Neuroscience Letters 564 (2014) 43–47
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Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Flash induced afterimage versus single spot visual object influence on visual–vestibular interaction in detection threshold for self-motion perception Ognyan I. Kolev ∗ , Keyvan Nicoucar Jenks Vestibular Physiology Laboratory, Department of Otology and Laryngology, MEEI, Harvard Medical School, Boston, MA, USA
h i g h l i g h t s • • • •
We studied the effect of visual afterimage on self-motion perception during rotation. Afterimage lowers the threshold for self-motion perception compared to darkness. Compared to a ‘real’ visual object fixation the threshold with afterimage is higher. The threshold is frequency dependent – it decreases with increase of the frequency.
a r t i c l e
i n f o
Article history: Received 20 October 2013 Received in revised form 17 January 2014 Accepted 2 February 2014 Keywords: Afterimage Self-motion Perception Threshold
a b s t r a c t In seven healthy subjects we studied the effect of flash induced afterimage on perceptual threshold for self-motion during sinusoidal vertical axis rotation compared to rotation in darkness, and rotation with subject’s gaze fixed on a ‘real’ visual object rotated with him. For a real object we used light-emitting diode (LED) aligned with subject’s head. A MOOG motion platform was used to generate motion. Single cycles of sinusoidal acceleration at four frequencies: 0.1, 0.2, 0.5, and 1 Hz were used as motion stimuli. The results show that the threshold when subjects stare at an afterimage during rotation is consistently lower compared to rotation in darkness. However, compared to the threshold during rotation with a ‘real’ object visual fixation it is higher, significantly at frequencies 0.5 and 0.2 Hz (p < 0.05). The threshold is frequency dependent – it decreases with increase of the frequency (p < 0.01). The probable mechanism of afterimage influence on perceptual threshold for self-motion is discussed. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Human organism uses overlap sensory systems for functioning. For instance the self-motion can be detected by the vestibular, visual, proprioceptive, and auditory sensory systems. Generally their role is to facilitate each other to allow a precise and a lower threshold perception. In some cases their interaction creates conflict; even so it results to a benefit for perception. For instance in earlier studies on self-motion perception during angular acceleration, the threshold in darkness, that is, when the vestibular system works only [1–6] has been found. When the visual system was involved by subject fixating his gaze on visual spot rotating with
∗ Corresponding author at: University Hospital of Neurology and Psychiatry, 4-th km, Tzarigradsko shosse Boulevard, 1113 Sofia, Bulgaria. Tel.: +359 8867 40392; fax: +359 2970 2142. E-mail address: kolev [email protected] (O.I. Kolev). http://dx.doi.org/10.1016/j.neulet.2014.02.002 0304-3940/© 2014 Elsevier Ireland Ltd. All rights reserved.
him (that is, in condition of visual–vestibular interaction) a change of the threshold has been established. This is a situation of sensory conflict between the vestibular information for rotation and that from the visual system for not moving visual object with respect to the subject. In such conflict condition a decrease of the threshold has been established [3,7–11]. It was expressed mostly for lower frequencies when sinusoidal rotation was applied [1]. The lowering of the threshold is due to the “oculogyral illusion”. This term was applied by Graybiel and Hupp [12] to define apparent motion of object in the visual field associated with angular acceleration of the body. For some reactions of the human organism to external stimuli we still do not completely understand the biological meaning. For example motion sickness. It manifests with opposing effects in different individuals – lowering blood pressure in some subjects and its increase in other. The same is with the pulse rate, skin color etc [13]. Another interesting phenomenon is ‘afterimage’. Its biological meaning and mechanism through which it operates is
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O.I. Kolev, K. Nicoucar / Neuroscience Letters 564 (2014) 43–47
for now also not completely revealed. Recent study implies that formation of afterimages involves neuronal structures that access input from both eyes but that do not correspond directly to the neuronal correlates of perceptual awareness [14]. Van Boxtel et al. [15] investigated the duration of afterimages for all four combinations of high versus low attention and visible versus invisible. Interestingly they showed that selective attention and visual consciousness have opposite effects: paying attention to the grating decreases the duration of its afterimage, whereas consciously seeing the grating increases the afterimage duration. Their findings provide clear evidence for distinctive influences of selective attention and consciousness on visual perception. With a head fixed target, perceptual thresholds for self-rotation are lower. The presence of a target improves perceptual threshold because of (i) visual suppression of the evoked vestibule-ocular reflex (VOR), and (ii) retinal slip of the target following eye drift caused by incomplete VOR suppression [16]. The purpose of this study was to investigate the influence of another visual cue that does not imply VOR cancelation, or retinal slip. Such visual cue is afterimage. 2. Subjects and methods 2.1. Subjects Seven healthy subjects (39 ± 12 years, 3 females and 4 males; 5 right-handed and 2 left-handed) were recruited to participate in this study. All subjects need first to complete a detailed vestibular diagnostic clinical examination to confirm a normal vestibular function before being included in the study. The vestibular screening examination consisted of Caloric electronystagmography, Hallpike testing, angular VOR evoked via rotation and posture control measures. Furthermore, a short health history questionnaire was administered; subjects were asked to indicate any known history of dizziness or vertigo, back/neck problems, cardiovascular, neurological and other physical problems. Subjects were also asked about their motion-sickness susceptibility. Informed consent was obtained from all subjects prior to participation in the study. The study was approved by the local ethics committee and has been performed in the Massachusetts Eye and Ear Infirmary building in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. 2.2. Apparatus and motion stimuli A MOOG motion platform (MOOG 6DOF2000E) was used to generate motion (Fig. 1). Single cycles of sinusoidal acceleration (a(t) = A sin (2ft) = A sin (2 t/T)) were used, where A is the acceleration amplitude and f is the frequency, which is the inverse of the period (and duration) of the stimulation (T = 1/f). Since the motion began at zero velocity, integration of the acceleration yields an oscillatory velocity, v(t) = AT/(2) [1 − cos (2t/T)], and a lateral displacement p(t) = AT/(2) [t − T/(2) sin (2 t/T)]. Therefore, both the peak velocity (vmax = AT/) and the total lateral displacement (p = AT2 /2) are proportional to the peak acceleration (A). These motion profiles were chosen because they mimic the characteristics shape of natural volitional head movements, because they have been successfully utilized in the only other study quantifying perceptual yaw rotation thresholds as a function of frequency [3], and because these motion profiles contain no discontinuities in acceleration, velocity, or position. 2.3. Visual stimuli Subjects were exposed to two different visual stimulations while sitting on a chair (Fig. 1). One with a red spot which is produced by a light emitting diode (LED) fixed 60 cm in front of them
Fig. 1. Schematic presentation of the experimental set-up: Moog platform with a tested subject and visual stimuli. Schematic presentation of the used stimuli. Abbreviations: VEST – vestibular stimulus, BS – body in space, OS – object in space, AIS – afterimage in space.
aligned with midline of the subject’s head. The red spot, which rotated with the chair, stayed in fixed alignment with their heads and subjects were asked to view the red spot only during motion. The brightness was just enough to be detected in darkness without illuminating the surrounding area and never changed during all the experiment. The second visual stimulation – flash induced afterimage was produced by a standard commercial xenon flash camera having a cross shaped aperture of 1 cm in height and width, fixated at the same position as LED, 60 cm in front of the subjects’ eyes. To avoid any dazzle effect the flash it was covered by green plastic filter. Subjects reported that they feel comfortable with the applied attenuated flash stimulus. The afterimage was centered on the fovea. Subjects were asked to stare straight ahead without attempting to fixate the afterimage. 2.4. Experimental procedures Subjects were seated in an upright position in a chair with a 5-point harness and rotated in darkness and under visual stimulations in yaw about an earth-vertical axis. The subject’s head was held in place via an adjustable helmet, and was carefully positioned relative to the axis of rotation using external landmarks. The head was centered left to right relative to the earth-vertical rotation axis. In addition, we identified the posterior edge of the external ear canal and located the rotation axis near this landmark in the fore-aft direction. To minimize the influence of non-vestibular cues regarding motion direction, trails were performed in the dark in a light-tight room. All skin surfaces expect the face were covered (long sleeves, light gloves) and a visor attached to the helmet surrounded the face. Earplugs reduced external noise by about 20 dB and the remaining auditory motion cues were masked by white noise (circa 60 dB). Tactile cues were distributed as evenly as possible using padding. Thresholds for self-motion in darkness, with red spot visual stimulation, and with flash induced after image were measured at four different frequencies, namely at 0.1, 0.2, 0.5, and 1 Hz. Each frequency was tested in a block of contiguous trials. These four blocks of trials were separated by a short break. The order of blocks was randomized across subjects. Subjects were rotated in yaw in three conditions randomized between the subjects: (1) in total darkness; (2) subjects were asked to fixate their gaze at the LED aligned with midline of the subject’s head, rotated together with the subjects (Fig. 1); (3) subjects
O.I. Kolev, K. Nicoucar / Neuroscience Letters 564 (2014) 43–47
were asked to stare straight ahead without attempting to fixate the afterimage (Fig. 1). Subjects were rotated either to the left or to the right. A brief low-pitch “warning” tone was administered 2 s before the onset of each motion stimulus. At the end of each trial a brief high-pitch sound was played to indicate that the subject needed to respond. The subjects were instructed to push the button in their left hand if they perceived a leftward rotation or to push the button in their right hand for rightward rotation. In case the subjects were uncertain of the direction of motion, they were instructed to make their best guess by pressing one of the two buttons. Before each testsession a few supra-threshold practice trials were administered to assure that the subjects understood the task and to minimize training effects. The button pushes were noted by the experimenter and recorded via computer. An adaptive two-alternative categorical forced-choice procedure [17,18] was used in all conditions. For the adaptative procedure, thresholds were measured using a 3-down, 1-up staircase paradigm (e.g., Leek [18]), where 3-down means that the subject had to correctly detect the direction of motion for three motion stimuli in a row in order for the acceleration level to be reduced and 1-up means that the acceleration level is increased every time the subject makes a mistake. This 3-down, 1-up paradigm targets a threshold at which the subject correctly detects motion 79.4% of the time [18], which we accepted as our threshold criteria. Typically, trials began well above threshold (starting values were 5.1 deg s−1 for condition 1 Hz, 10.2 deg s−1 for 0.5 Hz, 8.8 deg s−1 for 0.2 Hz, and 4.1 deg s−1 for 0.1 Hz). Testing continued until each test demonstrated nine direction reversals in the adaptive track: five minimum and four maximum direction reversals. Minimum reversals occur when the subject makes an error and the stimulus level goes up. Maximum reversals occur when the subject correctly detects motion at a given acceleration level three times in row immediately after incorrectly detecting motion on the previous trial. Threshold was defined as the mean of the last two-one minimum and one maximum-reversals. The significance of the change of the self-motion perception threshold was analyzed with two-way repeated measure ANOVA (SigmaPlot for Windows 11.0, SysStat Soft Inc.) with within-subject factor: ‘visual signal’ (darkness, LED single spot, and afterimage), and within-subject factor: ‘frequency’ (0.1, 0.2, 0.5 and 1 Hz). For
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post-hoc analysis we applied Student–Newman–Keuls tests. The level of significance was fixed at P < 0.05. 3. Results Two-way repeated measures ANOVA showed significant effect of both factors: ‘visual signal’ (F = 26.44, p < 0.0015) and ‘frequency’ (F = 52.53, p < 0.001). Self-motion perception thresholds with an afterimage (Fig. 2) are significantly lower compared to thresholds in darkness for the used frequencies (p < 0.05). Thresholds depend on stimulus frequency. They decreased significantly with increasing the frequency (p < 0.01). The threshold is highest at frequency 0.1 Hz and lowest at frequency 1 Hz. The variability between subjects also decreases with increase of the frequency. The thresholds with an afterimage compared to those with a LED single spot are significantly higher, compared at frequencies 0.5 and 0.2 Hz (p < 0.05). However at frequencies 0.1 and 1 Hz the thresholds between both visual stimuli are not significantly different (p = 0.3 and p = 0.7, respectively). The threshold with a LED single spot and in darkness showed also frequency dependence (p < 0.01). The threshold with a LED single spot is approximately double lower than that in total darkness (p < 0.01). 4. Discussion The present study shows that self-motion perceptual threshold during vertical axis sinusoidal rotation decreases when a subject stares straight ahead without attempting to fixate an afterimage compared to the threshold obtained during the same rotation but in total darkness. The study shows also a difference in the perceptual threshold for self-motion between conditions when subject stares at an afterimage compared to that when he fixates his gaze during vertical axis rotation on a ‘real’ object rotated together with him, aligned with the subject’s head. Both images differ between in their visual characteristics and genesis. The difference in perception for motion between condition of rotation with a ‘real’ visual target aligned with subject’s head and
Fig. 2. Plot of mean velocity ± SEM values of self-motion perception thresholds in the three tested conditions – with afterimage, with LED single spot real image, and in darkness, for four frequencies: 0.1, 0.2, 0.5, and 1 Hz, of sinusoidal acceleration.
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a visual afterimage is implied in several earlier studies. Graybiel and Hupp [12] were the first to investigate oculogyral illusion and to compare afterimage movement during and after vertical axis rotation to that of a ‘real’ target fixed with respect to the subject’s head. Interestingly they found that the direction of the apparent movement of the afterimage following rotation was exactly opposite to that observed when a ‘real’ target is fixated. Roman et al. [19] established in parabolic flight weightlessness that while the visual afterimage raises at the same time a real target appears lowered in the visual field. Although the aforementioned studies show certain effect of afterimage on perception for motion nobody so far has investigated how a visual afterimage changes perceptual threshold for self-motion. Here it has to be mentioned that although photobiophysical retinal mechanisms are essential for generating negative afterimages, cortical neurons have also essential contribution in the interpretation and modulation of negative afterimages [20]. There are two main mechanisms generally accepted to explain the lower threshold for self-motion perception when subject is rotated while viewing head-fixed target [16]. One is visual suppression of the evoked vestibulo-ocular reflex (VOR) with target fixation. To suppress the VOR the central nervous system requires to encode a predictive eye pursuit command [21–23]. In our study however there is no visual suppression since there is no target fixation – subjects were instructed not to fixate the afterimage but to stare straight ahead without attempting to fixate the afterimage. The difference in the command has been shown in our earlier study in which when one do not fixate the afterimage the post-rotatory VOR is not suppressed [24]. The second mechanism is retinal slip of the target following eye drift caused by incomplete suppression of the VOR [16]. However this mechanism couldn’t be applied to our afterimage experiment because, unlike viewing head-fixed ‘real’ target, the afterimage is not fixed to the head neither to the space but is “fixed” to the retina. Therefore in this condition there is no retinal slip factor. We sustain the following hypothesis. In sinusoidal rotation in darkness there are several efferent motor signals: VOR, efference copy signal, and proprioception from extraocular ocular muscles [25]. These motor signals are contributing at a subthreshold level to influence the perceptual threshold. However, when an afterimage is added as a visual signal, although it has no characteristics of a ‘real’ object, it obviously interacts with these motor signals, which causes perception of motion – subjects report for afterimage systematic motion, but not in the same pattern to that observed in condition with head-fixed target. So there is visual-vestibular-proprioceptive interaction, which operates through another mechanism. This mechanism functions at a relatively higher threshold level compared to that with a ‘real’ visual object fixation. In both cases perception of visual motion is detected but in opposite direction. In one case it creates oculogyral illusion – ‘real’ object motion, while in the other – afterimage motion. The weak self control over spontaneous, uncontrolled, free eye movements, or those provoked inattentionally or by spontaneous gazing toward the afterimage, lead to afterimage drift misinterpreted from the brain like caused by VOR. These act as a noise and presumably could contribute to the established difference, between self-motion perception threshold with an afterimage and that with a head-fixed ‘real’ object. We have to mention that the present study gives also confirmative information for substantial lowering of perceptual threshold for self-motion during visual fixation of a target rotating together with the subject’s head compared to that obtained during rotation in total darkness and that it is frequency dependent. The lowering was nearly twice (Fig. 2), which is less than the difference established by Clark and Stewart [8]. They found nearly tree
times lowering the perceptual threshold. However in their next experiment when they compared three methods: constant method, forced-choice, double-staircase method, and method of constantly increasing acceleration (ramp method) they found some difference [5]. Technical limitations of the rotation devices used in earlier studies also could explain some difference in the results. Some difference in the threshold for self motion perception with real object fixation rotating together with the subject’s head could be seen between the present study and our earlier one [1]. Our explanation is that in the previous study we used a different detection threshold method – ‘lower and upper limit’ and different rotation device. In conclusion, the present study shows that when a subject stares at an afterimage during angular acceleration the perceptual threshold for self-motion lowers compared to the threshold during acceleration in darkness. However, compared to that obtained during angular acceleration when a subject fixates his gaze on a ’real’ visual object rotated together with him the threshold is higher; the mechanism of self-motion perception operating with afterimage differs from that operating with head fixed ‘real’ visual object. The threshold with an afterimage is frequency dependent. Acknowledgements Authors thank to Dr. Daniel M. Merfeld, Director of Jenks Vestibular Physiology Laboratory, MEEI, Otolaryngology and Laryngology, Harvard Medical School, Boston, MA, USA, and to all personnel of the laboratory for helping to perform this study. The study was supported in part by ONR Global grant (N0001406-1-4030) to O.I. Kolev. K. Nicoucar was supported by the Swiss Foundation for Fellowships in Medicine and Biology (PASMP3-123225) in collaboration with the Swiss National Science Foundation. References [1] O. Kolev, T. Mergner, H. Kimmig, W. Becker, Detection thresholds for object motion and self-motion during vestibular and visuo-oculomotor stimulation, Brain Res. Bull. 40 (5-6) (1996) 451–457. [2] L. Grabherr, K. Nicoucar, F.W. Mast, D.M. Merfeld, Vestibular thresholds for yaw rotation about an earth-vertical axis as a function of frequency, Exp. Brain Res. 186 (4) (2008) 677–681. [3] A.J. Benson, E.C. Hutt, S.F. Brown, Thresholds for the perception of whole body angular movement about a vertical axis, Aviat. Space Environ. Med. 60 (1989) 205–213. [4] F. Guedry, Psychophysics of vestibular sensation, in: H.H. Kornhuber (Ed.), Handbook of Sensory Physiology, VI, Springer-Verlag, New York, 1974, pp. 1–154. [5] B. Clark, J.D. Stewart, Comparison of three methods to determine thresholds for the perception of passive, bodily angular acceleration, Am. J. Psychol. 81 (1968) 207–216. [6] B. Clark, Thresholds for the perception of angular acceleration in man, Aerospace Med. 38 (1967) 443–450. [7] R.L. Doty, Effect of duration of stimulus presentation on the angular acceleration threshold, J. Exp. Psychol. 80 (2) (1969) 317–321. [8] B. Clark, J.D. Stewart, Comparison of sensitivity for the perception of bodily rotation and the oculogyral illusion, Percept. Psychophys. 3 (1968) 253– 256. [9] L.J. Roggeveen, P. Nijhoff, The normal and pathological thresholds of the perception of angular accelerations for the optogyral illusion and the turning sensation, Acta Otolaryngol. 46 (1956) 533–541. [10] C.S. Hallpike, J.D. Hood, The speed of the of the slow component of the ocular nystagmus induced by angular acceleration of the head: its experimental determination and application to the physical theory of the cupular mechanism, Proc. R. Soc. Lond. Biol. 141 (1953) 216–230. [11] A. Graybiel, W.A. Kerb, S.H. Hartley, Stimulus thresholds of the semicircular canals as a function of angular acceleration, Am. J. Psychol. 61 (1948) 21– 36. [12] A. Graybiel, D.I. Hupp, The oculogyral illusion, J. Aviat. Med. 17 (1946) 3–27. [13] K.E. Money, Motion sickness, Physiol. Rev. 50 (1) (1970) 1–39. [14] N. Tsuchiya, C. Koch, Continuous flash suppression reduces negative afterimages, Nat. Neurosci. 8 (2005) 1096–1101. [15] J.A. van Boxtel, N. Tsuchiya, C. Koch, Opposing effects of attention and consciousness on afterimages, Proc. Natl. Acad. Sci. U. S. A. 107 (19) (2010) 8883–8888.
O.I. Kolev, K. Nicoucar / Neuroscience Letters 564 (2014) 43–47 [16] J. Carriot, A. Bryan, P. DiZio, J.R. Lackner, The oculogyral illusion: retinal and oculomotor factors, Exp. Brain Res. 209 (2011) 415– 423. [17] B. Treutwein, Adaptive psychophysical procedures, Vision Res. 35 (1995) 2503–2522. [18] M.R. Leek, Adaptive procedures in psychophysical research, Percept. Psychophys. 63 (2001) 1279–1292. [19] J.A. Roman, B.H. Warren, A. Graybiel, Observations of the elevator illusion during subgravity preceded by negative accelerations, Aerospace Med. 35 (1964) 121–124. [20] I. Bókkon, R.L. Vimal, C. Wang, J. Dai, V. Salari, F. Grass, I. Antal, Visible light induced ocular delayed bioluminescence as a possible origin of negative afterimage, J. Photochem. Photobiol. B 103 (2) (2011) 192–199.
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[21] G.R. Barnes, Head-eye co-ordination: visual and nonvisual mechanisms of vestibulo-ocular reflex slow-phase modification, Prog. Brain Res. 76 (1988) 319–328. [22] G.R. Barnes, R.D. Eason, Effects of visual and non-visual mechanisms on the vestibulo-ocular reflex during pseudo-random head movements in man, J. Physiol. 395 (1988) 383–400. [23] T.C. Whiteside, A. Graybiel, J.I. Niven, Visual illusions of movement, Brain 88 (1995) 193–210. [24] O.I. Kolev, Comparative investigation of vestibular influence on visual hallucinations and flash induced afterimage, Acta Otolaryngol. Suppl. 481 (1991) 262–265. [25] R.J. Leigh, D.S. Zee, in: The Neurology of Eye Movements, Oxford University Press, New York, 2006.
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Flash induced afterimage versus single spot visual object influence on visual–vestibular interaction in detection threshold for self-motion perception Ognyan I. Kolev ∗ , Keyvan Nicoucar Jenks Vestibular Physiology Laboratory, Department of Otology and Laryngology, MEEI, Harvard Medical School, Boston, MA, USA
h i g h l i g h t s • • • •
We studied the effect of visual afterimage on self-motion perception during rotation. Afterimage lowers the threshold for self-motion perception compared to darkness. Compared to a ‘real’ visual object fixation the threshold with afterimage is higher. The threshold is frequency dependent – it decreases with increase of the frequency.
a r t i c l e
i n f o
Article history: Received 20 October 2013 Received in revised form 17 January 2014 Accepted 2 February 2014 Keywords: Afterimage Self-motion Perception Threshold
a b s t r a c t In seven healthy subjects we studied the effect of flash induced afterimage on perceptual threshold for self-motion during sinusoidal vertical axis rotation compared to rotation in darkness, and rotation with subject’s gaze fixed on a ‘real’ visual object rotated with him. For a real object we used light-emitting diode (LED) aligned with subject’s head. A MOOG motion platform was used to generate motion. Single cycles of sinusoidal acceleration at four frequencies: 0.1, 0.2, 0.5, and 1 Hz were used as motion stimuli. The results show that the threshold when subjects stare at an afterimage during rotation is consistently lower compared to rotation in darkness. However, compared to the threshold during rotation with a ‘real’ object visual fixation it is higher, significantly at frequencies 0.5 and 0.2 Hz (p < 0.05). The threshold is frequency dependent – it decreases with increase of the frequency (p < 0.01). The probable mechanism of afterimage influence on perceptual threshold for self-motion is discussed. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Human organism uses overlap sensory systems for functioning. For instance the self-motion can be detected by the vestibular, visual, proprioceptive, and auditory sensory systems. Generally their role is to facilitate each other to allow a precise and a lower threshold perception. In some cases their interaction creates conflict; even so it results to a benefit for perception. For instance in earlier studies on self-motion perception during angular acceleration, the threshold in darkness, that is, when the vestibular system works only [1–6] has been found. When the visual system was involved by subject fixating his gaze on visual spot rotating with
∗ Corresponding author at: University Hospital of Neurology and Psychiatry, 4-th km, Tzarigradsko shosse Boulevard, 1113 Sofia, Bulgaria. Tel.: +359 8867 40392; fax: +359 2970 2142. E-mail address: kolev [email protected] (O.I. Kolev). http://dx.doi.org/10.1016/j.neulet.2014.02.002 0304-3940/© 2014 Elsevier Ireland Ltd. All rights reserved.
him (that is, in condition of visual–vestibular interaction) a change of the threshold has been established. This is a situation of sensory conflict between the vestibular information for rotation and that from the visual system for not moving visual object with respect to the subject. In such conflict condition a decrease of the threshold has been established [3,7–11]. It was expressed mostly for lower frequencies when sinusoidal rotation was applied [1]. The lowering of the threshold is due to the “oculogyral illusion”. This term was applied by Graybiel and Hupp [12] to define apparent motion of object in the visual field associated with angular acceleration of the body. For some reactions of the human organism to external stimuli we still do not completely understand the biological meaning. For example motion sickness. It manifests with opposing effects in different individuals – lowering blood pressure in some subjects and its increase in other. The same is with the pulse rate, skin color etc [13]. Another interesting phenomenon is ‘afterimage’. Its biological meaning and mechanism through which it operates is
44
O.I. Kolev, K. Nicoucar / Neuroscience Letters 564 (2014) 43–47
for now also not completely revealed. Recent study implies that formation of afterimages involves neuronal structures that access input from both eyes but that do not correspond directly to the neuronal correlates of perceptual awareness [14]. Van Boxtel et al. [15] investigated the duration of afterimages for all four combinations of high versus low attention and visible versus invisible. Interestingly they showed that selective attention and visual consciousness have opposite effects: paying attention to the grating decreases the duration of its afterimage, whereas consciously seeing the grating increases the afterimage duration. Their findings provide clear evidence for distinctive influences of selective attention and consciousness on visual perception. With a head fixed target, perceptual thresholds for self-rotation are lower. The presence of a target improves perceptual threshold because of (i) visual suppression of the evoked vestibule-ocular reflex (VOR), and (ii) retinal slip of the target following eye drift caused by incomplete VOR suppression [16]. The purpose of this study was to investigate the influence of another visual cue that does not imply VOR cancelation, or retinal slip. Such visual cue is afterimage. 2. Subjects and methods 2.1. Subjects Seven healthy subjects (39 ± 12 years, 3 females and 4 males; 5 right-handed and 2 left-handed) were recruited to participate in this study. All subjects need first to complete a detailed vestibular diagnostic clinical examination to confirm a normal vestibular function before being included in the study. The vestibular screening examination consisted of Caloric electronystagmography, Hallpike testing, angular VOR evoked via rotation and posture control measures. Furthermore, a short health history questionnaire was administered; subjects were asked to indicate any known history of dizziness or vertigo, back/neck problems, cardiovascular, neurological and other physical problems. Subjects were also asked about their motion-sickness susceptibility. Informed consent was obtained from all subjects prior to participation in the study. The study was approved by the local ethics committee and has been performed in the Massachusetts Eye and Ear Infirmary building in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. 2.2. Apparatus and motion stimuli A MOOG motion platform (MOOG 6DOF2000E) was used to generate motion (Fig. 1). Single cycles of sinusoidal acceleration (a(t) = A sin (2ft) = A sin (2 t/T)) were used, where A is the acceleration amplitude and f is the frequency, which is the inverse of the period (and duration) of the stimulation (T = 1/f). Since the motion began at zero velocity, integration of the acceleration yields an oscillatory velocity, v(t) = AT/(2) [1 − cos (2t/T)], and a lateral displacement p(t) = AT/(2) [t − T/(2) sin (2 t/T)]. Therefore, both the peak velocity (vmax = AT/) and the total lateral displacement (p = AT2 /2) are proportional to the peak acceleration (A). These motion profiles were chosen because they mimic the characteristics shape of natural volitional head movements, because they have been successfully utilized in the only other study quantifying perceptual yaw rotation thresholds as a function of frequency [3], and because these motion profiles contain no discontinuities in acceleration, velocity, or position. 2.3. Visual stimuli Subjects were exposed to two different visual stimulations while sitting on a chair (Fig. 1). One with a red spot which is produced by a light emitting diode (LED) fixed 60 cm in front of them
Fig. 1. Schematic presentation of the experimental set-up: Moog platform with a tested subject and visual stimuli. Schematic presentation of the used stimuli. Abbreviations: VEST – vestibular stimulus, BS – body in space, OS – object in space, AIS – afterimage in space.
aligned with midline of the subject’s head. The red spot, which rotated with the chair, stayed in fixed alignment with their heads and subjects were asked to view the red spot only during motion. The brightness was just enough to be detected in darkness without illuminating the surrounding area and never changed during all the experiment. The second visual stimulation – flash induced afterimage was produced by a standard commercial xenon flash camera having a cross shaped aperture of 1 cm in height and width, fixated at the same position as LED, 60 cm in front of the subjects’ eyes. To avoid any dazzle effect the flash it was covered by green plastic filter. Subjects reported that they feel comfortable with the applied attenuated flash stimulus. The afterimage was centered on the fovea. Subjects were asked to stare straight ahead without attempting to fixate the afterimage. 2.4. Experimental procedures Subjects were seated in an upright position in a chair with a 5-point harness and rotated in darkness and under visual stimulations in yaw about an earth-vertical axis. The subject’s head was held in place via an adjustable helmet, and was carefully positioned relative to the axis of rotation using external landmarks. The head was centered left to right relative to the earth-vertical rotation axis. In addition, we identified the posterior edge of the external ear canal and located the rotation axis near this landmark in the fore-aft direction. To minimize the influence of non-vestibular cues regarding motion direction, trails were performed in the dark in a light-tight room. All skin surfaces expect the face were covered (long sleeves, light gloves) and a visor attached to the helmet surrounded the face. Earplugs reduced external noise by about 20 dB and the remaining auditory motion cues were masked by white noise (circa 60 dB). Tactile cues were distributed as evenly as possible using padding. Thresholds for self-motion in darkness, with red spot visual stimulation, and with flash induced after image were measured at four different frequencies, namely at 0.1, 0.2, 0.5, and 1 Hz. Each frequency was tested in a block of contiguous trials. These four blocks of trials were separated by a short break. The order of blocks was randomized across subjects. Subjects were rotated in yaw in three conditions randomized between the subjects: (1) in total darkness; (2) subjects were asked to fixate their gaze at the LED aligned with midline of the subject’s head, rotated together with the subjects (Fig. 1); (3) subjects
O.I. Kolev, K. Nicoucar / Neuroscience Letters 564 (2014) 43–47
were asked to stare straight ahead without attempting to fixate the afterimage (Fig. 1). Subjects were rotated either to the left or to the right. A brief low-pitch “warning” tone was administered 2 s before the onset of each motion stimulus. At the end of each trial a brief high-pitch sound was played to indicate that the subject needed to respond. The subjects were instructed to push the button in their left hand if they perceived a leftward rotation or to push the button in their right hand for rightward rotation. In case the subjects were uncertain of the direction of motion, they were instructed to make their best guess by pressing one of the two buttons. Before each testsession a few supra-threshold practice trials were administered to assure that the subjects understood the task and to minimize training effects. The button pushes were noted by the experimenter and recorded via computer. An adaptive two-alternative categorical forced-choice procedure [17,18] was used in all conditions. For the adaptative procedure, thresholds were measured using a 3-down, 1-up staircase paradigm (e.g., Leek [18]), where 3-down means that the subject had to correctly detect the direction of motion for three motion stimuli in a row in order for the acceleration level to be reduced and 1-up means that the acceleration level is increased every time the subject makes a mistake. This 3-down, 1-up paradigm targets a threshold at which the subject correctly detects motion 79.4% of the time [18], which we accepted as our threshold criteria. Typically, trials began well above threshold (starting values were 5.1 deg s−1 for condition 1 Hz, 10.2 deg s−1 for 0.5 Hz, 8.8 deg s−1 for 0.2 Hz, and 4.1 deg s−1 for 0.1 Hz). Testing continued until each test demonstrated nine direction reversals in the adaptive track: five minimum and four maximum direction reversals. Minimum reversals occur when the subject makes an error and the stimulus level goes up. Maximum reversals occur when the subject correctly detects motion at a given acceleration level three times in row immediately after incorrectly detecting motion on the previous trial. Threshold was defined as the mean of the last two-one minimum and one maximum-reversals. The significance of the change of the self-motion perception threshold was analyzed with two-way repeated measure ANOVA (SigmaPlot for Windows 11.0, SysStat Soft Inc.) with within-subject factor: ‘visual signal’ (darkness, LED single spot, and afterimage), and within-subject factor: ‘frequency’ (0.1, 0.2, 0.5 and 1 Hz). For
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post-hoc analysis we applied Student–Newman–Keuls tests. The level of significance was fixed at P < 0.05. 3. Results Two-way repeated measures ANOVA showed significant effect of both factors: ‘visual signal’ (F = 26.44, p < 0.0015) and ‘frequency’ (F = 52.53, p < 0.001). Self-motion perception thresholds with an afterimage (Fig. 2) are significantly lower compared to thresholds in darkness for the used frequencies (p < 0.05). Thresholds depend on stimulus frequency. They decreased significantly with increasing the frequency (p < 0.01). The threshold is highest at frequency 0.1 Hz and lowest at frequency 1 Hz. The variability between subjects also decreases with increase of the frequency. The thresholds with an afterimage compared to those with a LED single spot are significantly higher, compared at frequencies 0.5 and 0.2 Hz (p < 0.05). However at frequencies 0.1 and 1 Hz the thresholds between both visual stimuli are not significantly different (p = 0.3 and p = 0.7, respectively). The threshold with a LED single spot and in darkness showed also frequency dependence (p < 0.01). The threshold with a LED single spot is approximately double lower than that in total darkness (p < 0.01). 4. Discussion The present study shows that self-motion perceptual threshold during vertical axis sinusoidal rotation decreases when a subject stares straight ahead without attempting to fixate an afterimage compared to the threshold obtained during the same rotation but in total darkness. The study shows also a difference in the perceptual threshold for self-motion between conditions when subject stares at an afterimage compared to that when he fixates his gaze during vertical axis rotation on a ‘real’ object rotated together with him, aligned with the subject’s head. Both images differ between in their visual characteristics and genesis. The difference in perception for motion between condition of rotation with a ‘real’ visual target aligned with subject’s head and
Fig. 2. Plot of mean velocity ± SEM values of self-motion perception thresholds in the three tested conditions – with afterimage, with LED single spot real image, and in darkness, for four frequencies: 0.1, 0.2, 0.5, and 1 Hz, of sinusoidal acceleration.
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a visual afterimage is implied in several earlier studies. Graybiel and Hupp [12] were the first to investigate oculogyral illusion and to compare afterimage movement during and after vertical axis rotation to that of a ‘real’ target fixed with respect to the subject’s head. Interestingly they found that the direction of the apparent movement of the afterimage following rotation was exactly opposite to that observed when a ‘real’ target is fixated. Roman et al. [19] established in parabolic flight weightlessness that while the visual afterimage raises at the same time a real target appears lowered in the visual field. Although the aforementioned studies show certain effect of afterimage on perception for motion nobody so far has investigated how a visual afterimage changes perceptual threshold for self-motion. Here it has to be mentioned that although photobiophysical retinal mechanisms are essential for generating negative afterimages, cortical neurons have also essential contribution in the interpretation and modulation of negative afterimages [20]. There are two main mechanisms generally accepted to explain the lower threshold for self-motion perception when subject is rotated while viewing head-fixed target [16]. One is visual suppression of the evoked vestibulo-ocular reflex (VOR) with target fixation. To suppress the VOR the central nervous system requires to encode a predictive eye pursuit command [21–23]. In our study however there is no visual suppression since there is no target fixation – subjects were instructed not to fixate the afterimage but to stare straight ahead without attempting to fixate the afterimage. The difference in the command has been shown in our earlier study in which when one do not fixate the afterimage the post-rotatory VOR is not suppressed [24]. The second mechanism is retinal slip of the target following eye drift caused by incomplete suppression of the VOR [16]. However this mechanism couldn’t be applied to our afterimage experiment because, unlike viewing head-fixed ‘real’ target, the afterimage is not fixed to the head neither to the space but is “fixed” to the retina. Therefore in this condition there is no retinal slip factor. We sustain the following hypothesis. In sinusoidal rotation in darkness there are several efferent motor signals: VOR, efference copy signal, and proprioception from extraocular ocular muscles [25]. These motor signals are contributing at a subthreshold level to influence the perceptual threshold. However, when an afterimage is added as a visual signal, although it has no characteristics of a ‘real’ object, it obviously interacts with these motor signals, which causes perception of motion – subjects report for afterimage systematic motion, but not in the same pattern to that observed in condition with head-fixed target. So there is visual-vestibular-proprioceptive interaction, which operates through another mechanism. This mechanism functions at a relatively higher threshold level compared to that with a ‘real’ visual object fixation. In both cases perception of visual motion is detected but in opposite direction. In one case it creates oculogyral illusion – ‘real’ object motion, while in the other – afterimage motion. The weak self control over spontaneous, uncontrolled, free eye movements, or those provoked inattentionally or by spontaneous gazing toward the afterimage, lead to afterimage drift misinterpreted from the brain like caused by VOR. These act as a noise and presumably could contribute to the established difference, between self-motion perception threshold with an afterimage and that with a head-fixed ‘real’ object. We have to mention that the present study gives also confirmative information for substantial lowering of perceptual threshold for self-motion during visual fixation of a target rotating together with the subject’s head compared to that obtained during rotation in total darkness and that it is frequency dependent. The lowering was nearly twice (Fig. 2), which is less than the difference established by Clark and Stewart [8]. They found nearly tree
times lowering the perceptual threshold. However in their next experiment when they compared three methods: constant method, forced-choice, double-staircase method, and method of constantly increasing acceleration (ramp method) they found some difference [5]. Technical limitations of the rotation devices used in earlier studies also could explain some difference in the results. Some difference in the threshold for self motion perception with real object fixation rotating together with the subject’s head could be seen between the present study and our earlier one [1]. Our explanation is that in the previous study we used a different detection threshold method – ‘lower and upper limit’ and different rotation device. In conclusion, the present study shows that when a subject stares at an afterimage during angular acceleration the perceptual threshold for self-motion lowers compared to the threshold during acceleration in darkness. However, compared to that obtained during angular acceleration when a subject fixates his gaze on a ’real’ visual object rotated together with him the threshold is higher; the mechanism of self-motion perception operating with afterimage differs from that operating with head fixed ‘real’ visual object. The threshold with an afterimage is frequency dependent. Acknowledgements Authors thank to Dr. Daniel M. Merfeld, Director of Jenks Vestibular Physiology Laboratory, MEEI, Otolaryngology and Laryngology, Harvard Medical School, Boston, MA, USA, and to all personnel of the laboratory for helping to perform this study. The study was supported in part by ONR Global grant (N0001406-1-4030) to O.I. Kolev. K. Nicoucar was supported by the Swiss Foundation for Fellowships in Medicine and Biology (PASMP3-123225) in collaboration with the Swiss National Science Foundation. References [1] O. Kolev, T. Mergner, H. Kimmig, W. Becker, Detection thresholds for object motion and self-motion during vestibular and visuo-oculomotor stimulation, Brain Res. Bull. 40 (5-6) (1996) 451–457. [2] L. Grabherr, K. Nicoucar, F.W. Mast, D.M. Merfeld, Vestibular thresholds for yaw rotation about an earth-vertical axis as a function of frequency, Exp. Brain Res. 186 (4) (2008) 677–681. [3] A.J. Benson, E.C. Hutt, S.F. Brown, Thresholds for the perception of whole body angular movement about a vertical axis, Aviat. Space Environ. Med. 60 (1989) 205–213. [4] F. Guedry, Psychophysics of vestibular sensation, in: H.H. Kornhuber (Ed.), Handbook of Sensory Physiology, VI, Springer-Verlag, New York, 1974, pp. 1–154. [5] B. Clark, J.D. Stewart, Comparison of three methods to determine thresholds for the perception of passive, bodily angular acceleration, Am. J. Psychol. 81 (1968) 207–216. [6] B. Clark, Thresholds for the perception of angular acceleration in man, Aerospace Med. 38 (1967) 443–450. [7] R.L. Doty, Effect of duration of stimulus presentation on the angular acceleration threshold, J. Exp. Psychol. 80 (2) (1969) 317–321. [8] B. Clark, J.D. Stewart, Comparison of sensitivity for the perception of bodily rotation and the oculogyral illusion, Percept. Psychophys. 3 (1968) 253– 256. [9] L.J. Roggeveen, P. Nijhoff, The normal and pathological thresholds of the perception of angular accelerations for the optogyral illusion and the turning sensation, Acta Otolaryngol. 46 (1956) 533–541. [10] C.S. Hallpike, J.D. Hood, The speed of the of the slow component of the ocular nystagmus induced by angular acceleration of the head: its experimental determination and application to the physical theory of the cupular mechanism, Proc. R. Soc. Lond. Biol. 141 (1953) 216–230. [11] A. Graybiel, W.A. Kerb, S.H. Hartley, Stimulus thresholds of the semicircular canals as a function of angular acceleration, Am. J. Psychol. 61 (1948) 21– 36. [12] A. Graybiel, D.I. Hupp, The oculogyral illusion, J. Aviat. Med. 17 (1946) 3–27. [13] K.E. Money, Motion sickness, Physiol. Rev. 50 (1) (1970) 1–39. [14] N. Tsuchiya, C. Koch, Continuous flash suppression reduces negative afterimages, Nat. Neurosci. 8 (2005) 1096–1101. [15] J.A. van Boxtel, N. Tsuchiya, C. Koch, Opposing effects of attention and consciousness on afterimages, Proc. Natl. Acad. Sci. U. S. A. 107 (19) (2010) 8883–8888.
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