- Email: [email protected]
Optokinetic stimulation affects temporal estimation in healthy humans
Brain and Cognition 64 (2007) 68–73 www.elsevier.com/locate/b&c
Optokinetic stimulation aVects temporal estimation in healthy humans Carmelo Mario Vicario a, Carlo Caltagirone b, Massimiliano Oliveri a,b,¤ a
Dipartimento di Psicologia, Università degli Studi di Palermo, Viale delle Scienze, EdiWcio 15, 90100 Palermo, Italy b Fondazione “Santa Lucia” IRCCS, Roma, Italy Accepted 7 December 2006 Available online 29 March 2007
Abstract The representation of time and space are closely linked in the cognitive system. Optokinetic stimulation modulates spatial attention in healthy subjects and patients with spatial neglect. In order to evaluate whether optokinetic stimulation could inXuence time perception, a group of healthy subjects performed “timecomparison” tasks of sub- and supra-second intervals before and after leftward or rightward optokinetic stimulation. Subjective time perception was biased by the direction of optokinetic stimulation. Rightward optokinetic stimulation induced an overestimation of time perception compared with baseline and leftward optokinetic stimulation. These results indicate a directional bias in time perception induced by manipulation of spatial attention and could argue for a mental linear representation of time intervals. © 2007 Elsevier Inc. All rights reserved. Keywords: Space; Time; Perception; Optokinetic stimulation
1. Introduction Mental representations of space and time represent elementary aspects of cognition and play a critical role in planning action and forming decisions in everyday life. Converging evidence from behavioral, neuroimaging and neuropsychological studies suggests the presence of close links between these diVerent cognitive systems (Walsh, 2003). At a behavioural level, spatial factors do aVect the perception of time and other magnitudes. When healthy subjects are asked to carry out tasks in environments built to 1/6, 1/12, or 1/24 of actual size and to stop when 30 min had passed, the ratio of time passed to time estimated scales according to environmental scale (De Long, 1981). The apparent duration of a dynamic stimulus can be manipulated in a local region of visual space by adapting to oscillatory motion or Xicker (Johnston, Arnold, & Nishida, 2006).
*
Corresponding author. Fax: +39 0917028431. E-mail address: [email protected] (M. Oliveri).
0278-2626/$ - see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.bandc.2006.12.002
The importance of visual factors is also supported by recent Wndings, showing that short intervals of time between two successive perisaccadic visual (and not auditory) events are underestimated, indicating a compression of perceived time (Morrone, Ross, & Burr, 2005). These data implicate spatially localised temporal mechanisms in duration perception. The link between spatial and temporal estimation has been also documented at a neural level. Neuropsychological studies show the occurrence of spatial as well as temporal deWcits following right hemispheric damage (Critchley, 1953; Koch, Oliveri, Carlesimo, & Caltagirone, 2002). Harrington, Haaland, and Knight (1998) showed that brain regions more frequently associated with in alterations of temporal perception tasks are the superior and middle frontal gyrus in the right frontal cortex, and the angular and supra-marginal gyri in the right parietal cortex. An important lesson comes from patients with contralesional spatial neglect. These patients overestimate durations of stimuli presented in the neglected space and underestimate durations of stimuli presented in the good right Weld (Basso, Nichelli, Frassinetti, & di Pellegrino, 1996).
C.M. Vicario et al. / Brain and Cognition 64 (2007) 68–73
Neuroimaging studies document an activation of the right parietal cortex in temporal as well as spatial tasks (Rao et al., 2001) and studies using transcranial magnetic stimulation show that disrupting the function of right prefrontal cortex transiently disrupts time perception (Koch, Oliveri, Torriero, & Caltagirone, 2003). A critical role in mediating the link between spatial and temporal perception could be made by attention. In fact, attention is known to inXuence perceived duration and temporal order (Enns, Breahaut, & Shore, 1999; Rose & Summers, 1995; Tse, Intriligator, Rivest, & Cavanagh, 2004). This suggests that procedures that manipulate spatial attention should also aVect temporal estimation tasks. A rich literature documents that manipulation of spatial attention towards the right or the left Weld by optokinetic stimulation is able to directionally inXuence spatial tasks. Fast optokinetic stimulation towards the neglected hemispace (Pizzamiglio, Frasca, Guariglia, Inoccia, & Antonucci, 1990), and slow horizontal background motion to the left (Mattingley, Bradshaw, & Bradshaw, 1994) have been shown to reduce the horizontal line bisection error probably by allocating selective attention to stimuli in the neglected space sector. Mattingley et al. (1994) using the OKS paradigm at speeds that did not elicit optokinetic nystagmus or perceptual after eVects, reported that control subjects were accurate in all conditions, and showed minimal eVects of background conditions. By contrast, patients with left unilateral spatial neglect were sensitive to leftward background motion, showing a signiWcant leftward shift in bisection error, relative to neutral, static, and rightward moving backgrounds. Other studies (KerkhoV, Schindler, Keller, & Marquardt, 1999) provide evidence that coherent visual background motion towards the neglected hemispace signiWcantly modulates the perceived horizontal object size, hence the size distortion, in neglect patients when comparing two stimuli separated in both hemispaces. This Wnding indicates that background motion not only aVects the subjective straight ahead (Karnath, 1996) and subjective midline in line bisection or line extension (Bisiach, Pizzamiglio, Nico, & Antonucci, 1996; Mattingley et al., 1994; Pizzamiglio et al., 1990), but also facilitates the accuracy of spatial judgments concerning two stimuli separated in left and right space. On the same theoretical position is Schindler (Schindler & KerkhoV, 2004), suggesting that visual motion stimulation in neglect alleviates both egocentric deviations (the subjective straight ahead) and allocentric perceptual distortions in neglect with or without visual Weld disorders. The combination of these studies conWrm that the paradigm of optokinetic stimulation is able to transiently move the “attentive focus” towards a speciWc side of space Weld (left vs. right), depending on the direction of optokinetic motion. The rationale behind the present study is that manipulation of spatial attention by means of optokinetic stimulation could be able to inXuence the performance not only in
69
spatial tasks but also in temporal tasks, thus arguing for the use of spatial codes in time perception. 2. Subjects and methods Thirty-Wve right-handed graduate students (17 male and 18 female, aged 22–31 years) with normal or corrected vision participated in the studies after providing written informed consent. 2.1. Optokinetic stimulation Optokinetic stimulation (OKS) was performed by presenting 384 series of a sequence of 17 § 2 white line segments, presented on a black background, each with a duration of 50 ms. Stimuli drifted either leftward or rightward, across the full width of a 14⬙ computer monitor, so that the direction of the apparent movement was from left to right and vice-versa in diVerent block of trials. The stroboscopic movement velocity was established functionally for individual subjects on the basis of subjective saccadic response, monitored by visual inspection by one experimenter. The average velocity was of 38°/s. In the Wrst experiment, the subjects were asked to Wxate a central mark on the screen, with the head immobilised over a chin-rest. Central Wxation was monitored by one experimenter. In the second and third experiment, the same paradigm of optokinetic stimulation was done without a central Wxation mark. 2.2. Time estimation task 2.2.1. Experiment 1 Fifteen subjects (8 men, 7 women, aged 21–26 years) participated in this experiment. They were positioned 60 cm opposite a white computer screen (the same used for OKS paradigm) and were required to determine whether a test cue (a red circle) had been presented for a time interval longer or shorter than a memorized standard duration of a reference cue (a blue circle). The duration of the reference cue was 300 ms in all trials. The test cue was presented immediately after the reference cue and its duration was selected randomly using intervals near the standard duration, ranging from 250 to 350 ms (in steps of 10 ms for a total of 10 intervals without presenting the average interval of 300 ms). The computer program selected interval lengths pseudo-randomly, so that each subject received Wve presentations of each interval length within a 50 trials block. The intertrial interval was of 2000 ms. Reference and test cues were presented as pairs at the centre of the screen. Total duration of a block was 130 s (50 trials ¤ (0.3 s reference cue duration + 0.3 s test cue average duration + 2 s intertrial interval)). Subjects indicated their judgment of the test cue’s duration by pressing either of two response buttons with their right and left index Wngers. In half of the trials, a right
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C.M. Vicario et al. / Brain and Cognition 64 (2007) 68–73
response indicated a smaller duration and a left response a bigger duration of the test cue and vice-versa in the other half of the trials. Time estimation task was performed in three sessions (on three consecutive days) to avoid carry over of aftereVects (optokinetic after-nystagmus) between blocks: a baseline session and a session immediately following a rightward or leftward block of optokinetic stimulation. The order of the sessions was randomised across subjects. In all experiments, subjects performed a 10-trials training on the time estimation task, before entering the main experiment. 2.2.2. Experiment 2 Ten subjects (5 men, 5 women, aged 20–24 years) diVerent from those recruited for experiment 1, participated in this experiment. OKS was performed without a central Wxation mark. All the other parameters of OKS and time estimation were identical to those of experiment 1. 2.2.3. Experiment 3 Ten subjects (4 men, 6 women, aged 20–23 years) participated in this experiment. None of them had participated in the previous experiments. The paradigm of OKS was identical to that of experiment 2 (OKS without a central Wxation mark). The time estimation task was similar to that of experiment 1 and 2 with the exception of the duration of reference and test cues. The duration of the reference cue was of 2000 ms. Test cue was presented immediately after the reference cue and its duration was selected randomly using intervals near the standard duration, ranging from 1500 to 2500 ms (in steps of 100 ms for a total of 10 intervals without presenting the average interval of 2000 ms). The computer program selected interval lengths pseudo-randomly, so that each subject received Wve presentations of each interval length within a 50 trials block. The intertrial interval was of 2000 ms. Reference and test cues were presented as pairs at the centre of the screen. Total duration of a block was 300 s (50 trials ¤ (2 s reference cue duration + 2 s test cue average duration + 2 s intertrial interval)). Response parameters and the other aspects of the experimental protocol were identical to those described for experiment 1.
leftward vs. rightward optokinetic stimulation) as withinsubject factor. Duncan’s post-hoc comparisons were made where appropriate. The level of signiWcance was set at p < .05. 3. Results 3.1. Experiment 1 Fig. 1 shows subjects’ performance in the three main experimental conditions. There was a signiWcant eVect of condition [F(2, 14) D 4, p D .01]. Rightward optokinetic stimulation induced a signiWcant time overestimation compared with both baseline (p D .04) and post-leftward optokinetic stimulation blocks (p D .008); the diVerence between leftward optokinetic stimulation and baseline was not signiWcant. 3.2. Experiment 2 Fig. 2 shows subjects’ performance in the time estimation tasks following OKS without a central Wxation mark. There was a signiWcant eVect of condition [F(2, 9) D 5.24; p D .005]. Rightward optokinetic stimulation induced a signiWcant time overestimation compared with both baseline (p D .01) and post-leftward optokinetic stimulation blocks (p D .003); the diVerence between leftward optokinetic stimulation and baseline was not signiWcant. 3.3. Experiment 3 Fig. 3 shows subjects’ performance in the time estimation task of supra-second intervals. OKS did not induce signiWcant eVects in the time task [F(2, 9) D 0.78; p D .47]. 4. Discussion The main result of the present study is that manipulation of spatial attention towards the right or left space by means
2.3. Data analysis In all experiments responses were analysed by assigning a value of 0 to correct responses, ¡1 to time underestimation (duration of an interval >300–2000 ms judged as shorter than the reference cue), 1 to time overestimation (duration of an interval <300–2000 ms judged as longer than the reference cue). The average responses were analyzed using ANOVA for repeated measures with the factor condition (baseline vs.
Fig. 1. Experiment 1. Percentage change vs. baseline in the time estimation task across the diVerent OKS conditions (grey bars: leftward OKS; white bars: rightward OKS). Error bars indicate 1 SE of mean.
C.M. Vicario et al. / Brain and Cognition 64 (2007) 68–73
Fig. 2. Experiment 2. Percentage change vs. baseline in the time estimation task across the diVerent OKS conditions (grey bars: leftward OKS; white bars: rightward OKS). Error bars indicate 1 SE of mean.
Fig. 3. Experiment 3. Percentage change vs. baseline in the time estimation task across the diVerent OKS conditions (grey bars: leftward OKS; white bars: rightward OKS). Error bars indicate 1 SE of mean.
of optokinetic stimulation induces a bias in a standard time estimation task performed immediately after the cessation of optokinetic stimulation. Moving attention towards the right hemispace induces time overestimation, while moving attention towards the left hemispace induces a trend towards time underestimation compared with baseline. This result was present when OKS was done with a central Wxation mark, but it was even more evident in the absence of OKN suppression, with the consequent increase in attention diversion. Optokinetic stimulation has been described to aVect healthy subjects’ exploration of space (Sandor, Bachtold, Henn, & Brugger, 2000). In a standard line bisection task, the bisection marks of both hands are shifted signiWcantly to the left during leftward stimulation, introducing a pseudoneglect for the left and right hands. On the other hand, rightward stimulation does not inXuence line bisection tasks. In contrast with these observations, in the present protocol leftward stimulation failed to signiWcantly aVect perfor-
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mance in the time estimation task, although a trend towards time underestimation was observed. DiVerences in the experimental protocol of OKS could partly explain this diVerence. Both phases of standard and test cue duration estimation seem to imply an explicit process of duration encoding. However, in the present protocol a peripheral sensory account based on the time of activation of a population of visual neurones cannot be totally excluded (Efron, 1970). In this case, an implicit process of time perception based on inspecting the time at which neural or perceptual systems supporting visual iconic memory become active would play some role (Dennett & Kinsbourne, 1992; Johnston & Nishida, 2001). Temporal duration can range from sub-second intervals to days and weeks. The temporal scale is critical when considering the neural mechanisms involved in time judgements. In the present study, modulation of time estimation by OKS was selectively observed when using sub-second intervals. In fact, the OKS paradigm did not induce a signiWcant eVect on time estimation of supra-second intervals. This result could likely be explained with reference to the neural pathways mediating the eVects of OKS. In fact, OKS induces a widespread activation of the cerebellum, a neural structure that has been reported to be selectively involved in timing sub-second intervals (Koch, Oliveri, Torriero, Salerno, & Caltagirone, 2006). The cerebellum has also been associated with spatial tasks (Townsend et al., 1999). Thus, the brain pathways connecting the cerebellum with the contralateral cerebral regions could be critical for the integration of spatial and temporal information. Critical regions in this system are the parieto insular vestibular cortex (PIVC) to which other areas of the central sulcus (area 3a) and the prefrontal and frontal cortex are connected to form a “vestibular cortical system” (Faugier-Grimaud, Baleydier, Magnin, & Jeannerod, 1997; Guldin & Grusser, 1998). Galvanic-vestibular stimulation (exciting both semicircular canals and otolitic eVerents) (Goldberg, Smith, & Fernandez, 1984) determines activations in the temporal parietal junction, central and intraparietal sulci and in the premotor regions of the frontal lobe (Lobel, Kleine, Bihan, Leroy-Willig, & Berthoz, 1998). Lesion studies in the monkey (Ventre & Faugier-Grimaud, 1986) show that unilateral surgical ablations of the convexity of the inferior parietal lobule (area 7a) reduce the gain of the slow phases of the VOR (vestibular–ocular response) directed ipsilesionally. The strong anatomo-functional links between vestibular and auditory systems from one hand, and between vestibular system and superior colliculi from the other hand (Crowder, Dawson, & Wylie, 2003) suggest that the observed manipulation of timing by OKS could also extend to the auditory domain. Distortions of duration perception have recently been demonstrated around the time of a saccadic eye movement (Morrone et al., 2005). Making a saccade can also deliver an apparent reversal of temporal order. Eye movement-
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dependent changes in duration perception and spatial distortion (Ross, Morrone, Goldberg, & Burr, 2001) have been related to predictive remapping of receptive Welds in lateral intraparietal area (LIP; Duhamel, Colby, & Goldberg, 1992). Another process that has been associated with saccades is the suppression of magnocellular activity (Burr, Morrone, & Ross, 1994; Ross et al., 2001). This mechanism would be speciWc for the visual modality (Johnston et al., 2006; Morrone et al., 2005). Although the paradigm adopted in the present study is not optimal for inducing saccades, our results could partly be in line with these observations. Whatever the mechanism is, the Wndings of this work are in line with previous work showing that for the brain time and space are not processed separately, but inXuence each other (Burr, 2000). Our study provides another example of the interactions between the two dimensions. One could argue that a bias in temporal estimation could reXect a bias in motor responses. In fact, left-hand responses could be facilitated following leftward- and right-hand responses following rightward optokinetic stimulation blocks. However, this bias cannot account entirely for the present Wndings given that right/left responses for the time estimation task were counterbalanced in the single subjects during each session. An alternative explanation for these results could be the use of a linear representation of time intervals in healthy subjects performing time estimation tasks. According to this hypothesis, an attentional bias towards the right hemispace could also have biased the temporal judgment of the test cue towards overestimation. Thus, the relation linking time and space perception could be similar to that between numbers and space processing, exempliWed by the metaphor of mental number line positing that low numbers are associated with left side space and higher numbers with right-side space (Dehaene, Dupoux, & Mehler, 1990). Future studies with diVerent experimental paradigms could further address this issue. References Basso, G., Nichelli, P., Frassinetti, F., & di Pellegrino, G. (1996). Time perception in a neglected space. Neuroreport, 7(13), 2111–2114. Bisiach, E., Pizzamiglio, L., Nico, D., & Antonucci, G. (1996). Beyond unilateral neglect. Brain, 119, 851–857. Burr, D. C. (2000). Motion vision: are ‘speed lines’ used in human visual motion? Current Biology, 10, 440–443. Burr, D. C., Morrone, M. C., & Ross, J. (1994). Selective suppression of the magnocellular visual pathway during saccadic eye movements. Nature, 371, 511–513. Critchley, M. (1953). The parietal lobes. Hafner Press. Crowder, N. A., Dawson, M. R. W., & Wylie, D. R. W. (2003). Temporal frequency and velocità-like tuning in the pigeon accessory optic system. Journal of Neurophysiology, 90, 1829–1841. Dehaene, S., Dupoux, E., & Mehler, J. (1990). Is numerical comparison digital? Analogical and symbolic eVects in two-digit number comparison. Journal of Experimental Psychology. Human Perception and Performance, 16, 626–641. De Long, A. J. (1981). Phenomenological space-time: towards an experiential relativity. Science, 213, 681–683.
Dennett, D. C., & Kinsbourne, M. (1992). Time and the observer: the where and when of consciousness in the brain. The Behavioral and Brain Science, 15, 183–247. Duhamel, J. R., Colby, C. L., & Goldberg, M. E. (1992). The updating of the representation of visual space in parietal cortex by intended eye movements. Science, 255, 90–92. Efron, R. (1970). EVect of stimulus duration on perceptual onset and oVset latencies. Perception & Psychophysics, 8, 231–234. Enns, J. T., Breahaut, J. C., & Shore, D. I. (1999). The duration of a brief event in the mind’s eye. The Journal of General Psychology, 126, 355– 372. Faugier-Grimaud, S., Baleydier, C., Magnin, M., & Jeannerod, M. (1997). Direct bilateral cortical projections to the vestibular complex in macaque monkey. In P. Thier & H. O. Karnath (Eds.), Parietal lobe contributions to orientation in 3D space (pp. 57–76). Springer. Goldberg, J. M., Smith, C. E., & Fernandez, C. (1984). Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve aVerents of the squirrel monkey. Journal of Neurophysiology, 51, 1236–1256. Guldin, W. O., & Grusser, O. J. (1998). Is there a vestibular cortex? Trends in Neurosciences, 21, 254–259. Harrington, D. L., Haaland, K., & Knight, R. (1998). Cortical networks underlying mechanism of time perception. The Journal of Neuroscience, 18(3), 1085–1095. Johnston, A., Arnold, D. H., & Nishida, S. (2006). Spatially localized distortions of event time. Current Biology, 16, 472–479. Johnston, A., & Nishida, S. (2001). Time perception: brain time or event time? Current Biology, 11, R427–R430. Karnath, H. O. (1996). Optokinetic stimulation inXuences the disturbed perception of body orientation in spatial neglect. Journal of Neurology, Neurosurgery, and Psychiatry, 60, 217–220. KerkhoV, G., Schindler, I., Keller, I., & Marquardt, C. (1999). Visual background motion reduces size distortion in spatial neglect. Neuroreport, 10(2), 319–323. Koch, G., Oliveri, M., Carlesimo, G. A., & Caltagirone, C. (2002). Selective deWcit of time perception in a patient with right prefrontal cortex lesion. Neurology, 59(10), 1658–1659. Koch, G., Oliveri, M., Torriero, S., & Caltagirone, C. (2003). Underestimation of time perception after repetitive transcranial magnetic stimulation. Neurology, 60(11), 1844–1846. Koch, G., Oliveri, M., Torriero, S., Salerno, S., & Caltagirone, C. (2006). Repetitive TMS of the cerebellum interferes with millisecond time processing. Experimental Brain Research, in press, [Epub ahead of print]. Lobel, E., Kleine, J. F., Bihan, D. L., Leroy-Willig, A., & Berthoz, A. (1998). Functional MRI of galvanic vestibular stimulation. Journal of Neurophysiology, 80, 2699–2709. Mattingley, J. B., Bradshaw, J. L., & Bradshaw, J. A. (1994). Horizontal visual motion modulates focal attention in left unilateral spatial neglect. Journal of Neurology, Neurosurgery, and Psychiatry, 57, 1228– 1235. Morrone, M. C., Ross, J., & Burr, D. (2005). Saccadic eye movements cause compression of time as well as space. Nature Neuroscience, 8, 950–954. Pizzamiglio, L., Frasca, R., Guariglia, C., Inoccia, C., & Antonucci, G. (1990). EVect of optokinetic stimulation in patients with visual neglect. Cortex, 26, 541–554. Rao, S. M. et al. (2001). The evolution of brain activation during temporal processing. Nature Neuroscience, 4, 317–323. Rose, D., & Summers, J. (1995). Duration illusion in a train of visual stimuli. Perception, 24, 1177–1187. Ross, J., Morrone, C. M., Goldberg, M. E., & Burr, D. C. (2001). Changes in visual perception at the time of saccades. Trends in Neurosciences, 24, 113–121. Sandor, P. S., Bachtold, D., Henn, V., & Brugger, P. (2000). EVects of optokinetically induced rotatory self-motion on spatial perception and representation. Neuropsychiatry Neuropsychology and Behavioral Neurology, 13(3), 188–194.
C.M. Vicario et al. / Brain and Cognition 64 (2007) 68–73 Schindler, I., & KerkhoV, G. (2004). Convergent and divergent eVects of neck proprioceptive and visual motion stimulation on visual space processing in neglect. Neuropsychologia, 42, 1149–1155. Townsend, J., Courchesne, E., Covington, J., WesterWeld, M., Harris, N. S., Lyden, P., et al. (1999). Spatial attention deWcits in patients with acquired or developmental cerebellar abnormality. The Journal of Neuroscience, 19(13), 5632–5643.
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Tse, P., Intriligator, J., Rivest, J., & Cavanagh, P. (2004). Attention and the subjective expansion of time. Perception & Psychophysics, 66, 1171–1189. Ventre, J., & Faugier-Grimaud, S. (1986). EVects of posterior parietal lesions (area7) on VOR in monkeys. Experimental Brain Research, 62, 654–658. Walsh, V. (2003). A theory of magnitude: common cortical metrics of time, space and quantity. Trends in Cognitive Sciences, 7(11), 483–488.
Optokinetic stimulation aVects temporal estimation in healthy humans Carmelo Mario Vicario a, Carlo Caltagirone b, Massimiliano Oliveri a,b,¤ a
Dipartimento di Psicologia, Università degli Studi di Palermo, Viale delle Scienze, EdiWcio 15, 90100 Palermo, Italy b Fondazione “Santa Lucia” IRCCS, Roma, Italy Accepted 7 December 2006 Available online 29 March 2007
Abstract The representation of time and space are closely linked in the cognitive system. Optokinetic stimulation modulates spatial attention in healthy subjects and patients with spatial neglect. In order to evaluate whether optokinetic stimulation could inXuence time perception, a group of healthy subjects performed “timecomparison” tasks of sub- and supra-second intervals before and after leftward or rightward optokinetic stimulation. Subjective time perception was biased by the direction of optokinetic stimulation. Rightward optokinetic stimulation induced an overestimation of time perception compared with baseline and leftward optokinetic stimulation. These results indicate a directional bias in time perception induced by manipulation of spatial attention and could argue for a mental linear representation of time intervals. © 2007 Elsevier Inc. All rights reserved. Keywords: Space; Time; Perception; Optokinetic stimulation
1. Introduction Mental representations of space and time represent elementary aspects of cognition and play a critical role in planning action and forming decisions in everyday life. Converging evidence from behavioral, neuroimaging and neuropsychological studies suggests the presence of close links between these diVerent cognitive systems (Walsh, 2003). At a behavioural level, spatial factors do aVect the perception of time and other magnitudes. When healthy subjects are asked to carry out tasks in environments built to 1/6, 1/12, or 1/24 of actual size and to stop when 30 min had passed, the ratio of time passed to time estimated scales according to environmental scale (De Long, 1981). The apparent duration of a dynamic stimulus can be manipulated in a local region of visual space by adapting to oscillatory motion or Xicker (Johnston, Arnold, & Nishida, 2006).
*
Corresponding author. Fax: +39 0917028431. E-mail address: [email protected] (M. Oliveri).
0278-2626/$ - see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.bandc.2006.12.002
The importance of visual factors is also supported by recent Wndings, showing that short intervals of time between two successive perisaccadic visual (and not auditory) events are underestimated, indicating a compression of perceived time (Morrone, Ross, & Burr, 2005). These data implicate spatially localised temporal mechanisms in duration perception. The link between spatial and temporal estimation has been also documented at a neural level. Neuropsychological studies show the occurrence of spatial as well as temporal deWcits following right hemispheric damage (Critchley, 1953; Koch, Oliveri, Carlesimo, & Caltagirone, 2002). Harrington, Haaland, and Knight (1998) showed that brain regions more frequently associated with in alterations of temporal perception tasks are the superior and middle frontal gyrus in the right frontal cortex, and the angular and supra-marginal gyri in the right parietal cortex. An important lesson comes from patients with contralesional spatial neglect. These patients overestimate durations of stimuli presented in the neglected space and underestimate durations of stimuli presented in the good right Weld (Basso, Nichelli, Frassinetti, & di Pellegrino, 1996).
C.M. Vicario et al. / Brain and Cognition 64 (2007) 68–73
Neuroimaging studies document an activation of the right parietal cortex in temporal as well as spatial tasks (Rao et al., 2001) and studies using transcranial magnetic stimulation show that disrupting the function of right prefrontal cortex transiently disrupts time perception (Koch, Oliveri, Torriero, & Caltagirone, 2003). A critical role in mediating the link between spatial and temporal perception could be made by attention. In fact, attention is known to inXuence perceived duration and temporal order (Enns, Breahaut, & Shore, 1999; Rose & Summers, 1995; Tse, Intriligator, Rivest, & Cavanagh, 2004). This suggests that procedures that manipulate spatial attention should also aVect temporal estimation tasks. A rich literature documents that manipulation of spatial attention towards the right or the left Weld by optokinetic stimulation is able to directionally inXuence spatial tasks. Fast optokinetic stimulation towards the neglected hemispace (Pizzamiglio, Frasca, Guariglia, Inoccia, & Antonucci, 1990), and slow horizontal background motion to the left (Mattingley, Bradshaw, & Bradshaw, 1994) have been shown to reduce the horizontal line bisection error probably by allocating selective attention to stimuli in the neglected space sector. Mattingley et al. (1994) using the OKS paradigm at speeds that did not elicit optokinetic nystagmus or perceptual after eVects, reported that control subjects were accurate in all conditions, and showed minimal eVects of background conditions. By contrast, patients with left unilateral spatial neglect were sensitive to leftward background motion, showing a signiWcant leftward shift in bisection error, relative to neutral, static, and rightward moving backgrounds. Other studies (KerkhoV, Schindler, Keller, & Marquardt, 1999) provide evidence that coherent visual background motion towards the neglected hemispace signiWcantly modulates the perceived horizontal object size, hence the size distortion, in neglect patients when comparing two stimuli separated in both hemispaces. This Wnding indicates that background motion not only aVects the subjective straight ahead (Karnath, 1996) and subjective midline in line bisection or line extension (Bisiach, Pizzamiglio, Nico, & Antonucci, 1996; Mattingley et al., 1994; Pizzamiglio et al., 1990), but also facilitates the accuracy of spatial judgments concerning two stimuli separated in left and right space. On the same theoretical position is Schindler (Schindler & KerkhoV, 2004), suggesting that visual motion stimulation in neglect alleviates both egocentric deviations (the subjective straight ahead) and allocentric perceptual distortions in neglect with or without visual Weld disorders. The combination of these studies conWrm that the paradigm of optokinetic stimulation is able to transiently move the “attentive focus” towards a speciWc side of space Weld (left vs. right), depending on the direction of optokinetic motion. The rationale behind the present study is that manipulation of spatial attention by means of optokinetic stimulation could be able to inXuence the performance not only in
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spatial tasks but also in temporal tasks, thus arguing for the use of spatial codes in time perception. 2. Subjects and methods Thirty-Wve right-handed graduate students (17 male and 18 female, aged 22–31 years) with normal or corrected vision participated in the studies after providing written informed consent. 2.1. Optokinetic stimulation Optokinetic stimulation (OKS) was performed by presenting 384 series of a sequence of 17 § 2 white line segments, presented on a black background, each with a duration of 50 ms. Stimuli drifted either leftward or rightward, across the full width of a 14⬙ computer monitor, so that the direction of the apparent movement was from left to right and vice-versa in diVerent block of trials. The stroboscopic movement velocity was established functionally for individual subjects on the basis of subjective saccadic response, monitored by visual inspection by one experimenter. The average velocity was of 38°/s. In the Wrst experiment, the subjects were asked to Wxate a central mark on the screen, with the head immobilised over a chin-rest. Central Wxation was monitored by one experimenter. In the second and third experiment, the same paradigm of optokinetic stimulation was done without a central Wxation mark. 2.2. Time estimation task 2.2.1. Experiment 1 Fifteen subjects (8 men, 7 women, aged 21–26 years) participated in this experiment. They were positioned 60 cm opposite a white computer screen (the same used for OKS paradigm) and were required to determine whether a test cue (a red circle) had been presented for a time interval longer or shorter than a memorized standard duration of a reference cue (a blue circle). The duration of the reference cue was 300 ms in all trials. The test cue was presented immediately after the reference cue and its duration was selected randomly using intervals near the standard duration, ranging from 250 to 350 ms (in steps of 10 ms for a total of 10 intervals without presenting the average interval of 300 ms). The computer program selected interval lengths pseudo-randomly, so that each subject received Wve presentations of each interval length within a 50 trials block. The intertrial interval was of 2000 ms. Reference and test cues were presented as pairs at the centre of the screen. Total duration of a block was 130 s (50 trials ¤ (0.3 s reference cue duration + 0.3 s test cue average duration + 2 s intertrial interval)). Subjects indicated their judgment of the test cue’s duration by pressing either of two response buttons with their right and left index Wngers. In half of the trials, a right
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response indicated a smaller duration and a left response a bigger duration of the test cue and vice-versa in the other half of the trials. Time estimation task was performed in three sessions (on three consecutive days) to avoid carry over of aftereVects (optokinetic after-nystagmus) between blocks: a baseline session and a session immediately following a rightward or leftward block of optokinetic stimulation. The order of the sessions was randomised across subjects. In all experiments, subjects performed a 10-trials training on the time estimation task, before entering the main experiment. 2.2.2. Experiment 2 Ten subjects (5 men, 5 women, aged 20–24 years) diVerent from those recruited for experiment 1, participated in this experiment. OKS was performed without a central Wxation mark. All the other parameters of OKS and time estimation were identical to those of experiment 1. 2.2.3. Experiment 3 Ten subjects (4 men, 6 women, aged 20–23 years) participated in this experiment. None of them had participated in the previous experiments. The paradigm of OKS was identical to that of experiment 2 (OKS without a central Wxation mark). The time estimation task was similar to that of experiment 1 and 2 with the exception of the duration of reference and test cues. The duration of the reference cue was of 2000 ms. Test cue was presented immediately after the reference cue and its duration was selected randomly using intervals near the standard duration, ranging from 1500 to 2500 ms (in steps of 100 ms for a total of 10 intervals without presenting the average interval of 2000 ms). The computer program selected interval lengths pseudo-randomly, so that each subject received Wve presentations of each interval length within a 50 trials block. The intertrial interval was of 2000 ms. Reference and test cues were presented as pairs at the centre of the screen. Total duration of a block was 300 s (50 trials ¤ (2 s reference cue duration + 2 s test cue average duration + 2 s intertrial interval)). Response parameters and the other aspects of the experimental protocol were identical to those described for experiment 1.
leftward vs. rightward optokinetic stimulation) as withinsubject factor. Duncan’s post-hoc comparisons were made where appropriate. The level of signiWcance was set at p < .05. 3. Results 3.1. Experiment 1 Fig. 1 shows subjects’ performance in the three main experimental conditions. There was a signiWcant eVect of condition [F(2, 14) D 4, p D .01]. Rightward optokinetic stimulation induced a signiWcant time overestimation compared with both baseline (p D .04) and post-leftward optokinetic stimulation blocks (p D .008); the diVerence between leftward optokinetic stimulation and baseline was not signiWcant. 3.2. Experiment 2 Fig. 2 shows subjects’ performance in the time estimation tasks following OKS without a central Wxation mark. There was a signiWcant eVect of condition [F(2, 9) D 5.24; p D .005]. Rightward optokinetic stimulation induced a signiWcant time overestimation compared with both baseline (p D .01) and post-leftward optokinetic stimulation blocks (p D .003); the diVerence between leftward optokinetic stimulation and baseline was not signiWcant. 3.3. Experiment 3 Fig. 3 shows subjects’ performance in the time estimation task of supra-second intervals. OKS did not induce signiWcant eVects in the time task [F(2, 9) D 0.78; p D .47]. 4. Discussion The main result of the present study is that manipulation of spatial attention towards the right or left space by means
2.3. Data analysis In all experiments responses were analysed by assigning a value of 0 to correct responses, ¡1 to time underestimation (duration of an interval >300–2000 ms judged as shorter than the reference cue), 1 to time overestimation (duration of an interval <300–2000 ms judged as longer than the reference cue). The average responses were analyzed using ANOVA for repeated measures with the factor condition (baseline vs.
Fig. 1. Experiment 1. Percentage change vs. baseline in the time estimation task across the diVerent OKS conditions (grey bars: leftward OKS; white bars: rightward OKS). Error bars indicate 1 SE of mean.
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Fig. 2. Experiment 2. Percentage change vs. baseline in the time estimation task across the diVerent OKS conditions (grey bars: leftward OKS; white bars: rightward OKS). Error bars indicate 1 SE of mean.
Fig. 3. Experiment 3. Percentage change vs. baseline in the time estimation task across the diVerent OKS conditions (grey bars: leftward OKS; white bars: rightward OKS). Error bars indicate 1 SE of mean.
of optokinetic stimulation induces a bias in a standard time estimation task performed immediately after the cessation of optokinetic stimulation. Moving attention towards the right hemispace induces time overestimation, while moving attention towards the left hemispace induces a trend towards time underestimation compared with baseline. This result was present when OKS was done with a central Wxation mark, but it was even more evident in the absence of OKN suppression, with the consequent increase in attention diversion. Optokinetic stimulation has been described to aVect healthy subjects’ exploration of space (Sandor, Bachtold, Henn, & Brugger, 2000). In a standard line bisection task, the bisection marks of both hands are shifted signiWcantly to the left during leftward stimulation, introducing a pseudoneglect for the left and right hands. On the other hand, rightward stimulation does not inXuence line bisection tasks. In contrast with these observations, in the present protocol leftward stimulation failed to signiWcantly aVect perfor-
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mance in the time estimation task, although a trend towards time underestimation was observed. DiVerences in the experimental protocol of OKS could partly explain this diVerence. Both phases of standard and test cue duration estimation seem to imply an explicit process of duration encoding. However, in the present protocol a peripheral sensory account based on the time of activation of a population of visual neurones cannot be totally excluded (Efron, 1970). In this case, an implicit process of time perception based on inspecting the time at which neural or perceptual systems supporting visual iconic memory become active would play some role (Dennett & Kinsbourne, 1992; Johnston & Nishida, 2001). Temporal duration can range from sub-second intervals to days and weeks. The temporal scale is critical when considering the neural mechanisms involved in time judgements. In the present study, modulation of time estimation by OKS was selectively observed when using sub-second intervals. In fact, the OKS paradigm did not induce a signiWcant eVect on time estimation of supra-second intervals. This result could likely be explained with reference to the neural pathways mediating the eVects of OKS. In fact, OKS induces a widespread activation of the cerebellum, a neural structure that has been reported to be selectively involved in timing sub-second intervals (Koch, Oliveri, Torriero, Salerno, & Caltagirone, 2006). The cerebellum has also been associated with spatial tasks (Townsend et al., 1999). Thus, the brain pathways connecting the cerebellum with the contralateral cerebral regions could be critical for the integration of spatial and temporal information. Critical regions in this system are the parieto insular vestibular cortex (PIVC) to which other areas of the central sulcus (area 3a) and the prefrontal and frontal cortex are connected to form a “vestibular cortical system” (Faugier-Grimaud, Baleydier, Magnin, & Jeannerod, 1997; Guldin & Grusser, 1998). Galvanic-vestibular stimulation (exciting both semicircular canals and otolitic eVerents) (Goldberg, Smith, & Fernandez, 1984) determines activations in the temporal parietal junction, central and intraparietal sulci and in the premotor regions of the frontal lobe (Lobel, Kleine, Bihan, Leroy-Willig, & Berthoz, 1998). Lesion studies in the monkey (Ventre & Faugier-Grimaud, 1986) show that unilateral surgical ablations of the convexity of the inferior parietal lobule (area 7a) reduce the gain of the slow phases of the VOR (vestibular–ocular response) directed ipsilesionally. The strong anatomo-functional links between vestibular and auditory systems from one hand, and between vestibular system and superior colliculi from the other hand (Crowder, Dawson, & Wylie, 2003) suggest that the observed manipulation of timing by OKS could also extend to the auditory domain. Distortions of duration perception have recently been demonstrated around the time of a saccadic eye movement (Morrone et al., 2005). Making a saccade can also deliver an apparent reversal of temporal order. Eye movement-
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dependent changes in duration perception and spatial distortion (Ross, Morrone, Goldberg, & Burr, 2001) have been related to predictive remapping of receptive Welds in lateral intraparietal area (LIP; Duhamel, Colby, & Goldberg, 1992). Another process that has been associated with saccades is the suppression of magnocellular activity (Burr, Morrone, & Ross, 1994; Ross et al., 2001). This mechanism would be speciWc for the visual modality (Johnston et al., 2006; Morrone et al., 2005). Although the paradigm adopted in the present study is not optimal for inducing saccades, our results could partly be in line with these observations. Whatever the mechanism is, the Wndings of this work are in line with previous work showing that for the brain time and space are not processed separately, but inXuence each other (Burr, 2000). Our study provides another example of the interactions between the two dimensions. One could argue that a bias in temporal estimation could reXect a bias in motor responses. In fact, left-hand responses could be facilitated following leftward- and right-hand responses following rightward optokinetic stimulation blocks. However, this bias cannot account entirely for the present Wndings given that right/left responses for the time estimation task were counterbalanced in the single subjects during each session. An alternative explanation for these results could be the use of a linear representation of time intervals in healthy subjects performing time estimation tasks. According to this hypothesis, an attentional bias towards the right hemispace could also have biased the temporal judgment of the test cue towards overestimation. Thus, the relation linking time and space perception could be similar to that between numbers and space processing, exempliWed by the metaphor of mental number line positing that low numbers are associated with left side space and higher numbers with right-side space (Dehaene, Dupoux, & Mehler, 1990). Future studies with diVerent experimental paradigms could further address this issue. References Basso, G., Nichelli, P., Frassinetti, F., & di Pellegrino, G. (1996). Time perception in a neglected space. Neuroreport, 7(13), 2111–2114. Bisiach, E., Pizzamiglio, L., Nico, D., & Antonucci, G. (1996). Beyond unilateral neglect. Brain, 119, 851–857. Burr, D. C. (2000). Motion vision: are ‘speed lines’ used in human visual motion? Current Biology, 10, 440–443. Burr, D. C., Morrone, M. C., & Ross, J. (1994). Selective suppression of the magnocellular visual pathway during saccadic eye movements. Nature, 371, 511–513. Critchley, M. (1953). The parietal lobes. Hafner Press. Crowder, N. A., Dawson, M. R. W., & Wylie, D. R. W. (2003). Temporal frequency and velocità-like tuning in the pigeon accessory optic system. Journal of Neurophysiology, 90, 1829–1841. Dehaene, S., Dupoux, E., & Mehler, J. (1990). Is numerical comparison digital? Analogical and symbolic eVects in two-digit number comparison. Journal of Experimental Psychology. Human Perception and Performance, 16, 626–641. De Long, A. J. (1981). Phenomenological space-time: towards an experiential relativity. Science, 213, 681–683.
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