effects are observed antagonistically (Pantle et al., 2000; Takeuchi et al., 2011). If so, a higher-order motion system, such as a feature-tracking mechanism or a third-order motion mechanism (Bowns, 2002; Cavanagh, 1992, 1994; Dawson, 1991; Del Viva & Morrone, 1998; Derrington, Allen, & Delicato, 2004; Lu & Sperling, 1995; Seiffert & Cavanagh, 1998; Ullman, 1979), could be a candidate. For feature-tracking mechanisms or third-order motion mechanisms, spatial localization of the prominent visual features is crucial for tracking the moving pattern. Stimulus manipulations, such as reductions in the stimulus contrast, increases in the velocity, reductions in the retinal illuminance, increases in the spatial distance between the priming and test stimulus, or changes in the location of the test stimulus in the peripheral visual field, must be a disadvantage for the spatial localization of features. For example, it has been reported that positional acuity is degraded under low retinal illuminance (Livingstone & Hubel, 1994). 

Our findings that prominent positive priming was observed when both priming and test stimuli were presented in the central visual field (Figures 4 and 5) and when they were separately presented under photopic conditions at 2 Hz velocity and 8× threshold contrast (Figure 4A) seem to support our hypothesis that a feature-tracking mechanism induces positive priming. 

If positive and negative priming are induced by separate visual motion mechanisms that function antagonistically, the apparent differences in Figure 7A through D can be explained; when the contribution of the feature-tracking system becomes larger (e.g., at low velocity and at high contrast under cone vision), positive priming prevails (Figure 7A). Negative priming becomes dominant in other conditions in which motion perception continued to depend on a first-order motion mechanism (Figure 7B through D). 

Reason for the reduction in motion priming under mesopic conditions

Keeping in mind all of the foregoing, we now return to the main subject of this article. When the priming and test stimuli were separately presented in the cone-mediated central and rod-mediated peripheral visual fields, the strength of the motion priming was reduced under mesopic conditions. As Billino et al. (2008) have suggested, the different spatiotemporal characteristics of the cone-mediated and rod-mediated systems induce a mismatch in information during the integration of priming and test stimuli, which could lead to a reduction of priming. In the final part of this section, we discuss the three following possible explanations for the mismatch of information that reduces motion priming under mesopic conditions: (a) the cancellation of motion signals from different types of motion detectors, (b) a mismatch of the perceived velocities of the priming and test stimuli, and (c) a temporal difference between the cone- and rod-generated signals. We suggest that the third explanation is the most plausible for our results of visual motion priming. 

Explanation 1: Cancellation of motion signals under mesopic conditions

When the priming stimulus was presented in the periphery and the test stimulus was presented at the center, the positive priming that was perceived under photopic conditions was greatly diminished under mesopic conditions (Figure 7A). Under scotopic conditions, only negative priming was perceived. As described previously, we assumed that the positive priming was induced by a higher-order motion system, such as a feature-tracking mechanism, while the negative priming was induced by a low-level energy-based motion mechanism. If the contributions of the two motion mechanisms were similar at some intermediate light levels, then the strength of the motion priming might be reduced because of the possible cancellation of the leftward-direction signal and the rightward-direction signal from these motion mechanisms. Even though this explanation is intuitively appealing and plausible for explaining the data in Figure 7A, it cannot reconcile with other results, such as those shown in Figure 6 and Figure 7B through D. Here, motion priming was greatly reduced at mesopic levels while negative priming was dominant at both photopic and scotopic levels. There was no reason to assume that the leftward and rightward direction signals were cancelled out. Thus, a cancellation of the different motion-direction signals that were induced by the different motion mechanisms, even if it existed, could not be the whole story for explaining the specific reduction in the strength of the motion priming under mesopic conditions. 

Explanation 2: Mismatch of velocity perceptions at different retinal eccentricities

Incongruent perceived velocities at different retinal eccentricities might reduce the strength of motion priming. Billino et al. (2008) discussed how, at mesopic light levels, the mismatch of rod- and cone-mediated velocity information exerts a detrimental effect on the analysis of temporal dynamics so that it becomes more difficult to extract the biological motion structure. In this study, because we separately presented the priming and test stimuli in the cone-dominant central and rod-dominant peripheral visual fields under mesopic conditions, a mismatch in the perceived velocities of the priming and test stimuli may have occurred. This possible mismatch of velocity perceptions could have made the effects of motion priming less strong in mesopic conditions. We tested this possibility in Experiment 2. 

Explanation 3: Temporal difference between rod- and cone-generated signals

As has been shown in several attempts to determine the mesopic luminous efficiency function as a sum of the weighted rod and cone components (see, e.g., Goodman et al., 2007; Ikeda & Shimozono, 1981; Palmer, 1966, 1967, 1968; Sagawa & Takeichi, 1992; Trezona, 1991), visual perceptions under mesopic vision appear to be extracted by the integration of rod- and cone-mediated signals. Our third explanation was based on the differences in the response characteristics between the cone and rod systems, which feed into motion-detection mechanisms. 

According to Raphael and MacLeod (2011) and in our mesopic conditions (0.048 cd/m²), cones are assumed to operate in the central retina and rods in the peripheral retina. Thus, visual inputs that were separately given to the cone and rod systems were not properly integrated, which might have induced the reduction in the strength of motion priming. Some subjects, including both authors, had the impression that the test stimulus that was presented subsequent to the priming stimulus was moving smoothly under photopic and scotopic conditions, but perceived it as a mere flicker under mesopic conditions. These impressions suggest that each priming stimulus and test stimulus was perceived as independently moving stimuli as a consequence of the weak or incomplete integration between cone- and rod-mediated signals. 

The substantial differences in the temporal properties of cone and rod receptors themselves and their postreceptor pathways are well-known (see, e.g., Baylor, 1987; Buck, 2004; MacLeod, 1972; Sharpe & Stockman, 1999). The temporal response of the visual system becomes slower as retinal illuminance decreases and as rods become more active (Burr & Morrone, 1993; Hess, 1990; Hess, Waugh, & Nordby, 1996; Kelly, 1971; Snowden et al., 1995; Swanson, Ueno, Smith, & Pokorny, 1987). It has been estimated that the temporal response under rod vision is about 80 ms slower than that under cone vision (MacLeod, 1972; Plainis & Murray, 2000; Stockman & Sharpe, 2006; Walkey, Harlow, & Barbur, 2006). Transmission delays that are based on retinal illuminance have been reported to modify the perceptions of motion direction itself. In the experiment using ISI reversal (Takeuchi & De Valois, 2009), motion reversal at an ISI of about 30 ms was most prominent at photopic levels, while it was about 100 ms at scotopic levels. Therefore, the induction of motion reversal under rod vision was delayed about 70 ms, which nearly corresponds to the known delay of the temporal response in the rod system. We assumed that this kind of delay in the rod system resulted in difficulty in integrating motion information and in reduction of the motion priming, which was accomplished by integrating the motion information of priming and test stimuli. We tested this possibility in Experiment 3. 

Experiment 2

It has been reported that velocity perception varies between cone-mediated and rod-mediated vision (see, e.g., Gegenfurtner et al., 2000; Hammett et al., 2007; Peterson, Ohzawa, & Freeman, 2001; Vaziri-Paskham & Cavanagh, 2008). In our mesopic conditions, we assumed that vision in the central retina is based on cone activity and in the peripheral retina mainly based on rod activity (Raphael & MacLeod, 2011). When the priming and test stimuli were separately presented in the center and periphery, a possible mismatch of velocity perceptions between the priming and test stimuli could have made the effects of motion priming less strong in mesopic conditions. We tested this possibility in Experiment 2. 

Methods

Stimuli

As in Experiment 1, we examined the manner via which the preceding moving grating modulates the perceived direction of the 180° phase-shifted test grating. Subjects judged the perceived directions of the test stimuli presented subsequent to the priming stimulus in the periphery (Figure 2B). The spatial distance between the priming and test stimuli was set to 10.0°. The velocity of the test stimulus was set to −30%, −20%, −10%, 0%, or 10% of the velocity of the priming stimulus, and it was moved at 4 Hz. Some studies have suggested that velocity is overestimated under low retinal illuminance (Hammett et al., 2007; Peterson et al., 2001; Pritchard & Hammett, 2012; Vaziri-Paskham & Cavanagh, 2008), while others have argued that velocity is perceived as slower under rod vision than under cone vision (Gegenfurtner et al., 2000). We therefore either reduced or increased the velocity of the test stimulus relative to that of the priming stimulus. The direction judgments of the test stimuli were examined under two retinal illuminances (2.4 or −0.1 log Td) at two contrasts (2× or 8× threshold contrast). 

Procedure

As described in the subsection “Direction judgment of the ambiguous test stimulus” for Experiment 1, the priming stimulus was displayed 500 ms after a beep that signaled the start of each trial. The presentation duration of the priming stimulus was 167 ms. The directionally ambiguous test stimulus was immediately presented after termination of the priming stimulus. Subjects were asked to judge whether the perceived direction of the test stimulus was leftward or rightward. Each session consisted of 150 trials: 15 trials for each of the five velocities of the test stimulus (−30%, −20%, −10%, 0%, and 10%) and for the two directions of the priming stimulus (rightward and leftward), which were presented in random order. Two retinal illuminances (2.4 and −0.1 log Td) and two contrasts (2× or 8× the direction-discrimination threshold that was measured in Experiment 1) were examined. In each session, the retinal illuminance and the contrast of the priming stimulus were fixed. Each subject completed one session for each of the retinal illuminances and contrasts. The contrast of the stimuli was varied in random order between sessions for each subject. Subjects were initially dark-adapted for 30 min prior to the task. We always started the experiment from the darkest adapting levels. The subjects included in Experiment 1, with the exception of one subject who did not know the purposes of the experiment, participated in this experiment. 

Results and discussion

Figure 8 shows the results of the averaged responses for the four subjects. If the difference in the perceived velocities between the priming and test stimuli reduces the strength of motion priming, subjects might report priming at mesopic levels (−0.1 log Td) when the perceived velocities of both stimuli match. However, the obtained functions were nearly flat, as shown in Figure 8. At an 8× threshold contrast (Figure 8A), a two-way ANOVA showed that the interaction between retinal illuminance and velocity was not significant, F(4, 12) = 0.42, ns. The main effect of retinal illuminance was significant, F(1, 3) = 15.26, p < 0.05, while that of the velocity of the test stimulus was not significant, F(4, 12) = 0.45, ns. At a 2× threshold contrast (Figure 8B), a two-way ANOVA showed that the interaction between retinal illuminance and velocity was not significant, F(4, 12) = 0.07, ns. The main effect of retinal illuminance was significant, F(1, 3) = 22.14, p < 0.05, while that of the velocity of the test stimulus was not significant, F(4, 12) = 0.22, ns. Thus, a mismatch of velocity perceptions between the priming and the test stimuli, even if it existed, was not a factor in the decrease in the strength of motion priming at mesopic levels. Furthermore, we should note that irrespective of the velocity difference or the contrast of the priming stimulus, no motion priming was reported under mesopic conditions (−0.1 log Td), while negative priming was prominent under photopic conditions (2.4 log Td). These results are consistent with our findings shown in Figures 5 and 6. 

Figure 8

 

Averaged data for the four subjects in Experiment 2. In each graph, the percentage response of positive priming (motion of the test stimulus in the same direction as the priming stimulus) is plotted as a function of the rate of change of the velocity of the test stimulus. The spatial distance between the priming and test stimuli was set to 10.0°. Each curve represents the data that were collected under two retinal illuminances (2.4 or −0.1 log Td). The error bars represent ±1 standard error of the mean. (A) The contrast was set to 8× the direction-discrimination threshold. (B) The contrast was set to 2× the threshold.

Experiment 3

When the priming stimulus was presented in the periphery and the test stimulus was presented at the center under mesopic conditions (Figure 2A), the processing of the test stimulus by the visual system might have started before the processing of the priming stimulus was finished, because of the delays in the rod system. In contrast, when the priming stimulus was presented at the center and the test stimulus was presented in the periphery (Figure 2B), a maximum 80-ms delay between the offset of the priming stimulus and the onset of the test stimulus would be produced by the slow rod system. In both cases, a loss in the proper timing between the priming and test stimuli could interfere with motion priming under mesopic conditions. 

We found that motion priming was perceived under photopic and scotopic conditions, and it was perceived under mesopic conditions when both the priming and test stimuli were presented in the central visual field. These results support this explanation, because either the cones or rods almost solely operated in all of these conditions. Note that the reduction in motion priming under mesopic conditions was more prominent when the test stimulus was presented in the periphery (Figure 6) than when it was presented at the center (Figure 7). Because the duration of the priming stimulus was set to 167 ms, the motion information of the first 80 ms of the priming stimulus could be transmitted to the next hypothetical stage, where the signals from the priming stimulus that were processed by the rod system and the signals from the test stimulus that were processed by the cone system are integrated, when the direction judgment of the test stimulus was examined at the central visual field (Figure 2A). The priming was predicted to be perceived in this case, even though its effects were weak (Figures 4 and 7). However, when the direction judgments of the test stimulus were examined in the periphery (Figure 2B), the priming and the test stimuli were temporally separated by the slow rod system. 

The effect of the ISI when both the priming and test stimuli were presented in the central visual field has been shown to reduce the priming effect (Kanai & Verstraten, 2005). Although the effects of the ISI (or temporal separation) when there is a spatial distance between the priming and test stimuli are not known, the ISI could have a detrimental effect on motion priming in a similar way. Presenting the test stimulus before the offset of the priming stimulus, to compensate for the presumed ISI induced by the processing delay of the rod pathway under mesopic conditions, would increase the frequency of motion priming compared to that observed in Figures 6 and 7. We tested this possibility in Experiment 3. 

Methods

Stimuli

As in Experiment 1, we examined the manner via which the preceding moving grating modulates the perceived direction of the 180° phase-shifted test grating. Stimulus configuration was similar to that shown in Figure 2B, with the exception that the timing of the onset of the test stimulus varied. The priming stimulus was presented in the center, whereas the test stimulus was presented in the periphery. The spatial distance between the priming and test stimuli was set to 10.0°. The onset timing of the test stimulus was determined by the overlap time between the test stimulus and the priming stimulus, which varied from 0.0 to 83.3 ms in five steps (0.0, 8.3, 16.7, 41.7, and 83.3 ms). Figure 9 shows the schematic representation of the timing relationship between the priming and test stimuli. When the overlap time was equal to zero, the test stimulus appeared soon after the offset of the priming stimulus, as in the previous experiments. When the overlap time was larger than zero, the test stimulus appeared before the offset of the priming stimulus, as shown in Figure 9. The largest overlap time examined, 83.3 ms, was close to the estimated value of the maximum delay of visual processing under scotopic conditions (see, e.g., Stockman & Sharpe, 2006). We aimed to clarify whether the frequency of motion priming increases as the overlap time increases under mesopic conditions. The velocity of the priming and test stimuli was 2 or 4 Hz. The contrast of the stimulus was 2× or 8× the direction-discrimination thresholds. The priming and test stimuli were observed under photopic (2.4 log Td) or mesopic (−0.1 log Td) conditions. 

Figure 9

 

Schematic representation of the timing relationship between the priming and test stimuli used in Experiment 3. The horizontal and vertical axes represent time and contrast, respectively. The overlap time of the priming and test stimuli varied from 0.0 to 83.3 ms. The presentation duration of the priming stimulus was 167 ms.

Procedure

As described in Experiment 1, the priming stimulus was displayed 500 ms after a beep that signaled the start of each trial. The presentation duration of the priming stimulus was 167 ms. Subjects were asked to judge whether the perceived direction of the test stimulus was leftward or rightward. Each session consisted of 150 trials: 15 trials for each of the five overlap times of the priming and test stimuli (0.0, 8.3, 16.7, 41.7, and 83.3 ms) and for the two directions of the priming stimulus (rightward and leftward), which were presented in random order. In each session, retinal illuminance, velocity, and the contrast of the priming stimulus were fixed. Two retinal illuminances (2.4 or −0.1 log Td), two velocities (2 or 4 Hz), and two contrasts (2× or 8× threshold contrast) were examined. The velocity and contrast of the stimuli were varied in random order between sessions for each subject. Subjects were initially dark-adapted for 30 min prior to the task. We always started the experiment from the darkest adapting levels. The subjects included in Experiment 2 participated in this experiment. 

Results and discussion

Figure 10 shows the results of the averaged responses of the four subjects to each retinal illuminance. As shown in Figure 10A, the functions gradually decreased from 50% as the overlap time between priming and test stimuli increased. When the overlap time was zero, the data suggest that no priming was present. However, when the overlap time was greater than 40 ms, subjects reported negative priming in more than 70% of the trials. We performed a two-way ANOVA using the overlap time and the stimulus parameters (velocity and contrast) as factors. At mesopic levels (Figure 10A), the two-way ANOVA showed that the interaction between overlap time and stimulus parameters was not significant, F(12, 36) = 1.38, ns. The main effect of overlap time was significant, F(4, 12) = 7.85, p < 0.01, while that of the stimulus parameters was not significant, F(3, 9) = 3.02, ns. These results are consistent with our conjecture that a certain amount of delay in the rod-dominant peripheral retina induces a factor in the decrease in the strength of motion priming at mesopic levels. 

Figure 10

 

Averaged data for the four subjects in Experiment 3. In each graph, the percentage response of positive priming (motion of the test stimulus in the same direction as the priming stimulus) is plotted as a function of the overlap time of the priming and test stimuli. The spatial distance between the priming and test stimuli was set to 10.0°. Each curve represents the data for the different stimulus-parameter combinations (velocity and contrast). The error bars represent ±1 standard error of the mean. (A) Data obtained when the retinal illuminance was −0.1 log Td (mesopic condition). (B) Data obtained when the retinal illuminance was 2.4 log Td (photopic condition).

At photopic levels (Figure 10B), irrespective of the overlap time, negative priming was reported in the majority of trials. No interaction was observed between overlap time and stimulus parameters (velocity and contrast), F(12, 36) = 1.35, ns. The main effect of overlap time was not significant, F(4, 12) = 0.27, ns, while that of the stimulus parameters was significant, F(3, 9) = 6.09, p < 0.05. The different characteristics of the priming effect observed between mesopic and photopic conditions further support our conjecture that the temporal-response characteristic of the rod pathway influences the perceived direction of the test stimulus. 

General discussion

The summary of our findings includes the following points: 

1.  
   When both priming and test stimuli were presented in the central visual field, positive priming was perceived irrespective of the retinal illuminance, velocity, and contrast of the priming stimulus (Figures 4 and 5). This does not contradict the results of the report of Takeuchi et al. (2011), who found that positive priming is greatly diminished under low retinal illuminance, because they presented the stimulus in the lower temporal retina and not in the central visual field.
2.  
   When the priming stimulus was presented in the periphery and the test stimulus was presented at the center (Figure 2A), the strength of the priming under mesopic conditions was weaker than that observed in most cases under photopic or scotopic conditions (Figure 7).
3.  
   When the priming stimulus was presented at the center and the test stimulus was presented in the periphery (Figure 2B), the strength of the motion priming was greatly reduced under mesopic conditions, while negative priming was dominant irrespective of the velocity and contrast of the priming stimulus under photopic and scotopic conditions (Figure 6).
4.  
   We found that a manipulation of up to 30% of the velocity differences between the priming and test stimuli did not influence the perception of motion priming (Figure 8). Negative motion priming was perceived under photopic levels, while no motion priming was observed under mesopic levels, irrespective of the velocity difference.
5.  
   When the overlap time of the priming and test stimuli was greater than about 40 ms, negative priming was observed in the majority of the trials under mesopic conditions (Figure 10A).

These results seem to support our Explanation 3 described in the “Discussion” subsection for Experiment 1, which suggests that the incompleteness of the integration of rod- and cone-mediated signals that originated from different retinal eccentricities caused the deterioration of motion perception under mesopic vision. Obviously, our conclusion does not suggest that there are no interactions between the cones in the central visual field and the rods in the peripheral visual field. Detection-threshold measurements of visual patterns have shown cone-rod interactions under mesopic vision (see, e.g., Buck, 2004). We are only suggesting that a time lag in the signals between separately excited cones and rods in the retina disturbs the integration of different motion signals. The interesting finding by Billino et al. (2008) that the detection of biological motion is more difficult under mesopic conditions than under scotopic conditions may be due to a disturbance in the integration of cone-rod information rather than to incongruent velocity information, as discussed in their study. 

In Experiment 3, negative priming was observed irrespective of the overlap time under photopic vision (Figure 10B). We assumed that this negative priming was induced by a spatially center-surround antagonistic motion-contrast detector. Murakami and Shimojo (1993) studied an induced motion in which a stationary pattern surrounded by moving patterns was perceived to move in the direction opposite to that of the moving patterns. They found that induced motion was perceived when the stimulus was large and presented from the center to the periphery of the visual field, whereas it was replaced by motion assimilation when the stimulus was small and presented only at the periphery. We assumed that a similar kind of computation by a spatially antagonistic motion mechanism induced negative priming in our stimulus condition. 

Negative priming was reported when the priming stimulus was presented in the periphery and the test stimulus was presented in the center under mesopic conditions, even though its effect was weak (Figures 4 and 7). This result could be explained by assuming the functioning of a spatially antagonistic motion-contrast detector on temporal overlapping of priming and test stimuli. 

Conclusions

We found that visual motion priming was greatly diminished under mesopic conditions when the priming and test stimuli were separately presented in the cone-dominant central retina and the rod-dominant peripheral retina. This result indicates that the incompleteness in the integration of signals that were induced by the temporal delay of rod pathways caused the degradation of motion perception under mesopic vision. 

Acknowledgments

Part of this study was presented at the Asia-Pacific Conference on Vision 2012, Incheon, Korea. We would like to thank Professor Yasuharu Okamoto of Japan Women's University and the anonymous reviewers for their insightful comments. This study was supported by JSPS KAKENHI Grant Number 24650058. 

Commercial relationships: none. 

Corresponding author: Sanae Yoshimoto. 

Email: [e-mail]. 

Address: Department of Psychology, Japan Women's University Kawasaki, Kanagawa, Japan.