Cerebral Cortex Advance Access originally published online on January 11, 2006
Cerebral Cortex 2006 16(12):1766-1770; doi:10.1093/cercor/bhj111
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Visual Area V5/MT Remembers "What" but Not "Where"
1 Dipartimento di Psicologia Generale, Università di Padova, Via Venezia 8, 35131 Padova, Italy, 2 Department of Experimental Psychology, University Oxford, South Parks Road, Oxford OX1 3UD, UK, 3 Institute of Cognitive Neuroscience and Department of Psychology, University College of London, 17 Queen Square, London WC1N 3AR, UK
Address correspondence to Gianluca Campana, Dipartimento di Psicologia Generale, Università di Padova, Via Venezia 8, 35131 Padova, Italy. Email: gianluca.campana{at}unipd.it.
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Abstract |
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Priming for motion direction has been shown to depend upon the functional integrity of extrastriate area V5/MT. Its retinotopic organization and the interactions recently found between motion adaptation and misperceived localization may suggest, for this area, a role for priming of spatial position in addition to the established priming of motion direction. Disruption of V5/MT with repetitive transcranial magnetic stimulation during the intertrial interval had the effect of abolishing priming of motion direction but no effect in priming of spatial position. These effects cannot be explained in terms of perception or task demands but only in terms of the effects of information irrelevant to the correct performance of the task stored over the intertrial interval. We suggest that the attribute of spatial position might be stored in short-term memory either in earlier areas of the motion pathways such as V3 or in higher cortical areas traditionally associated with the analysis of spatial information, for example, posterior parietal cortex or the frontal eye fields.
Key Words: motion direction • priming • spatial position • TMS, V5/MT
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Introduction |
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Repetition of an object's feature or spatial position facilitates subsequent detection or identification of that object (Maljkovic and Nakayama 1994
, 1996, 2000). This visual priming effect relies on those low-level areas functionally specialized for the analysis and representation of simple stimulus attributes as proposed by the perceptual representation system (PRS) hypothesis (Tulving and Schacter 1990) and the sensory memory hypothesis (SMH, Magnussen and Greenlee 1999). Functionally specialized cells in the secondary visual cortex, however, contribute to the perception of more than one attribute, and the coding of these attributes may interact. For example, cells in V3 may respond to orientation and/or motion (Galletti and others 1990); cells in V4 respond to form and color (Desimone and Schein 1987; Lueck and others 1989); and cells in V5 show tuning for depth, velocity, and direction of motion (Chawla and others 1998; Cornette and others 1998; DeAngelis and others 1998).
These extrastriate areas are retinotopically organized, and it is therefore also possible that they convey spatial as well as attribute information in their responses. The interaction of motion and spatial position is one such case: adaptation to motion can distort subsequent perception of the position of stationary stimuli (Nishida and Johnston 1999; McGraw and others 2002), and the most likely site of this interaction between space and movement is in cortical visual area V5 (Culham and others 2000; Whitney and others 2003; McGraw and others 2004).
In a previous study (Campana and others 2002) we found, in agreement with the predictions of PRS hypothesis and SMH, that priming for motion direction depends on the functional integrity of area V5/MT. Here, we further investigate the interactions between spatial position and visual motion direction in perceptual priming. Several other magnetic stimulation studies have also established that V5/MT continues to be influenced by stimuli once they have ceased to be presented to the retina. Stewart and others (1999), for example, were the first to show that magnetic stimulation over V5/MT interfered with the duration of motion aftereffect (see also Theoret and others 2002). Ellison and others (2003) have also shown that the effects of transcranial magnetic stimulation (TMS) applied to V5/MT depend partly on the stimuli/responses in the previous trial. With the exception of our previous paper (Campana and others 2002), however, these studies do not address the predictions of the PRS hypothesis and SMH.
We begin by replicating our earlier finding showing that priming for motion direction is abolished by TMS applied to area V5/MT (Campana and others 2002). In that study, we systematically varied target position from trial to trial to avoid any possible confounding of repetition of spatial position with repetition of target direction. In the current study, we investigate whether the priming for motion direction occurs when repeating the same target position and if so whether it is still entirely reliant on an intact V5/MT. Using identical stimuli, we establish that spatial priming occurs with a similar pattern to direction priming. We also ask whether there is any interaction between motion direction and target position in determining the priming effect and if so whether area V5/MT is also responsible for priming of spatial position at least with stimuli defined by their direction of global motion. Based on the predictions of the PRS hypothesis and SMH, on our previous studies of V5/MT, and on studies of the neuronal properties of human and nonhuman primate motion areas (although the species differ in important ways, cf., Orban and others 2002), we expected both spatial and motion direction priming to be disrupted by magnetic stimulation over V5/MT.
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Methods |
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Subjects
Eight subjects, 4 males and 4 females, aged between 22 and 34 years (mean = 26.4, standard deviation = 4.4), all right handed, participated. The order of presentation of the various tasks and conditions was counterbalanced across subjects. All subjects understood the information given about magnetic stimulation and gave written informed consent according to the Declaration of Helsinki. The experiment was approved by the Oxford Research Ethics Committee (Oxrec CO2.304).
Stimuli and Procedure
Stimuli were presented on a 17-inch Sony CPD-G200 Trinitron flat-screen monitor with a refresh rate of 100 Hz. Subjects were seated 57 cm from the screen and were restricted by a head and chin rest. Stimuli, responses, and TMS triggering were generated and measured by E-Prime software running on a Pentium IV computer.
Subjects were presented with 6 sinusoidal gratings arranged in 2 columns as shown in Figure 1. Each column was positioned 1.8 degrees from the center of fixation. Each grating occupied a square area of 2.3 x 2.3 degrees of visual angle, the top of the upper grating being 3.95 degrees above fixation, the center of the middle grating being at the level of fixation, and the lower edge of the bottom grating being 3.95 degrees below fixation.
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The gratings had a spatial frequency of 0.5 cycles/degree. The space-averaged luminance of the gratings ranged from 2 to 65 cd/m2, and the background had a luminance of 90 cd/m2. The gratings were shown for 300 ms, and their speed was 14 degree/s.
The 3 sinusoidal gratings on the left were horizontally aligned and always moved in a bottom-up fashion. The 3 gratings on the right were vertically aligned and could move left-to-right or vice versa; 2 of these gratings were always moving in 1 direction, whereas the 3rd grating was always moving in the opposite direction. The odd grating could only be the top one or the bottom one, and the odd direction could be left-to-right or vice versa. Subjects were instructed to fixate the center of the screen, ignore the gratings on the left, and respond to the gratings on the right. The purpose of the gratings on the left was to help the subject to fixate the center of the screen and to engage the right hemisphere in the processing of motion direction irrelevant to the task. An example of the stimuli is shown in Figure 1.
Each trial began with a black fixation cross, which lasted for 500 ms, followed by the 6 moving gratings, which appeared for 300 ms, then a blank screen was shown until the subject responded. Subjects had to respond either to the spatial position or to the direction of motion of the odd grating (in different experimental sessions) using 1 of 2 designated keys on a computer keyboard. After each response was given, a 1000-ms intertrial interval (blank screen) was given, and repetitive transeranial magnetic stimulation (rTMS) (in the TMS condition only) was applied during the 2nd half of the intertrial interval (500 ms).
A target was present on every trial and could appear with same or different position with respect to the previous trial and with same or different motion direction with respect to the previous trial. Spatial position and motion direction with respect to the previous trial were pseudorandomized and counterbalanced across trials. Every session consisted of 60 trials. Accuracy and reaction times were measured.
- Experiment 1: The task was to judge the spatial position of the target (top vs. bottom grating).
- Experiment 2: The task was to judge the motion direction of the target (leftward vs. rightward motion).
- Experiment 2: The task was to judge the motion direction of the target (leftward vs. rightward motion).
Note that subjects were unaware that data analysis was to be done on the basis of previous trial target position or motion direction. The only instruction given to subjects was to judge, on each trial, the spatial position (experiment 1) or the motion direction (experiment 2) of the target (irrespective of position or motion direction of the target in the previous trial). Therefore, this is a purely perceptual task, not a memory task.
As found by Maljkovic and Nakayama (1994, 1996), we expected priming to occur for the "nonresponding feature," that is, for the feature (or position) not directly linked to the motor response. In other words, we expected priming for motion direction when the task was to judge the spatial position and priming for spatial position when the task was to judge the motion direction.
Both tasks were run with and without rTMS over V5/MT during the interstimulus interval.
Magnetic Stimulation
The stimulator was a Magstim 200 Super-Rapid Stimulator delivering current to a 70-mm figure-of-eight coil. Details of the stimulator, coil, selection, and focality of stimulation have been given in detail elsewhere (Ashbridge and others 1997; Campana and others 2002). rTMS was applied to a site on the skull immediately above V5/MT. The coil was held tangential to the skull with the handle pointing backward at 
90 degrees to the axis of the spinal cord. Pulses were delivered at 60% of the maximum output intensity at 10 Hz for 500 ms. The location of V5/MT was determined anatomically (Dumoulin and others 2000) on the magnetic resonance imaging (MRI) structural scan of each subject's brain, and coil position on the skull was guided via a stereotactic image guidance system (Brainsight Frameless) based on the MRI site localization (Fig. 2). To double-check that we were actually stimulating V5/MT, we also provided functional evidence by inducing phosphenes with TMS at 10 Hz for 500 ms and 85% of the maximum output intensity. All subjects perceived phosphenes, and 5 out of 8 of them reported that the phosphenes moved. The average coordinates and standard deviations in stereotaxic Talairach space of left V5/MT of the subjects we tested (x = –45 ± 3, y = –73 ± 5, z = 2 ± 2) were similar to those reported by Dumoulin and others (2000) (x = –47 ± 3.8, y = –76 ± 4.9, z = 2 ± 2.7).
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Statistics
A univariate 3-way repeated measures analysis of variance, with previous direction (direction: same vs. different) by previous position (position: same vs. different) by TMS condition (no TMS vs. TMS), was performed for each experiment. The sphericity assumption was assessed with Mauchly's test and never resulted in significance. The t-tests were used for planned post hoc comparisons.
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Results |
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Accuracy results showed no difference between the different conditions in either of the 2 experiments. Accuracy was above 90% across all conditions and experiments.
Priming for Motion Direction
Response time results showed that when subjects were judging the spatial position of moving stimuli (Fig. 3a), they were faster when the direction of motion was the same as on the previous trial (direction: F1,7 = 6.9, P < 0.05) irrespective of the previous position of the stimulus (position: F1,7 = 0.08, P > 0.05; direction x position: F1,7 = 0.12, P > 0.05). In other words, motion priming is independent of spatial position. When TMS was applied over V5/MT (Fig. 3b), this priming effect was abolished (TMS x direction: F1,7 = 11.6, P < 0.02), again irrespective of the spatial position of the moving stimulus (all other interactions were nonsignificant). Indeed, post hoc tests show a significant effect of direction in the no TMS condition (t7 = –5.8, P < 0.001). This difference is eliminated when the functional integrity of V5/MT is disrupted with TMS (t7 = –0.9, P > 0.05). V5/MT, then, is important for normal direction priming independently of information about the position at which the motion has been presented. Although the effect was not statistically significant in either of the experiments, there seems to be a general decrease in response time when rTMS is applied. As previously reported, this is due to a nonspecific intersensory facilitation (Campana and others 2002).
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Priming for Position
When subjects were judging the direction of motion of the stimuli (Fig. 4), they showed the expected priming for the spatial position of stimuli (position: F1,7 = 18.4, P < 0.005). There was also a significant effect of the direction of motion, which elicited overall slower responses on the same direction trials (F1,7 = 6, P < 0.05) and a significant interaction between motion direction and spatial position (F1,7 = 5.8, P < 0.05): position priming was only observed on trials in which the direction of motion was the same as on the previous trial (t7 = –3.5, P < 0.01), not when the direction of motion was different (t7 = –1.3, P > 0.05). The overall slower responses on the same direction trial are not due to any form of negative priming for motion direction but due to the simple fact that when motion direction is the same and spatial position is different mean response times (RTs) are about 100 ms slower (inhibition of different position) than all other conditions both with and without TMS (Fig. 4). When motion direction does not repeat on successive trials, priming for spatial position is nearly absent both in the facilitatory condition of same position and in the inhibitory condition of different position. This accounts for the slower RTs on same direction than on different direction when position is different (Fig. 4a, gray bars). When TMS was applied over V5/MT, however, unlike in the case of motion priming, there was no change in RT (F1,7 = 0.25, P > 0.05), that is, the large difference between same and different position when motion direction is the same occurs whether or not TMS is applied over V5/MT. In other words, spatial position priming still occurred on same direction trials despite TMS over V5/MT.
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Discussion |
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Our results show that space and motion interact in short-term memory during visual priming. We observed behavioral priming of both direction and spatial position and also an interaction between these 2 attributes, which caused spatial priming to be enhanced when motion direction was repeated. As we expected, TMS over V5/MT abolished priming of visual motion, but our prediction that priming of position would also be affected was not fulfilled, despite an interaction between space and motion in behavioral priming. Thus, there is an asymmetry in the storage of location and direction to be explained. In experiment 1, the priming of motion direction was independent of location, but in experiment 2, the priming of location depended on the direction of motion being the same as on previous trial. One possibility, suggested by a reviewer, is that the subjects employed different strategies on the 2 kinds of trials, encoding and retaining only location explicitly in experiment 1 but trying to remember explicitly both location and direction in experiment 2. A priori, it is not clear why subjects would opt for different strategies in the 2 tasks when each requires only one decision, and there is nothing in the reaction times to suggest that the tasks were of greatly differing difficulty. The subjects of course did not know there was any relevance to the information in previous trials or that any aspect of memory was being tested.
It is highly unlikely that TMS disrupts the sensory aspects of the 2 tasks differentially and independently of the priming effect, first because TMS was delivered during the intertrial interval, not during visual stimulation, and second because TMS had an effect on the "primed feature," not on the "responding feature."
The effects of TMS on motion direction priming can be explained on the basis of the dominance of V5/MT in motion perception and are in accord with our previous results (Campana and others 2002). The absence of any effect of TMS on spatial position priming, despite the fact that position priming is not independent of motion direction (Fig. 4a,b), requires further explanation and could cast light on the pathways and interactions involved in spatial and motion priming.
On the basis of previous psychophysical (Magnussen and Greenlee 1999; Magnussen 2000), brain imaging (Jiang and others 2002), and TMS experiments (Campana and others 2002; McGraw and others 2002), we can be confident that V5/MT is the locus of motion priming. It has also been shown that the posterior parietal cortex (Campana and others 2002) is not necessary for motion priming and that V1 is not critical for mediating motion-dependent spatial mislocalization (McGraw and others 2004). As Pasternak and Greenlee (2005) argued, "elemental sensory dimensions are represented by segregated memory systems that probably involve those cortical areas that are involved in encoding stimulus features." There are at least 2 reasons why V5/MT is not required for holding spatial position information in short-term memory but is required for holding motion direction information: 1) whereas V5/MT is the principal region for encoding motion, it is not the principal area for encoding spatial position and 2) it may of course be involved in conjunction of space and motion (McGraw and others 2002), but there are many other areas that could encode spatial position per se. We suggest therefore that although the motion processing hierarchy is highly dependent on V5/MT, spatial information may interact with motion signals either in other areas of the motion pathway, such as V3, or in higher order cortical areas known to deal with spatial information, such as posterior parietal cortex or the frontal eye fields.
A question remains concerning the reason for a spatial role in V5/MT. One possibility, currently under investigation, is the use of spatial location in computing velocity. Direction of motion, as used in this study, can be computed from relative location signals but velocity, also a key function of V5/MT cells, cannot. In the context of velocity perception, the cells responding to spatial location in V5/MT may be more taxed and more relevant to the task. We may therefore see a more symmetrical behavioral interaction between space and velocity in priming experiments and also conditions under which the retention of spatial information occurs in V5/MT.
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Acknowledgments |
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This study was supported by a Marie Curie European Fellowship, Consiglio Nazionale delle Ricerche (CNR) short-term mobility program grant, and the Wellcome Trust. VW is supported by The Royal Society.
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