Neural responses related to point-light walker perception: A ...

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Neural responses related to point-light walker perception: A ...

Neural responses related to point-light walker perception:

A magnetoencephalographic study

Masahiro Hirai a,b, *, Yoshiki Kaneoke a,c , Hiroki Nakata a,d , Ryusuke Kakigi a,c

a

Department of Integrative Physiology, National Institute for Physiological Sciences, 38 Nishigonaka, Myoudaiji, Okazaki, 444-8585, Japan

b

Japan Society for the Promotion of Science (JSPS), Japan

c

Department of Physiological Sciences, School of Life Sciences, The Graduate University for Advanced Studies, Japan

d

School of Health Sciences, Nagoya University, Nagoya, Japan

article info

Article history:

Accepted 6 September 2008

Available online 18 October 2008

Keywords:

Biological motion

Magnetoencephalography

Motion detection

Inversion effect

Form-from-motion

1. Introduction

abstract

Our visual system can extract much information on human actions

from very limited cues. Biological motion (BM) is the phenomenon

whereby one can perceive vivid actions with only

twelve point-lights attached to the joints (Johansson, 1973). Interestingly,

we can extract rich information from point-lights motion,

such as identifying individuals (Cutting and Kozlowski, 1977), gender

(Kozlowski and Cutting, 1977) or emotion (Dittrich, 1993). Recently,

BM perception was also studied in the context of social

perception (Allison et al., 2000). For example, a behavioral study

revealed that the performance on a BM detection task in 8- to

10-year-old children with autism was poor compared with typically

developing children; however, the performance on the static

version of a form-from-motion task was equivalent between these

groups (Blake et al., 2003). Not only behavioral studies, but also

* Corresponding author. Address: Department of Integrative Physiology, National

Institute for Physiological Sciences, 38 Nishigonaka, Myoudaiji, Okazaki, 444-8585,

Japan. Tel.: +81 564 55 7811; fax: +81 564 52 7913.

E-mail address: hirai@nips.ac.jp (M. Hirai).

Clinical Neurophysiology 119 (2008) 2775–2784

Contents lists available at ScienceDirect

Clinical Neurophysiology

journal homepage: www.elsevier.com/locate/clinph

Objective: The aim of this study is to extract magnetoencephalographic responses relating to the processing

of point-light walker (PLW).

Methods: To attenuate neural activities in the lower visual areas, we presented a scrambled-PLW as a first

stimulus and then either an upright- or inverted-PLW/scrambled-PLW as a second stimulus. Each point of

the scrambled-PLW stimulus had the same velocity vector as the points of the PLW stimulus, but points

were interchanged randomly.

Results: The peak neuromagnetic response to the first stimulus was observed at around 250 ms after

stimulus onset, whereas the peak latency in response to second stimulus was around 350 ms after stimulus

onset. The peak amplitude induced by the PLW stimulus was significantly larger than that by the

scrambled-PLW during the second stimulus. Moreover, the signal source of the responses to the PLW

was estimated to lie in the occipitotemporal region, more anterior than the source of the response to

the first stimulus.

Conclusions: These findings indicate that the response to the first stimulus reflects general motion processing,

while responses to the second stimuli are involved in PLW processing.

Significance: This is the first evidence to specify a single neuromagnetic response to a PLW stimulus.

Ó 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights

reserved.

many neuroimaging studies have investigated the neural correlates

underlying BM perception, and suggest that the posterior

superior temporal sulcus (pSTS) plays an important role in BM perception

(for examples, see (Bonda et al., 1996; Grossman et al.,

2000, 2005; Grossman and Blake, 2001; Howard et al., 1996; Peuskens

et al., 2005; Saygin et al., 2004; Vaina et al., 2001).

The previous neuroimaging studies were not able to provide an

accurate temporal assessment of the underlying neural changes

that support the rapid psychological phenomenon such that the

human visual system detects meaningful human behaviors via

BM stimuli with only 200 ms exposure (Johansson, 1976). Recent

event-related potential (ERP) and magnetoencephalography

(MEG) studies have tried to clarify the neural dynamics underlying

BM perception (for examples, see (Hirai et al., 2003; Jokisch et al.,

2005; Pavlova et al., 2004, 2006). In ERP studies, two components

were observed at around 200 ms and 240–330 ms after onset of an

upright version of a point-light walker (PLW) stimulus; the amplitudes

of both components were significantly different from those

in response to a scrambled version of the upright PLW stimulus

(Hirai et al., 2003; Jokisch et al., 2005). In a MEG study, the response

to an upright PLW stimulus was modulated by periventricular

1388-2457/$34.00 Ó 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.

doi:10.1016/j.clinph.2008.09.008


2776 M. Hirai et al. / Clinical Neurophysiology 119 (2008) 2775–2784

lesions at around 140–170 ms, but there was no difference in the

response to a scrambled version of the upright PLW stimulus

(Pavlova et al., 2006). Thus, these studies show that the neural response

related to PLW perception occurs within 200 ms after the

stimulus onset. It is not clear, however, whether the response is related

to the detection of the walker via the specific motions of the

point-lights or the detection of the figure of a walker based on the

specific alignment of the point-lights at the beginning of the stimulus.

The visual stimuli used to evoke a PLW in these studies were

composed of multiple frames of point-lights, each of which indicates

the posture of a walking human at each moment. Thus, the

initial frame can evoke the impression of a human figure, whereas

the control scrambled version of a PLW does not. Because recent

ERP studies have reported that the static human body-sensitive

ERP component is observed at around 170–190 ms in the occipitotemporal

electrode (Peelen and Downing, 2007; Stekelenburg and

de Gelder, 2004; Thierry et al., 2006), the early evoked responses

might reflect the human figure evoked by the alignments of

point-lights. Further, in previous studies, the visual stimuli were

simply presented; thus, it is possible that the neural signals were

also confounded by neural signals from the lower and higher visual

areas, such as stimulus onset or motion onset responses.

Specifically, we developed a stimulus condition to evoke a PLW

and a scrambled version of the PLW with the same initial pointlight

alignments to investigate the timing of the response related

to the detection of the PLW from the motion of the point-lights

(‘double stimulus presentation’ method, see Methods). In this

experiment, we tried to extract the neural response relating to a

PLW stimulus by our developed experimental stimulus.

2. Methods

2.1. Participants

Twelve healthy participants (4 females and 8 males) with normal

or corrected-to-normal vision volunteered (mean age = 30.8,

SD = 6.1 years). All participants provided informed consent for

the experimental protocol, which was approved by the Ethics Committee

of the National Institute for Physiological Sciences.

2.2. Experimental stimuli and task

We applied a ‘double stimulus presentation’ method to extract

the VEF response relating to PLW perception. Previous

MEG studies of motion perception have attempted to extract

the VEF response relating to coherent and incoherent motion

perception by adopting a ‘double stimulus presentation’ method

(Aspell et al., 2005; Handel et al., 2007; Lam et al., 2000;

Nakamura et al., 2003; Sofue et al., 2003). In these experiments,

the stimulus sequence consisted of two phases: an incoherent

motion was presented for several milliseconds or several seconds

and coherent motion followed immediately. It is well known

that a long duration of the incoherent phase ensures that the

general motion onset response, which occurs in response to

the onset of incoherent motion, is well over before the transient

response to the change to coherent motion begins. Thus, this

method has the advantage of differentiating between general

motion onset responses and coherent motion onset responses

(Aspell et al., 2005). In the present experiment, we applied this

technique to extract the VEF response to a PLW stimulus, as

shown in Fig. 1. We used a scrambled point-light walker (SCB;

see later) as a prestimulus (S1), a point-light walker (PLW) as

a target stimulus (S2) to attenuate the motion-related VEF response

to S2. In the following section, the precise procedures

are described.

2.2.1. Stimuli

We used four kinds of point-light motion stimuli: (1) an upright

point-light walker (PLW); (2) an upright scrambled point-light

walker (SCB); (3) an inverted point-light walker (iPLW); and (4)

an inverted scrambled point-light walker (iSCB). The PLW (basic

stimulus) is a conventional point-light walker stimulus, which

was generated from computer algorithms developed by Cutting

(Cutting, 1978). The animation consisted of 14 moving point-lights

attached to the head and main joints, and the animation looked as

if an individual was walking on a treadmill. This produced an animation

in which a walking motion was immediately obvious to

participants. Importantly, this animation is periodic; thus, the

coordinates of point-lights in the first and final frames were identical

(Fig. 1). In this experiment, the speed of gait was two steps per

second, and the frame duration was 33 ms, which produced a

smooth animation. For the SCB animation, the number of pointlights

and the velocity vector were the same as those in the PLW

animation, but each point was interchanged randomly. Thus, the

participants perceived neither a walking figure nor a global direction

change, but only a swaying point-light motion. For the iPLW

animation, the animation was rotated 180 degrees. Both iPLW

and iSCB animations were created by rotating the PLW and SCB

animations.

The present experiment consisted of four conditions (PLW condition,

SCB condition, iPLW condition and iSCB condition). For

example, in the PLW condition, the SCB stimulus was presented

for 1980 or 2970 ms during the S1 period; then, the PLW stimulus

was presented immediately. Thus, the participants perceived

swaying point-lights that transiently formed a human figure. In

the SCB condition, the SCB stimulus was presented for 1980 or

2970 ms during the S1 period; then, another version of the SCB

stimulus was presented immediately. Thus, the participants perceived

swaying point-lights that transiently formed a different pattern.

A cue animation (S1) was presented for 1980 or 2970 ms for

the following reasons. First, as mentioned above, previous MEG

studies of motion perception have indicated that a long duration

of prestimulus (incoherent motion) ensures that the general motion

onset response, which occurs in response to the onset of a

prestimulus (incoherent motion), is well over before the transient

response to the change to a target stimulus (coherent motion) begins.

In other words, this method enables us to detect the VEF response

relating to the change in stimulus. Based on this

methodology, previous MEG studies of motion perception set the

duration of the prestimulus at 500 ms (Handel et al., 2007),

883 ms (Aspell et al., 2005), 1293, 2976, or 4659 ms (Nakamura

et al., 2003). Second, the duration of one cycle of walking was

990 ms; thus, we used stimulus durations of multiples of 990 ms,

and, to avoid an effect of the transition of the animation on anticipation,

we used two S1 durations. Finally, to get the baseline period

for S2, we allowed sufficient time for the MEG waveforms to

return to baseline. Based on these previous MEG studies and the

stimulus properties of the PLW stimulus, we set the duration of

S1 to 1980 or 2970 ms. For the PLW and SCB conditions, the S1

was the SCB animation, whereas for the iPLW and iSCB conditions,

the S1 was the iSCB animation. Importantly, for both SCB and iSCB

conditions, the pattern of SCB and iSCB animations in S1 and S2

was quite different. Thus, it was easy for participants to notice

the switch from S1 to S2 animations. In a preliminary behavioral

study, we also confirmed the ability of participants to detect

changes between S1 and S2 stimuli, in all conditions. The result

indicated that there was no statistical difference in participants’

ability to detect changes in all conditions. After the presentation

of S2, a blank screen with a fixation point was displayed for 960–

1056 ms, randomly.

Animations were displayed subtending a visual angle of 3 3°

on a projector screen at a viewing distance of 200 cm. All points


S1

(1980-2970 ms)

were white (1.6 cd/m 2 ) against a black background (0.4 cd/m 2 ). A

red fixation point was presented at the center of the screen

throughout the experiment.

2.2.2. Experimental task and design

Experiment consisted of seven sessions. In one session, each

experimental condition (PLW condition, SCB condition, iPLW condition

and iSCB condition) was presented 12 times randomly. To

maintain their attention at the center of the screen, participants

were instructed to press a button with their right thumb when static

point-lights were presented instead of the S2. In a single session,

a static point-lights stimulus was presented 2–4 times

randomly. In the PLW and SCB conditions, S1 (SCB) was presented

168 times, and the S2 stimulus (PLW or SCB) was presented 84

times. In the iPLW and iSCB conditions, the S1 stimulus (iSCB)

was presented 168 times, and the S2 stimulus (iPLW or iSCB)

was presented 84 times. To maintain their attention at the center

of the screen, participants were instructed to press a button with

their right thumb when static point-lights were presented instead

of the S2 stimulus.

After the experiment, participants were presented with each visual

stimulus and were then required to answer verbally what the

presented stimuli (PLW, iPLW, SCB and iSCB animations) looked

like. In the verbal task, participants were allowed to describe freely

whatever came to mind.

2.3. MEG recordings

Smooth transition

Different pattern of SCB animation

VEFs were recorded using a helmet-shaped 306-channel detector

array (Vectorview, ELEKTA, Neuromag, Helsinki, Finland),

which comprised 102 identical triple sensor elements. Each sensor

element consisted of two orthogonal planar gradiometers and one

magnetometer coupled to a multi-SQUID (superconducting quantum

interference device), thus providing three independent measurements

of the magnetic fields. We analyzed the MEG signals

recorded from the 204 planar-type gradiometers as in a previous

M. Hirai et al. / Clinical Neurophysiology 119 (2008) 2775–2784 2777

S2

Time

(a) PLW condition

study (Noguchi et al., 2004), because the signals from these planar

sensors are strongest when the sensors are located just above local

cerebral sources (Hamalainen, 1995). Eye position was also monitored

using an infrared eye tracker (Iscan Pupil/Corneal Reflection

Tracking System, Cambridge, MA) and trials contaminated by eye

movements (>0.5°) or blinks were rejected. Data on MEG signals

were recorded using 0.1–100 Hz band-pass filters and digitized at

500 Hz.

In advance of the MEG recordings, four head position indicator

(HPI) coils were placed at specific sites on the scalp. To determine

the exact head location with respect to the MEG sensors, an electric

current was supplied to the HPI coils, and the resulting magnetic

fields were measured by the magnetometer. These procedures allowed

us to align the individual head coordinate system. The locations

of HPI coils with respect to three anatomical landmarks

(nasion and bilateral preauricular points) were also measured

using a 3-D digitizer to align the MEG coordinates with magnetic

resonance (MR) images obtained using a 3-T MRI system (Allegra,

Siemens). We adopted the head-based coordinate system used in

our previous study (Wasaka et al., 2003). The x-axis was fixed with

the preauricular points, the positive direction being to the right.

The positive y-axis passed through the nasion; thus, the z-axis

pointed upward.

2.4. Data analyses

static frame

Time

(b) SCB condition

S2

(990 ms)

Time

(c) Target

Fig. 1. Detail of the experimental procedure. This figure represents the experimental procedure for (a) the PLW condition, (b) the SCB condition and (c) target stimulus. In the

PLW condition, S1 is an upright SCB stimulus and S2 is an upright PLW stimulus. In the SCB condition, S1 is an upright SCB stimulus and S2 is a different pattern of the upright

SCB stimulus, as shown in (b). The end frame of the S1 stimulus is identical to the start frame of the S2 stimulus. This enables us to produce a smooth transition from S1 to S2.

In off-line analyses of MEG recordings, a 0.1–30 Hz bandpass filter

was applied (Hirai et al., 2005) to the data and the signals evoked

by six visual stimuli (two S1 stimuli and four S2 stimuli) were averaged

separately. Trials in which the MEG signal variation exceeded

3000 fT/cm were discarded. The analysis window was extended for

1000 ms following the onset of both S1 and S2. A prestimulus period

of 200 ms was used as the baseline for both S1 and S2. The baseline

period for S2 was defined as the 200-ms time window before the offset

of S1. The averaged MEG signals in planar sensors were then calculated

from the strength of the synthesized vector [gradient


strength (GS):

ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi

ðdBz=dxÞ 2 þðdBz=dyÞ 2

2778 M. Hirai et al. / Clinical Neurophysiology 119 (2008) 2775–2784

q

] from two magnetic fields re- 3.2. Verbal report

corded by orthogonal planar-type gradiometers at a sensor’s location

to obtain a better measurement of the magnetic activity After the experiment, all participants reported that the PLW

below a sensor (Renvall and Hari, 2002; Tanaka et al., 2007). The animation had the appearance of a ‘walking human figure’ and that

location showing the largest magnetic field gradient deflection pro- the iPLW animation looked like an inverted version of the PLW anivides

the best measurement of cortical activation when a localized mation; however, all participants perceived both SCB and iSCB ani-

cortical area is activated (Hämäläinen et al., 1993). This calculation

was carried out for all 102 sensors individually. Next, we used the

mations as a swaying of point-lights.

obtained GS waveforms to look for a peak sensor showing the responses

to both S1 and S2 stimuli with the greatest amplitudes be-

3.3. VEF waveforms

tween 200 and 500 ms after the onset of the stimulus in both All participants had a vivid impression of a walking figure from

hemispheres, as in a previous MEG study (Tanaka et al., 2007). This the upright PLW stimulus. However, the VEF elicited by S2 was

time window was also based on previous MEG studies (Amano et al., very poor in three participants. That is, we could not observe sig-

2005; Amano et al., 2006; Lam et al., 2000; Noguchi et al., 2004). We nificant deflection (>2 SD of the fluctuation level in baseline period

used the GS value instead of the dipole strength because we evalu- of each sensor) or clear peaks in three participants; thus, we exated

direct cortical responses, not estimated cortical responses. The cluded the data from these three participants from the waveform

distributions of the selected sensors for all conditions across partic- analysis.

ipants are shown in the left panels in Fig. 2(A). Most of the selected Fig. 2(B–E) shows the VEF waveforms evoked by the four condi-

sensors were located in the bilateral occipitotemporal regions. The tions in one representative participant. A peak response to S1

peak amplitude and latency (the peak latency was calculated by (MS1) was found at around 200–300 ms after stimulus onset, for

subtracting 33 ms as a projector delay) of prominent responses in both SCB (Fig. 2B and C) and iSCB (Fig. 2D and E) stimuli. On the

the GS waveform were then measured at the peak sensors (Tanaka other hand, the peak response to S2 (MS2), between 300 and

et al., 2007).

400 ms after stimulus onset, was manifest only in the PLW condi-

To estimate the locations of the cortical activities that protion (Fig. 2B and D). Compared with the PLW stimulus, the peak reduced

the magnetic fields (Sarvas, 1987), the single current disponse to the SCB condition was very weak. To quantify the VEF

pole model was used in bilateral hemispheres. In each responses to the four conditions, we carried out a statistical analy-

hemisphere, the equivalent current dipole (ECD) at the peak of

each VEF component was estimated from the magnetic signals

sis as follows.

obtained from 28 sensors, including the peak sensor. We selected

the sensors so that the peak sensor was centrally located.

3.4. Peak amplitude and latency of MS1

The distributions of selected sensors are shown in the right pan- In order to elucidate the VEF responses to S1 stimuli (moels

in Fig. 2(A). The sensors from only one hemisphere were setion related response), we carried out a two-way ANOVA with

lected for the fit of the ECD in that hemisphere. In each hemisphere (left, right) and orientation (upright, inverted) as

participant, the numbers and locations of selected sensors were factors. Neither amplitude nor latency was statistically different

identical for all conditions. This analysis resulted in a 3D loca- [amplitude: Fs < 0.5, ps > 0.5; latency: Fs < 4.9, p > 0.06].

tion, moment and direction for each ECD in a spherical conduc- Fig. 3(A) shows the grand-averaged waveforms, and Fig. 4(A)

tor model, which was based on the subjects’ MRI scans. The and (C) show the averaged peak amplitude and latency of

goodness-of-fit (GOF) value of an ECD was calculated to show

in percentage terms how much the dipole accounts for the mea-

MS1, respectively.

sured field variance. We adopted ECD data with a GOF above

80%.

3.5. Peak amplitude and latency of MS2

We calculated the statistical differences among the peak To elucidate the VEF responses to the PLW stimulus, we carried

amplitudes and latencies of VEFs elicited by the SCB and iSCB out a three-way ANOVA with hemisphere, orientation and stimu-

S1 stimuli, and by the PLW, iPLW, SCB and iSCB S2 stimuli, in lus as factors. For peak amplitude, only a main effect of stimulus

both hemispheres. We also calculated the statistical differences was significant [F(1,8) = 8.2, p < 0.05] and the main effect of hemi-

in peak latencies between VEFs elicited by S1 and S2 stimuli sphere approached significance [F(1,8) = 5.1, p = 0.05]. Subsequent

in both hemispheres. For the VEFs elicited by S1 stimuli, the analysis revealed that the peak amplitude of the PLW stimulus was

peak amplitudes and latencies were subjected to a two-way significantly larger than that of the SCB stimulus (41.0 ± .8 vs.

analysis of variance (ANOVA) with hemisphere (left, right) and 30.9 ± .0 fT/cm; mean ± SE). For peak latency, no significant effect

orientation (upright, inverted) as factors. For the VEFs elicited was observed (Fs < 1.6, ps > 0.2). The grand-averaged GS peak

by S2 stimuli, the peak amplitudes and latencies were subjected waveforms are shown in Fig. 3(A), and the grand-averaged peak

to a three-way ANOVA with hemisphere (left, right), orientation amplitude and latency of MS2 are shown in Fig. 4(B) and (D),

(upright, inverted) and stimulus (PLW, SCB) as factors. In the

ECD analysis, ECD results satisfying our criterion (GOF > 80%)

respectively.

were only obtained in the PLW and iPLW conditions. We then

applied a two-way ANOVA with stimulus (S1, S2) and orienta-

3.6. Comparison of MS1 and MS2

tion (upright, inverted) as factors to each coordinate in both In order to confirm the difference between MS1 and MS2,

hemispheres.

that is, to clarify the differential VEF response to the general motion

stimulus and the PLW stimulus, we performed a three-way

ANOVA analyzing the peak latencies of MS1 and MS2. The main

3. Results

effect of stimulus was significant [F(2,16) = 11.8, p < 0.01]. Subsequent

analysis revealed that the latencies of the responses to S2

3.1. Behavioral performance

stimuli were significantly longer than those of the responses to

S1 stimuli [S1 vs. S2 (PLW): 254.2 ± 11.4 vs. 355.0 ± 14.4 ms,

The rate at which subjects correctly performed target detection p < 0.05; S1 vs. S2 (SCB): 254.2 ± 11.4 vs. 324.4 ± 13.5 ms,

was 98.6 ± 4.5% (mean ± SD).

p < 0.05, mean ± SE].


Gradient Strength (GS) [fT/cm]

Gradient Strength (GS) [fT/cm]

Gradient Strength (GS) [fT/cm]

Gradient Strength (GS) [fT/cm]

140

120

100

80

60

40

20

0

-2

00

140

120

100

80

60

40

20

0

-2

00

140

120

100

80

60

40

20

0

-2

00

140

120

100

80

60

40

20

0

-2

00

Sensors

14

0

MS1

MS1

SCB

[fT/cm]

140

0 200

0 40

Time [ms]

600 800

MS1

iSCB

[fT/cm]

140

0 200

0 40

Time [ms]

600 800

70

70

S1

1980ms or 2970ms

0

SCB

[fT/cm]

140

0 200

0 40

Time [ms]

600 800

MS1

0 200

0 40

Time [ms]

600 800

M. Hirai et al. / Clinical Neurophysiology 119 (2008) 2775–2784 2779

N

8

0

70

0

0

iSCB

[fT/cm]

140

70

0

180

0

280

0

180

0

280

0

180

0

280

0

180

0

280

0

MS2

1980 218

0 238

0 258

0 278

0 298

0

2970 317

0 337

0

Time [ms]

357

0 377

0 397

0

MS2 ?

MS2

PLW time

[fT/cm]

140

1980 218

0 238

0 258

0 278

0 298

0

2970 317

0 337

0

Time [ms]

357

0 377

0 397

0

iPLW time

[fT/cm]

140

1980 218

0 238

0 258

0 278

0 298

0

2970 317

0 337

0

Time [ms]

357

0 377

0 397

0

MS2 ?

1980 218

0 238

0 258

0 278

0 298

0

2970 317

0 337

0

Time [ms]

S2

990ms

357

0 377

0 397

0

70

0

SCB time

[fT/cm]

140

70

0

70

0

iSCB time time

[fT/cm]

140

70

0

(S1 = 1980 ms)

(S1 = 2970 ms)

(S1 = 1980 ms)

(S1 = 2970 ms)

(S1 = 1980 ms)

(S1 = 2970 ms)

(S1 = 1980 ms)

(S1 = 2970 ms)

Fig. 2. (A) Left: The distribution of the selected peak sensors across 9 participants in all conditions. The number of times each sensor was the selected peak sensor in a given

condition was summed across participants in all conditions and color-coding on the contour map depicted over the topographical layout of the 102 sensor positions. Right:

The distribution of the selected sensors for dipole estimation across 8 participants. The color at each location indicates for how many subjects the sensor was selected for

dipole estimation. (B–E) For better understandability, Gradient Strength (GS) waveforms were extracted from 10 sensors that were selected from among the peak sensors in

all experimental conditions (one representative participant). The locations of sensors are indicated by white circles superimposed on the isocontour map. (B) Time course of

GS waveforms in the PLW condition. (C) SCB condition. (D) iPLW condition. (E) iSCB condition. In all conditions, the peak component in response to S1 was observed at around

200–300 ms after the stimulus onset. For the VEF peak elicited by S2, a clear peak was observed in response to the PLW stimulus at around 300–400 ms after stimulus onset,

but not in response to the SCB stimulus. Isocontour maps of each peak component indicate that activity was present in the occipitotemporal region, mainly in the right

hemisphere.


2780 M. Hirai et al. / Clinical Neurophysiology 119 (2008) 2775–2784

GS Peak Amplitude [fT/cm]

60

50

40

30

20

10

Sub

1

Sub

4

0

-200 0 200 400

Time [ms]

S2 PLW

S2 SCB

S2 iPLW

S2 iSCB

S2 PLW

S2 SCB

S2 iPLW

S2 iSCB

Left Hemisphere

-200 0 200 400 600 800 1000

[ms]

-200 0 200 400 600 800 1000

[ms]

600

800

Sub

2

S2 PLW

S2 SCB

S2 iPLW

S2 iSCB

Sub

5

S2 PLW

S2 SCB

S2 iPLW

S2 iSCB

100

0

GS Peak Amplitude [fT/cm]

0

-200 0 200 400

Time [ms]

-200 0 200 400 600 800 1000

[ms]

60

50

40

30

20

10

Right Hemisphere

-200 0 200 400 600 800 1000

[ms]

Sub3

S2 PLW

S2 SCB

S2 iPLW

S2 iSCB

S2 PLW

S2 SCB

S2 iPLW

S2 iSCB

S1 SCB

S1 iSCB

S2 PLW

S2 SCB

S2 iPLW

S2 iSCB

600 800 1000

50 fT/cm

-200 0 200 400 600 800 1000

[ms]

Sub6

-200 0 200 400 600 800 1000

[ms]

Fig. 3. (A) Grand-averaged peak GS waveform (response to S1, S2) from the single sensor that recorded the maximum amplitude in each participant (N = 9) in both

hemispheres. (B) GS waveforms (from 36 bilateral occpitotemporal sensors; the location of selected sensors is shown in the right upper panel) in the S2 PLW, S2 SCB, S2 iPLW

and S2 iSCB conditions of six participants. Prominent response was observed in PLW and iPLW stimulus, however, the weak responses were also observed in SCB and iSCB

stimulus in some participants.


GS Peak Amplitude [fT/cm]

A

90

80

70

60

50

40

30

20

10

0

3.7. ECD analyses

GS Peak Amplitude [fT/cm]

B

90

80

70

60

50

40

30

20

10

* p


2782 M. Hirai et al. / Clinical Neurophysiology 119 (2008) 2775–2784

All the dipoles for MS1 and MS2 seemed to lie within the occipitotemporal

region. Notably, the dipole for MS1 seemed to lie within

a small region around the middle temporal area, and that for

MS2 seemed to lie around the posterior temporal area, probably

in the posterior part of the superior temporal gyrus or sulcus

region.

We calculated the statistical significance of differences in x, y

and z coordinates to evaluate the locations of dipoles (Table 1).

For the x coordinate, the main effect of stimulus was not significant

in either hemisphere (LH: Fs < 3.5, ps > 0.1; RH: Fs < 4.9, ps > 0.06).

For the y coordinate, the main effects of stimulus [F(1,7) = 7.8,

p < 0.05] and orientation [F(1,7) = 21.9, p < 0.01] were significant

in the left hemisphere. This indicates that the dipole location of

the responses to S2 stimuli was significantly more anterior than

that of the responses to S1 stimuli (S1 vs. S2: 33.7 ± 4.2 vs.

9.2 ± 6.6 mm; mean ± SE), and also that the dipole in the inverted

condition was significantly more anterior than that in the upright

condition (Upright vs. Inverted: 25.0 ± 6.5 vs. 17.9 ± 6.0 mm;

mean ± SE). In the right hemisphere, the main effect of stimulus

approached significance [F(1,7) = 5.4, p = 0.05] (S1 vs. S2:

25.2 ± 4.4 vs. 13.1 ± 3.7 mm; mean ± SE). For the z coordinate,

the main effect of stimulus was not significant in the left hemisphere

(Fs < 2.5, ps > 0.16). In the right hemisphere, the main effect

of orientation was significant [F(1,7) = 10.7, p < 0.05]. This implies

that the dipole location of the response to an inverted stimulus was

significantly more superior than that of the response to an upright

stimulus (Upright vs. Inverted: 58.3 ± 3.0 vs. 71.4 ± 3.8 mm;

mean ± SE).

4. Discussion

Using a double stimulus presentation (S1 and subsequent S2)

method, we extracted the two response components (MS1 and

MS2): the first component (MS1) was evoked by the onset of the

SCB/iSCB stimulus (S1) and the second component (MS2) was

evoked by the transition from the first SCB stimulus to the subsequent

PLW or another SCB stimulus (S2). MS1 showed a peak

amplitude at around 254 ms after S1 onset, whereas MS2 had a

peak amplitude at around 324–355 ms after S2 onset. The MS2 response

was stronger when the PLW stimulus was used as S2 compared

with when the SCB was used as S2. We consider that MS1

reflects neural activity related to the detection of point-lights motion

and that MS2 reflects neural activity more related to the

detection of PLW.

4.1. The function of the MS2 component

We consider that the response component (MS2) represents

neural activity related to the perception of PLW from the motion

of point-lights. This is because the response amplitude was significantly

larger with the PLW stimulus than with the SCB stimulus,

even though both visual stimuli (PLW and SCB) had the same num-

Table 1

The 3D coordinates of ECDs in response to each stimulus (N =8)

ber of point-lights and identical velocity vectors. The only difference

between PLW and SCB stimulus was the spatial alignment

of point-lights; therefore, it is natural to presume that the differential

neural response would reflect the presence of a coherent form

conveyed by point-light motion. At a glance, the grand averaged

amplitude induced by the SCB stimulus was quite weak compared

with the PLW stimulus, thus it might be thought that no responses

would be observed at the SCB stimulus in the S2 period; however,

as shown in Figs. 2 and 3B, slight MS2 responses were observed in

SCB and iSCB stimulus on an individual level. This implies that the

MS2 was observed even in the condition when spatial point-light

motion switched from S1 to S2; however, it was not enough to elicit

a prominent response of MS2.

The attenuation of the MS2 component in SCB and iSCB stimuli

was mainly due to the presentation method introduced here. In the

present experiment, we introduced a ‘double stimulus presentation’

method; thus, the neural responses relating to onset- or motion-related

responses would be observed in the S1 period and

attenuated in the S2 period. Therefore, neural responses relating

to a PLW perception from point-lights motion would be attenuated

during the S2 period when the stimulus was SCB or iSCB, because

both stimuli did not elicit the impression of a coherent form from

point-light motion.

The peak latency of MS2 corresponds to the second component

seen in previous ERP studies (Hirai et al., 2005; Jokisch et al., 2005).

Previous studies also reported that the early neural response was

modulated by PLW and SCB stimuli at around 170–200 ms (Hirai

et al., 2003; Jokisch et al., 2005). Interestingly, the MEG response

to the upright PLW stimulus was modulated by periventricular lesions

at around 140–170 ms, whereas there is no difference in the

response to a scrambled version of the upright PLW stimulus (Pavlova

et al., 2006). In contrast to these studies, we did not find an

earlier response component (within 200 ms) that was different

from that for SCB. This discrepancy can be explained by the stimulus

presentation method. In this study, we presented the SCB

stimulus first, and then the PLW stimulus. Thus, the brain response

(MS2) would be related to the motion pattern that represents a human

figure. By contrast, previous studies presented the PLW stimulus

at the beginning. Thus, the brain response to this stimulus

condition can be related to the luminance change, specific alignment

of the point lights at the first frame, and the subsequent motion

of the lights.

We consider that the earlier differential response found to be

related to the perception of PLW is evoked by the configuration

of the point lights in the first frame of the stimulus in the previous

studies. This is because the luminance change and velocity profile

of the individual point-lights would be similar for both PLW and

SCB stimuli. It is known that a human body figure evokes a specific

brain response at around 170 ms (Peelen and Downing, 2007; Stekelenburg

and de Gelder, 2004; Thierry et al., 2006). Thus, it would

not be surprising that the human brain responds to a human figure

more than randomly positioned lights. Further study is necessary

Condition Coordinates (mm)

Left hemisphere Right hemisphere

x y z x y z

S1(SCB)

Upright 35.5(3.7) 40.0(4.1) 63.3(5.0) 40.5(5.1) 29.3(6.2) 62.9(4.1)

Inverted 35.6(6.7) 27.4(6.8) 67.5(4.4) 33.7(5.1) 21.2(6.4) 69.0(4.1)

S2 (PLW)

Upright 46.9(2.7) 10.1(10.1) 67.9(4.0) 52.4(7.8) 12.8(7.0) 53.7(4.1)

Inverted 44.9(6.2) 8.4(9.1) 64.9(4.1) 44.5(4.5) 13.5(3.1) 73.8(6.5)

Means (±SE).


to confirm this consideration, but it should be noted that the previous

studies provided an intriguing function of the brain; that is,

our brains may be able to identify human posture from the static

configuration of point lights as well as from the motion of the

lights.

One might argue that the MS2 simply represents a delayed MS1

response related to motion perception of S1. Using a similar experimental

paradigm to that described here, Aspell et al. reported that

the peak latency of the VEF response to the S2 stimuli appeared at

156–265 ms, and the dipole was estimated to lie in the extrastriate

cortex (Aspell et al., 2005). Using an adaptation paradigm, Amano

et al. reported that the VEF evoked by velocity increments peaked

at around 250 ms after stimulus onset (Amano et al., 2005). These

studies suggest that responses related to motion perception would

be observed at up to 300 ms after stimulus onset in the occipitotemporal

region, even when the preceding stimulus was also a visual

motion stimulus. On the other hand, the peak latency of MS2

was delayed by approximately 80–100 ms on average, compared

with these studies, and was also significantly delayed compared

with MS1. Furthermore the estimated location of the MS2 dipole

was more anterior than that of the MS1 dipole (Fig. 5A and B).

It should be noted that we used different patterns of animation

between S1 and S2 in all experimental conditions; each point-light

was exchanged between S1 and S2, even in the SCB condition. One

might think that the weak deflection in the S2 period might simply

reflect the detection of the transition in stimulus from S1 to S2.

However, despite the fact that the exchange of point-lights was

identical in both PLW/iPLW and SCB/iSCB conditions, the amplitude

of the response to the PLW stimulus was significantly larger

than that of the response to the SCB S2 stimulus. Thus, we presume

that the appropriate spatial configuration of point-lights, that is,

the meaningful spatial configuration of point-lights, would enhance

the amplitude of MS2. Moreover, in our preliminary behavioral

experiment, we could not find a statistically significant

difference in detection of the change from S1 to S2, in any condition.

This suggests that all participants were aware of the change

in stimuli between S1 and S2, even in the SCB/iSCB condition; thus,

it is hard to explain the difference in amplitudes between responses

to PLW and SCB stimuli on the basis of a difference in

attentional level.

4.2. The function of the MS1 component

The peak amplitude of the MS1 was prominent in the occipitotemporal

region and found at around 250 ms after the onset of the

S1 stimulus; this amplitude was not affected by S1 orientation.

Previous motion-MEG studies using a similar stimulus presentation

showed that the peak neuromagnetic response to S1 in the

occipitotemporal region occurred at around 265 ms (Lam et al.,

2000) or 220 ms after the onset of S1 (Aspell et al., 2005). Another

study (Nakamura et al., 2003) also revealed that the VEF latency of

responses to random dot kinematograms was around 230–250 ms.

Although the motion trajectories in our study were different from

those in the previous MEG studies, we observed the MS1 component

at around 220–240 ms after the onset of the S1 stimulus,

which seems to be concordant with those MEG studies concerning

latency and regions. Supporting the possibility of the neural response

relating to the motion perception, the dipole for MS1 was

estimated to be located in the vicinity of the middle temporal

region.

4.3. Comparison with other neuroimaging findings

Although there is a limitation of spatial resolution in MEG (Hari

et al., 2000), the locations of the dipoles for MS1 and MS2 components

seem to be concordant with those described in the previous

M. Hirai et al. / Clinical Neurophysiology 119 (2008) 2775–2784 2783

neuroimaging studies. ECD analysis revealed that the dipole for

MS1 (SCB) seems to lie within a small region around the middle

temporal area, whereas the dipole for MS2 (PLW and iPLW) was

estimated to lie in the occipitotemporal region, presumably the

middle temporal area and part of the pSTS. The dipole of MS2

was significantly more anterior than that of MS1 in the left hemisphere,

while a similar shift in the location approached significance

in the right hemisphere. It should be noted here that the selected

sensors were identical across conditions for each participant; thus,

the dipole location would not be biased by the numbers and locations

of sensors.

This finding seems to be consistent with the results of dipole

estimation, as many neuroimaging studies have revealed that the

posterior STS appears to be an important region for PLW perception

(Bonda et al., 1996; Grossman et al., 2000; Grossman and

Blake, 2001; Peuskens et al., 2005; Vaina et al., 2001). The importance

of the pSTS region for PLW perception was also confirmed

by a repetitive transcranial magnetic stimulation study (Grossman

et al., 2005). The present result implies that the spatially distinct

cortical region might be involved in the processing of SCB and

PLW stimuli.

The results of this study showed no significant difference in

MS2 amplitude between upright and inverted PLW stimuli. Consistent

with the present findings, a previous ERP study indicated that

the amplitude of the later component ( 300 ms), that is, the response

to the upright PLW stimulus, was not significantly different

from that of the response to the inverted PLW stimulus (Jokisch

et al., 2005). On the other hand, a recent oscillatory MEG study

(Pavlova et al., 2004) revealed a gamma-band response to an upright

PLW stimulus in the parietal (130 ms) and right temporal cortices

(170 ms); however, the responses to an inverted walker are

limited to the left occipital cortex. This finding suggests that the

early stage of the neural response is modulated by orientation. This

is somewhat inconsistent with the present results. However, we

presume that this relates to the difference between the evoked response

and the oscillatory response; the evoked response contains

a wider range of frequency components compared with the specific

gamma band oscillatory response (25–30 Hz) in their study. Moreover,

the present experimental paradigm was different from that

used in this previous oscillatory MEG study; this might also affect

the VEF responses. For these reasons, we cannot directly compare

our study with the previous oscillatory MEG studies; however, further

studies should address the orientation effect on both evoked

and oscillatory responses.

For laterality, we could not find a significant main effect of the

laterality for the MS2 amplitude (approached significance,

p = 0.05); however, the amplitude in the right hemisphere seems

to be larger than in the left hemisphere (Fig. 3A). The right-lateralized

activities underlying BM perception have also been reported

in several neuroimaging studies (Bonda et al., 1996; Grossman

et al., 2000). For example, Grossman et al. reported that the activities

in the posterior part of the STS region during the perception of

BM were bilateral; however, in the group average, they were greater

in the right hemisphere (Grossman et al., 2000). Also in our previous

ERP studies (e.g. Hirai et al., 2003), right-lateralized activities

were also confirmed. In the present study, we also found a consistent

result in terms of laterality.

The present findings might contribute to the elucidation of the

timing of activation in brain areas involved in PLW perception, as

proposed by Peuskens (Peuskens et al., 2005). According to their

schematic representation of functional interactions, the complex

motion pattern is encoded in the hMT/V5+ region, and the STS plays

an important role in coding visual representations of actions themselves.

Based on the present results, in our experimental paradigm,

we speculate that PLW patterns from point-light motion are processed

at around 300–350 ms after stimulus onset, in the STS region.


2784 M. Hirai et al. / Clinical Neurophysiology 119 (2008) 2775–2784

In conclusion, we extracted a neuromagnetic response component

(MS2) related to a PLW perception from point pattern change

by introducing a ‘double stimulus presentation method’. The response

amplitude was significantly larger in the PLW stimulus condition

than in SCB condition. The response latency of 300–350 ms

was about 100 ms later than that for motion onset. We consider

that the neural process specific for the detection of a PLW stimulus

from the motion of the lights occurs about 100 ms after the neural

process for general motion detection, which occurs within 260 ms

of the visual stimulus onset.

Acknowledgements

We thank Mr. O. Nagata and Mr. Y. Takeshima for their technical

support. M.H. was supported by a Grant-in-Aid for JSPS Fellows

No. 18-11826 by the Ministry of Education, Science, Sports, and

Culture, Japan.

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