Developmental changes in point-light walker processing during childhood and adolescence: An event-related potential study

Neuroscience 161 (2009) 311–325

DEVELOPMENTAL CHANGES IN POINT-LIGHT WALKER PROCESSING DURING CHILDHOOD AND ADOLESCENCE: AN EVENT-RELATED POTENTIAL STUDY M. HIRAI,a,b* S. WATANABE,a Y. HONDAa AND R. KAKIGIa,c

The visual system can extract much information about human actions from very limited cues. Biological motion (BM) is the phenomenon whereby one perceives vivid actions with only a dozen point-lights designated to the joints (Johansson, 1973). Interestingly, much information can be extracted from point-lights motion, such as individual identification (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 performance on a BM detection task in 8 –10-year-old children with autism compared poorly with that in normal developing children; however, performance on the static version of a form-frommotion task was equal in both groups (Blake et al., 2003). Neuroimaging studies by using functional magnetic resonance imaging (fMRI) and positron-emission tomography (PET), have enabled the exploration of neural substrates for the processing of BM (Bonda et al., 1996; Howard et al., 1996; Grossman et al., 2000; Grezes et al., 2001; Grossman and Blake, 2001, 2002; Vaina et al., 2001; Santi et al., 2003; Saygin et al., 2004; Michels et al., 2005; Peuskens et al., 2005). These studies suggest that the posterior superior temporal sulcus (pSTS) plays an important role in the processing of BM (Bonda et al., 1996; Grossman et al., 2000; Grossman and Blake, 2001; Vaina et al., 2001; Peuskens et al., 2005). Further, along with pSTS, regions, such as the human middle temporal complex and satellites (hMT/V5⫹) (Howard et al., 1996; Grezes et al., 2001), fusiform gyrus (FG) (Grossman and Blake, 2002; Grossman et al., 2004), lingual gyrus (Vaina et al., 2001; Servos et al., 2002), kinetic occipital area (Vaina et al., 2001; Santi et al., 2003), amygdala (Bonda et al., 1996), and frontal region (Saygin et al., 2004), are also involved in BM processing. Previous neuroimaging studies have not been able to provide an accurate temporal assessment of the underlying neural changes that support the rapid psychological phenomenon in which the human visual system detects meaningful human behaviors via BM stimuli from only a 200-ms exposure (Johansson, 1976). Recent event-related potential (ERP) or magnetoencephalography (MEG) studies (Pavlova et al., 2004, 2006) have shown the neural dynamics of BM processing. ERP studies (Hirai et al., 2003, 2005; Jokisch et al., 2005; Hirai and Kakigi, 2008) have demonstrated that two negative components are specified around 200 and 240⫺330 ms after stimulus onset in the bilateral occipitotemporal region. These results suggest that the first component might reflect general mo-

a Department of Integrative Physiology, National Institute for Physiological Sciences, 38 Nishigonaka, Myodaiji, Okazaki, 444 – 8585, Japan b

Japan Society for the Promotion of Science, Chiyoda-ku, Tokyo 1028472, Japan

c

Department of Physiological Sciences, The Graduate University for Advanced Studies (Sokendai), Hayama, Kanagawa 240-0193, Japan

Abstract—To investigate developmental changes in the neural responses to a biological motion stimulus, we measured event-related potentials (ERPs) in 50 children aged from 7 to 14 years, and 10 adults. Two kinds of visual stimuli were presented: a point-light walker (PLW) stimulus and a scrambled point-light walker (sPLW) stimulus as a control. The sPLW stimulus had the same number of point-lights and the same velocity vector of point-lights as the PLW stimulus, but the initial starting positions were randomized. Consistent with previous ERP studies, one positive peak (P1) and two negative peaks (N1 and N2) were observed at around 130, 200 and 330 ms, respectively, in bilateral occipitotemporal regions, in all age groups. The latency of the P1 component was significantly shorter for the PLW than sPLW stimulus in all age groups, whereas the amplitude was significantly larger for the PLW than sPLW stimulus only for the 7-year-old group. The P1 amplitude and N1 latency were linearly decreased with age. The negative amplitudes of both N1 and N2 components of the PLW stimulus were significantly larger than those of the sPLW stimulus in all age groups. P1-N1 amplitude was changed by development, but not N2 amplitude. These results suggest that the intensity (P1) and timing (N1) of early visual processing for the PLW stimulus changed linearly throughout childhood and P1-N1 amplitude at occipitotemporal electrodes and N1 latency in 10-year-olds, but not 11-year-olds, was significantly larger than that in adults. For the amplitudes of the N2 component in response to PLW and sPLW stimuli in 7– 8-year-old subjects were not statistically different from those in adults at occipitotemporal electrodes. These results suggest that the neural response to the PLW stimulus has developed by 10 years of age at the occipitotemporal electrode. © 2009 IBRO. Published by Elsevier Ltd. All rights reserved. Key words: biological motion, point-light walker, event related potential, ERP, cross-sectional study, developmental change. *Correspondence to: M. Hirai, Department of Integrative Physiology, National Institute for Physiological Sciences, 38 Nishigonaka, Myodaiji, Okazaki, 444 – 8585, Japan. Tel: ⫹81-564-55-7811; fax: ⫹81-564-52-7913. E-mail address: [email protected] (M. Hirai). Abbreviations: ANOVA, analysis of variance; BM, biological motion; EEG, electroencephalogram; EOG, electro-oculogram; ERP, eventrelated potential; FG, fusiform gyrus; fMRI, functional magnetic resonance imaging; MEG, magnetoencephalography; PLW, point-light walker; pSTS, posterior superior temporal sulcus; SM, scrambled motion; sPLW, scrambled point-light walker; STG, superior temporal gyrus; STS, superior temporal sulcus.

0306-4522/09 $ - see front matter © 2009 IBRO. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.neuroscience.2009.03.026

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tion information processing (local motion processing), or the processing of the human form from the alignment of the point-lights, such as body-sensitive neural responses that are observed at 170 –190 ms (Stekelenburg and de Gelder, 2004; Thierry et al., 2006; Peelen and Downing, 2007). The second component might be related to the specific analysis of motion patterns that provide biologically relevant information or form-from-motion processing. ERP and MEG-based studies have attempted to reveal the temporal aspect of BM processing in human adults. Nevertheless, several questions still remain unanswered: how does the neural system begin to process BM and, furthermore, how do the neural responses to BM change during development? Previous behavioral studies have demonstrated that 3–9-month-old infants can recognize differences between BM and scrambled motion (SM: each point had the same velocity vector as BM, but the initial starting positions were randomized) or other kinds of motion stimuli (Fox and McDaniel, 1982; Bertenthal et al., 1984, 1987) whereas, 2-month-old infants did not show any preference for BM displays (Fox and McDaniel, 1982). However, a recent behavioral study revealed that even 2-day-old infants can differentiate BM from other kinds of motion stimuli (Simion et al., 2008). Therefore, this important problem has not been solved. These behavioral studies in infants indicate that the visual system can detect the BM stimulus in the early stages of development. Moreover, several behavioral studies have shown that the ability to detect BM can change during childhood. According to behavioral studies in children (Pavlova et al., 2001; Jordan et al., 2002; Blake et al., 2003; Freire et al., 2006), children as young as 5 years of age performed as well as adults in detecting BM without masking noise, by contrast, 6-year-olds performed significantly poorer than 9-year-olds and adults with regard to “sensitivity” (detecting BM from the masking noise dots). Among the 9-year-olds, sensitivity was not significantly different from that in adults (Freire et al., 2006). Results from these behavioral studies have revealed that BM-detecting mechanisms emerge during an early stage of development and also change with development; nevertheless, the neural mechanisms involved in these developmental changes remain unclear. At present, there are few ERP, MEG, or fMRI studies on BM processing in infants or children (Hirai and Hiraki, 2005; Carter and Pelphrey, 2006; Pavlova et al., 2006; Reid et al., 2006). In one ERP study, the differential neural response to upright BM and SM stimulus in 8-month old infants (Hirai and Hiraki, 2005) suggested that the averaged BM amplitude between 200 and 300 ms was significantly larger than the SM in the 8-month old infants and adults. In 8-month old infants, Reid et al. (2006) demonstrated a differential neural response to upright BM and inverted BM stimulus. In addition, a recent fMRI study in 7–10-year-old children revealed increasing activity in the superior temporal sulcus (STS) region with BM processing (no point-light walker [PLW] animation, but rather computer-generated human, robot, and grandfather clock animation) (Carter and Pelphrey, 2006).

The results of these studies imply that the visual processing of BM stimuli changes during development in school-aged children, however, electrophysiological studies to clarify the temporal profile of neural responses are lacking. As mentioned above, at least two negative components were observed during perception of the BM stimulus within 500 ms (Hirai et al., 2003; Jokisch et al., 2005), thus it is necessary to elucidate the developmental changes of the neural dynamics for the perception of BM stimuli by measuring ERP with high temporal resolution. We focused on this age period (7–14 years) for two reasons. First, as mentioned above, a recent behavioral study reported that performance of a BM detection task was significantly impaired among children with autism (average age of 8.4 years) compared to typically developed children (average age of 7.9 years) (Blake et al., 2003). Thus, in addition to the behavioral measures, it is necessary to establish an electrophysiological index that relates to the visual processing of the PLW stimulus at this age. Second, from the viewpoint of the neural basis of social perception (Allison et al., 2000), in addition to electrophysiological evidence of face perception in children (Taylor et al., 1999, 2001, 2004; Itier and Taylor, 2004), it would be interesting to clarify the developmental changes of the neural response to the BM stimulus in children. To address this issue, ERPs were measured in children aged 7–14 years, and the developmental changes in neural responses to BM stimuli were compared. In the present experiment, we focused on not only the two negative components (N1 and N2) which may be related to the visual processing of BM stimuli as previously reported in ERP studies (Hirai et al., 2003; Jokisch et al., 2005), but also the P1 component. We did this because, in a previous ERP-based study on body perception, the early positive component (P1) was modulated by stimulus category, that is, the P1 elicited by objects was significantly delayed relative to that elicited by faces and bodies (Thierry et al., 2006). Thus it is possible that the P1 component can also be modulated by the alignment of the point-lights whether they represents the human body or not. Thus, in the present experiment, to investigate the possibility of the early modulation of the ERP responses to the PLW stimulus, we focused on the P1 component in addition to the N1 and N2 components which have been investigated in previous ERP studies. Prior to the experiment, we hypothesized that the modulation of each component occurs as follows. For P1, if it is sensitive to the form of a human figure from the alignment of the point-lights, the latency of the P1 component induced by the PLW stimulus can be shortened compared with the scrambled point-light walker (sPLW) stimulus, which would be similar to the results of studies on body perception (Thierry et al., 2006). For the N1 and N2 components, if the neural response to the PLW stimulus in children is similar to that in the adults, an enhanced amplitude in the response to PLW stimulus compared with the sPLW stimulus can be observed as in previous studies (Hirai et al., 2003; Jokisch et al., 2005). For the developmental changes of each component, P1 amplitude and N1

M. Hirai et al. / Neuroscience 161 (2009) 311–325 Table 1. Study participants

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Eighty-nine children and 10 adults participated in this study. Children were recruited from elementary school and junior high school at Okazaki City. Adult participants were recruited from our institute. No subject had a neurological disorder. All children and their parents, and all adults, provided informed consent for the experimental protocol, which was approved by the Ethics Committee of the National Institute for Physiological Sciences. In the EEG analysis, 39 children did not reach the criterion for averaging (see data analysis section) and thus, were excluded from further analysis. We divided the 50 remaining children into five age groups, as shown in Table 1.

tion). Each point of the sPLW had the same velocity vector (that is, the same speed and direction for each point) as the PLW and there was the same number of point-lights, but the initial spatial position was randomized. Thus, the only difference between PLW and sPLW stimuli was the spatial configuration of point-lights. In each stimulus, we created 10 different patterns (created by shifting the starting frame from the original stimulus) of stimulus. The two kinds of walker (namely left- and right-facing) were presented randomly. In this experiment, the speed of gait was 2.0 steps per second and the frame duration was 33 ms producing a smooth animation. Each stimulus was presented for 500 ms and the inter-stimulus interval was varied randomly between 960 and 1440 ms. Animations were displayed subtending a visual angle of 3⫻2° (height⫻width) on the 21-in. CRT monitor at a viewing distance of 150 cm. All points were white (1.6 cd/m2) against a black background (0.4 cd/m2). A red fixation point was presented at the center of the screen throughout both the stimulus presentation and the interstimulus interval, and participants were required to fixate on this point. The fixation point was placed in the center of both PLW and sPLW stimuli. The experiment consisted of seven blocks. In one block, each experimental stimulus (PLW and sPLW stimuli) was presented 12 times randomly. Two kinds of tasks were required during and after the experiment. During the experiment, to keep participants’ attention on the center of the screen, participants were instructed to press the button with their right thumb when a target (static point-lights) was presented instead of the animation. The target was created by extracting one frame from a PLW or sPLW animation. After the experiment, children were presented with each visual stimulus and were then required to answer verbally what the presented stimuli (both PLW and sPLW) looked like. In the verbal task, children were allowed to describe freely whatever came to mind. Within a block, a static point-light stimulus was presented twice randomly.

Experimental stimuli and task

Electroencephalogram (EEG) recording

We used two kinds of visual stimuli (PLW and sPLW; Fig. 1) as in previous studies (for example; Hirai and Hiraki, 2005). The PLW (basic stimulus) was generated from computer algorithms developed by Cutting (1978). The animation consisted of 11 moving point-lights attached to the head and main joints, and the animation looked as if a person were walking on a treadmill. We created two kinds of walker (one facing to the left and one facing to the right). As a control, a sPLW stimulus was used (we manipulated only spatial relations, not temporal synchrony or phase informa-

EEGs were recorded using Ag/AgCl disk electrodes placed on the scalp at 21 locations: Nose, A1, A2, O1, O2, P3, P4, Pz, T3, T4, C3, C4, Cz, F3, F4, Fz, FCz, T5, T6, T5=, and T6=, According to the International 10 –20 System. T5= and T6= were located 2 cm below T5 and T6, as in our previous studies (Watanabe et al., 2003; Hirai and Kakigi, 2008). Two electrodes, HEOG (right temple) and VEOG (above the right eye), were used to record electro-oculograms (EOGs) for identification of horizontal and vertical eye movements. Impedance was maintained at less than 5 k⍀. All

Group

No.

Mean age (SD)

Female

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7Y 9Y 10Y 11Y 13Y A

10 10 10 10 10 10

7 y 7 mo (⫾4.9 mo) 9 y 3 mo (⫾5.2 mo) 10 y 4 mo (⫾4.7 mo) 11 y 11 mo (⫾7.1 mo) 13 y 11 mo (⫾3.9 mo) 28 y 5 mo (⫾3 y 6.2 mo)

5 4 6 3 2 5

5 6 4 7 8 5

7Y: 7-year-olds, 9Y: 9-year-olds, 10Y: 10-year-olds, 11Y: 11-yearolds, 13Y: 13-year-olds, A: adults.

latency would be decreased with development as in previous ERP-based studies in children (Itier and Taylor, 2004).

EXPERIMENTAL PROCEDURES Participants

Fig. 1. An example of the experimental stimuli. (A) PLW stimulus and (B) sPLW stimulus.

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EEG signals were collected on a signal processor (EEG-1100, Nihon-Kohden, Tokyo, Japan). The bandpass filter was set at 0.1–100 Hz. All recordings were initially referenced to C3 and C4 (based on system settings), but later to the tip of the nose as in a previous ERP study (Jokisch et al., 2005; Hirai and Kakigi, 2008). Electrical potential was digitized at a 1000-Hz sampling rate, and data were stored on a computer disk for off-line analysis.

and sPLW) at O1/O2 and T5=/T6= electrodes. In the analysis, if the sphericity assumption was violated in Mauchly’s sphericity test, the Greenhouse-Geisser correction coefficient epsilon was used to correct the degrees of freedom; then, F and P-values were recalculated. We considered statistical significance to be P⬍0.05.

Data analysis

Behavioral performance

In the off-line analysis of EEG recordings, a 0.1–30 Hz bandpass filter (24 dB/octave) was applied to the data. Trials in which the EEG or EOG signal variation exceeded an absolute value of ⫾75 ␮V were discarded. The analysis window was extended for 500 ms following the onset of each stimulus. This duration corresponded to the duration of the stimulus. The mean amplitude during the 100 ms before stimulus presentation was used as the baseline and applied to individual data. We analyzed ERP data only from participants in which over 30 trials showed a signal variation of less than ⫾75 ␮V for each stimulus, and calculated a grand-averaged waveform for each group. For all participants, the minimum number of acceptable trials was 30; thus, we analyzed data from 50 children and 10 adults. The average number of accepted trials for each group was as follows: 7-year-olds (PLW: 53⫾6.7, sPLW: 53.1⫾7.4 trials; mean⫾SD), 9-year-olds (PLW: 53.4⫾18.1, sPLW: 54.6⫾15.5 trials), 10-year-olds (PLW: 59.0⫾8.3, sPLW: 60.2⫾7.4 trials), 11-year-olds (PLW: 64.3⫾14.5, sPLW: 63⫾16.3 trials), 13-year-olds (PLW: 56.3⫾17.1, sPLW: 55.7⫾17.2 trials), and adults (PLW: 70.3⫾10.7, sPLW: 70.6⫾9.8 trials).

The percentages of correct performances on a targetdetection task (detecting the static version of the stimulus) are shown in Table 2. We performed a one-way ANOVA with correct performance on target detection as the dependent measure and group as a between-subjects factor. As a result, no significant effect was observed for Group [F(5,54)⫽1.2, P⫽0.3], suggesting that all participants kept their attention on the screen. Regardless of age group, all participants perceived the PLW stimulus as “a walking human.” On the other hand, it was hard for participants to perceive the sPLW stimulus as a human figure. No participant described the sPLW stimulus as “a walking person.” Thus, the impression of the sPLW stimulus was quite different from that of the PLW stimulus.

ERP waveform analysis

Fig. 2 shows the grand averaged ERPs across age groups, for each PLW and sPLW stimulus. From these figures, we observed two prominent components (P1 and N1) at O1/O2 and three components (P1, N1 and N2) at T5=/T6= electrodes, in response to both PLW and sPLW stimuli, as found in previous studies (Hirai et al., 2003, 2005; Jokisch et al., 2005; Hirai and Kakigi, 2008). We carried out a statistical analysis of the latency and amplitude of each component.

Each peak component was determined from the following time window: P1 component (80 –160 ms), N1 component (100 –280 ms) and N2 component (220 –500 ms). As in a previous study, we observed one positive component (P1) and two negative components (N1 and N2) at the T5=/T6= electrodes (Hirai and Kakigi, 2008), and the P1 and N1 components were also observed at the O1/O2 electrodes. Thus, we carried out statistical analysis of the amplitude and latency of P1, N1 and N2 components at the T5=/T6= electrodes, and of the P1 and N1 components at the O1/O2 electrodes. The window of analysis overlapped because the latency of each component varied across age groups. In the analysis, the same peak was not identified as N1 and N2. In addition to the analysis of each component, we analyzed the peak-to-peak (P1-N1) amplitude, because the differences in P1 amplitude were so large across age groups. For statistical analysis, behavioral data were analyzed using a one-way analysis of variance (ANOVA), with group as a factor. Both the P1 and N1 components and peak-to-peak (P1-N1) amplitude were analyzed using mixed-design repeated measures ANOVAs, with the Greenhouse-Geisser epsilon correction for nonsphericity, and Tukey’s HSD was applied for multiple comparisons. A four-way ANOVA was applied to the amplitude and latency of each component (P1 and N1) and P1-N1 amplitude. Group (7-year-olds, 9-year-olds, 10-year-olds, 11-year-olds, 13-year-olds and Adults) was used as an intersubject factor and Hemisphere (Left hemisphere and Right hemisphere), Stimulus (PLW and sPLW) and Electrode (Occipital and Occipitotemporal) were used as intrasubject factors. For the N2 component, a three-way ANOVA was applied to the amplitude and latency of N2. Group (7-year-olds, 9-year-olds, 10-year-olds, 11-year-olds, 13-year-olds and Adults) was used as an intersubject factor and Hemisphere (Left hemisphere and Right hemisphere) and Stimulus (PLW and sPLW) was used as an intrasubject factor. To verify the age-related changes, regression analysis was also applied to the latency and amplitude of the three ERP components (P1, N1, and N2) for the two stimulus conditions (PLW

RESULTS

ERP data

P1 component For P1 amplitude, the analyzed data are shown in Fig. 3 (left side). The analysis revealed a main effect of Hemisphere [F(1,54)⫽12.0, P⬍0.01], suggesting that the amplitude was significantly larger in the right hemisphere than left. In addition to the main effect, we observed a significant threeway interaction (Electrode⫻Group⫻Stimulus) [F(5,54)⫽3.6, P⬍0.01]. A follow-up analysis revealed a significant two-way interaction (Electrode⫻Group) for the PLW [F(5,54)⫽10.0, P⬍0.01] and sPLW [F(5,54)⫽6.1, P⬍0.01] stimuli, and anTable 2. Behavioral performance Group

Performance (%)

7Y 9Y 10Y 11Y 13Y A

97.5⫾0.1 92.7⫾0.2 94.0⫾0.1 96.0⫾0.1 100.0⫾0 100.0⫾0

Means⫾SD. 7Y: 7-year-olds, 9Y: 9-year-olds, 10Y: 10-year-olds, 11Y: 11-year-olds, 13Y: 13-year-olds, A: adults.

M. Hirai et al. / Neuroscience 161 (2009) 311–325

315 P1

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+5.0ǴV

7 Years 9 Years 10 Years 11 Years

-5.0ǴV

13 Years Adults

Fig. 2. Grand-averaged ERPs at four electrodes (O1, O2, T5=, T6=) in response to (A) PLW and (B) sPLW stimuli displayed to subjects in six age groups. (A, B) Each color indicates a group (the blue line indicates 7-year-olds, the aqua line is 9-year-olds, the green line is 10-year-olds, the orange line is 11-year-olds, the pink line is 13-year-olds and the red line is adults). Three prominent components, P1, N1 and N2, were observed at around 130, 200 and 300⫺400 ms after the stimulus onset, respectively. The P1 component was observed at the O1/O2 electrodes, and its amplitude decreased significantly with development. The latency of the P1 component at the O1/O2 electrodes was not modulated by development. The N1 and N2 components were mainly observed at the T5=/T6= electrodes. Both negative amplitudes induced by the PLW stimulus were significantly larger than those induced by the sPLW stimulus. The N1 latency decreased significantly with development, but the N2 latency did not.

other significant two-way interaction (Group⫻Stimulus) at the occipital electrode [F(5,54)⫽3.1, P⬍0.05]. For the interaction of Electrode⫻Group, a subsequent post hoc Tukey’s HSD analysis revealed that P1 amplitude was significantly larger at the occipital electrode than occipitotemporal electrode in the 7-, 9-, 10- and 11- and 13-year-olds. Regarding group differences, at the occipital electrode, P1 amplitude was significantly larger in the 7-, 9-, 10- and 11-year-olds than in the 13-year-olds and adults for the PLW stimulus. For the sPLW stimulus, the amplitude was significantly larger in the 7-, 9-, 10- and

11-year-olds than in the 13-year-olds. Moreover, it was significantly larger in the 13-year-olds than that in the adults. At the occipitotemporal electrode, group differences were also significant: P1 amplitude was significantly larger in the 7- and 9-year-olds than in the adults when the visual stimulus was sPLW. For significant interaction (Group⫻Stimulus) at the occipital electrode, a significant effect of Stimulus was observed in 7-yearolds: the P1 amplitude induced by the PLW stimulus was significantly larger than that induced by the sPLW stimulus.

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Fig. 3. The averaged amplitude and latency of the P1 component. (A) O1/O2 electrodes and (B) T5=/T6= electrodes. The error bars indicate the standard errors (SE) of the mean.

For P1 latency, the analyzed data are shown in Fig. 3 (right side). The statistical analysis revealed a significant two-way interaction (Electrode⫻Stimulus) [F(1,54)⫽6.6, P⬍0.05]. Subsequent analysis revealed that the P1 induced by the PLW stimulus was significantly shorter in latency than that induced by the sPLW stimulus at the occipital electrode [F(1,18)⫽5.5, P⬍0.05]. N1 component The analyzed data for N1 amplitudes are shown in Fig. 4 (left side). The statistical analysis revealed a significant four-way interaction (Group⫻Hemisphere⫻Electrode⫻ Stimulus) [F(1,54)⫽2.9, P⬍0.05]. A follow-up analysis revealed a significant two-way interaction (Electrode⫻Group) in the left hemisphere for both stimuli [PLW stimulus: F(5,54)⫽6.9, P⬍0.01; sPLW stimulus: F(5,54)⫽5.2, P⬍0.01] and the right hemisphere for both stimuli [PLW stimulus: F(5,54)⫽2.9, P⬍0.05; sPLW stimulus: F(5,54)⫽3.1, P⬍0.05]. For the interaction between Electrode and Group, significant effect on a group was found at the occipital electrode. Post hoc Tukey’s HSD analysis revealed that N1 amplitude was significantly larger in the

7-year-olds and adults than in the 9-, 10- and 11-year-olds for both visual stimuli (i.e. PLW and sPLW stimuli) and in the left hemisphere (i.e. the O1 electrode). Moreover, at the O1 electrode, N1 amplitude was significantly larger in the 13-year-olds than in the 10-year-olds. In the right hemisphere (i.e. O2 electrode), N1 amplitude was significantly larger in the 7-year-olds and adults than in the 11-year-olds. Furthermore, the amplitude was significantly larger in the adults than in the 9-year-olds. In addition to the significant interaction, a main effect of Stimulus was significant at the occipitotemporal electrode [left hemisphere: F(1,54)⫽14.8, P⬍0.01, right hemisphere: F(1,54)⫽11.9, P⬍0.01]. This suggests that the N1 induced by the PLW stimulus was significantly larger in amplitude than that induced by the sPLW stimulus at the occipitotemporal electrode. For N1 latency, the analyzed data are shown in Fig. 4 (right side). The statistical analysis revealed a significant main effect of Electrode [F(1,54)⫽16.5, P⬍0.01], Stimulus [F(1,54)⫽11.6, P⬍0.01] and Group [F(1,54)⫽4.6, P⬍0.01]. The results suggest that the N1 latency at the occipital electrode was shorter than that at the occipitotemporal electrode

M. Hirai et al. / Neuroscience 161 (2009) 311–325

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Fig. 4. The averaged amplitude and latency of the N1 component. (A) O1/O2 electrodes and (B) T5=/T6= electrodes. The error bars indicate the standard errors (SE) of the mean.

and the N1 latency induced by the PLW stimulus was significantly longer than that by the sPLW stimulus. Moreover, post hoc Tukey’s HSD analysis revealed that the N1 latency was significantly shorter in the adult group than in the 7-, 9-, and 10-year-olds. P1-N1 amplitude Because the inter-individual difference in P1 amplitudes was very large across age groups, we analyzed peak-topeak (P1-N1) amplitudes. The analyzed data for P1-N1 amplitudes are shown in Fig. 5. The statistical analysis revealed a significant four-way interaction [F(5,54)⫽3.1, P⬍0.05]. A follow-up analysis revealed a significant twoway interaction (Electrode⫻Group) in the left hemisphere for both stimuli [PLW stimulus: F(5,54)⫽6.3, P⬍0.01; sPLW stimulus: F(5,54)⫽4.8, P⬍0.01] and the right hemisphere for both stimuli [PLW stimulus: F(5,54)⫽3.0, P⬍0.05; sPLW stimulus: F(5,54)⫽4.5, P⬍0.01]. Moreover, another interaction (Hemisphere⫻Group) was significant for the PLW stimulus at the occipitotemporal electrode [F(5,54)⫽2.5, P⬍0.05]. In addition, a main effect of stimulus was significant at the occipitotemporal electrode in

each hemisphere [left hemisphere: F(1,54)⫽23.5, P⬍0.01; right hemisphere: F(1,54)⫽16.8, P⬍0.01]. The results suggest that the P1-N1 amplitude induced by the PLW stimulus was significantly larger than that induced by the sPLW stimulus at the T5=/T6= electrodes. For the interaction between Electrode and Group, a post hoc Tukey’s HSD analysis revealed that the amplitude was significantly larger at the occipital electrode than occipitotemporal electrode in the 7-, 9-, 10-, 11- and 13-yearolds. Group differences were also observed at each electrode. At the occipital electrode, the amplitude was significantly larger in the 7-year-olds than in the 9-, 10-, 11-, and 13-year-olds and adults for both stimuli in the left hemisphere and for the sPLW stimulus in the right hemisphere. The amplitude was significantly larger in the 7-year-olds than in the 9-, 11-, and 13-year-olds and adults for the PLW stimulus in the right hemisphere. Moreover, it was significantly smaller in the adults than in the 9-, 10- and 11-year-olds for both stimuli in the right hemisphere and for the sPLW stimulus in the left hemisphere. For the PLW stimulus in the left hemisphere, the amplitude was significantly smaller in the adults than in the 9- and 10-year-olds.

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Fig. 5. The averaged P1-N1 amplitude. (A) O1/O2 electrodes and (B) T5=/T6= electrodes. The error bars indicate the standard error (SE) of the mean.

Additionally, the amplitude was significantly larger in the 9-year-olds than 13-year-olds for both stimuli in the left hemisphere and for the sPLW stimulus in the right hemisphere. Finally, the amplitude was significantly larger in the 10-year-olds than 13-year-olds for both stimuli in the right hemisphere. At the occipitotemporal electrode, the amplitude was significantly larger in the 7- and 9-year-olds than in the 13-year-olds and adults. Moreover, it was significantly larger in the 10-year-olds than in the adults. Additionally, the amplitude was significantly larger in the 7-year-olds than 11-year-olds for the PLW stimulus in the right hemisphere. For the interaction between Hemisphere and Group, a post hoc Tukey’s HSD analysis revealed that the amplitude was significantly larger in the right than left hemisphere among the 7-, 9- and 10-year-olds. Moreover, group differences were also significant. That is, the amplitude was significantly larger in the 7- and 9-year-olds than in the adults, and significantly larger in the 7-year-olds than 13year-olds in the left hemisphere. In the right hemisphere, it

was significantly larger in the 7- and 9-year-olds than in the 13-year-olds and adults. Moreover, it was significantly larger in the 7-year-olds than in the 11-year-olds. N2 component The analyzed data for the N2 amplitudes are shown in Fig. 6 (left side). At the T5=/T6= electrodes (Fig. 6), the interaction of Hemisphere and Stimulus was significant [F(1,54)⫽8.2, P⬍0.01]. Subsequent analysis revealed that the negative amplitudes of the N2 component induced by the PLW stimulus were significantly larger than those induced by the sPLW stimulus in the left hemisphere [F(1,18)⫽7.9, P⬍0.05] and right hemisphere [F(1,18)⫽36.4, P⬍0.01]. Moreover, the negative amplitude of the N2 component in the left hemisphere was significantly larger than that in the right hemisphere when the stimulus was a sPLW [F(1,18)⫽5.5, P⬍0.05]. The analyzed data for the N2 latencies are shown in Fig. 6 (right side). There were no significant differences in

Fig. 6. The averaged amplitude and latency of the N2 component at the T5=/T6= electrodes. The error bars indicate the standard errors (SE) of the mean.

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the N2 components at the T5=/T6= electrodes [Fs⬍1.3, Ps⬎0.26]. Regression analysis Regression analysis demonstrated significant linear age trends for P1 amplitude (Fig. 7, Table 3) and N1 latency, with the exception of that induced by the PLW stimulus at the T5= electrode (P⬍0.05, see Table 3). However, significant linear trends were not observed for P1 latency, N1 and N2 amplitudes and N2 latency (Table 4).

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DISCUSSION The present study aimed to systematically clarify the developmental changes in the temporal profile of the neural response to BM stimuli. To achieve this purpose, we measured both verbal and ERP responses to PLW and sPLW stimuli in 50 children aged from 7 to 14 years, and 10 adults. We obtained three main results: first, the amplitude, but not the latency of the early P1 component was linearly decreased during development. Moreover, P1 amplitude in 7-year-olds and P1 latency in all age groups were signifi-

Fig. 7. Regression analysis of the P1 amplitude (left panel) and N1 latency (right panel) at the (A) O1/O2 and (B) T5=/T6= electrodes. We found a significant negative correlation except for the N1 latency of the sPLW stimulus at T5= electrode (see Table 3).

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Table 3. The results of the regression analysis of P1 amplitude and N1 latency at O1/O2 and T5=/T6= electrodes

P1 amplitude PLW sPLW N1 latency PLW sPLW

P1 amplitude PLW sPLW N1 latency PLW sPLW

O1

O2

y⫽⫺0.18x⫹42.5, R2⫽0.24** y⫽⫺0.13x⫹36.2, R2⫽0.18**

y⫽⫺0.19x⫹43.8, R2⫽0.25** y⫽⫺0.16x⫹40.0, R2⫽0.22**

y⫽⫺0.37x⫹242.2, R2⫽0.10* y⫽⫺0.33x⫹233.8, R2⫽0.11*

y⫽⫺0.38x⫹244.3, R2⫽0.15** y⫽⫺0.39x⫹243.4, R2⫽0.13*

T5=

T6=

y⫽⫺0.05x⫹12.7, R2⫽0.16** y⫽⫺0.05x⫹12.4, R2⫽0.19**

y⫽⫺0.09x⫹19.8, R2⫽0.26** y⫽⫺0.08x⫹18.5, R2⫽0.25**

y⫽⫺0.29x⫹241.5, R2⫽0.06 y⫽⫺0.39x⫹248.8, R2⫽0.08*

y⫽⫺0.42x⫹264.0, R2⫽0.14** y⫽⫺0.49x⫹267.6, R2⫽0.17**

** P⬍0.01, * P⬍0.05.

cantly modulated by stimulus category. Second, both N1 (P1-N1) amplitude and N2 amplitude were significantly larger for the PLW stimulus than sPLW stimulus. Finally, the latency, but not amplitude, of the N1 component decreased linearly during development. P1-N1 amplitude at the T5=/T6= electrodes had changed by the age of 10, but N2 amplitude did not changed with development. These results imply that there are differences in the development of early and later visual processing: the P1 amplitude changed linearly throughout childhood, but the differential neural response (P1-N1) at occipitotemporal electrodes between PLW and sPLW stimuli in 11-year-old subjects was not significantly different from that in adults.

Behavioral data As expected, all participants reported that the PLW stimulus appeared to be a “walking human figure.” In verbal reports, regardless of age group, all participants perceived the PLW stimulus as a “walking figure.” On the other hand, it is hard for participants to perceive a human figure from the sPLW stimulus. The present result is highly concordant with previous behavioral studies in children (Pavlova et al., 2001; Blake et al., 2003; Freire et al., 2006). These studies suggested that children as young as 5 years of age performed as well as adults and at ceiling level for detecting BM without masking noise. In fact, all children in 7-year-old group (mean age: 7 years and 7 months) reported that a

Table 4. The results of the regression analysis at O1/O2 (P1 latency and N1 amplitude) and T5=/T6= electrodes (P1 latency, N1 and N2 amplitudes, and N2 latency)

P1 latency PLW sPLW N1 amplitude PLW sPLW

P1 latency PLW sPLW N1 amplitude PLW sPLW N2 amplitude PLW sPLW N2 latency PLW sPLW NS.

O1

O2

y⫽⫺0.07x⫹136.5, R2⫽0.01 y⫽0.11x⫹118.7, R2⫽0.03

y⫽0.03x⫹126.4, R2⫽0.00 y⫽0.18x⫹110.3, R2⫽0.05

y⫽0.03x⫺2.09, R2⫽0.01 y⫽0.05x⫺4.65, R2⫽0.03

y⫽0.00x⫹1.62, R2⫽0.00 y⫽0.04x⫺3.68, R2⫽0.02

T5=

T6=

y⫽⫺0.09x⫹143.8, R2⫽0.02 y⫽⫺0.02x⫹132.1, R2⫽0.00

y⫽⫺0.18x⫹157.3, R2⫽0.07 y⫽⫺0.11x⫹146.3, R2⫽0.03

y⫽0.03x⫺7.47, R2⫽0.03 y⫽0.02x⫺4.93, R2⫽0.02

y⫽0.03x⫺7.74, R2⫽0.03 y⫽0.02x⫺4.77, R2⫽0.02

y⫽0.00x⫺3.58, R2⫽0.00 y⫽0.01x⫺3.32, R2⫽0.01

y⫽0.01x⫺4.61, R2⫽0.00 y⫽0.00x⫺0.20, R2⫽0.00

y⫽⫺0.22x⫹336.6, R2⫽0.01 y⫽⫺0.18x⫹329.9, R2⫽0.01

y⫽⫺0.25x⫹333.7, R2⫽0.02 y⫽0.10 x⫹288.9, R2⫽0.00

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PLW stimulus looked like a “walking human.” Contrary to the PLW stimulus, no one reported that the sPLW stimulus looked like a “walking person.” Thus, we considered that the sPLW was an effective control stimulus and that the experimental stimulus would be valid to investigate developmental changes in the neural responses to a PLW stimulus. P1 component In the present study, age had an influence on P1 amplitude in the group analysis. This result was also obtained by regression analysis: the P1 amplitudes in the occipital and occipitotemporal regions decreased linearly during development. Moreover, we also found a significant effect of stimulus on P1 amplitude at the O1/O2 electrodes in the 7-year-old group and on the P1 latency in all age groups. Consistent with the present results for P1 amplitude, several visual-evoked potential studies have shown that P1 amplitude during development decreases according to visual stimulus, such as color, motion, and face (Taylor et al., 2001, 2004; Itier and Taylor, 2004; Mitchell and Neville, 2004; Coch et al., 2005). To date, several interpretations for the decreased P1 component have been proposed. One plausible explanation is the developmental change of the occipital cortex. The P1 component is known to be an early component that reflects encoding of low-level visual properties (Allison et al., 1999) and is generated from occipital cortex (Arroyo et al., 1997). It seems to be appropriate to suggest that the P1 component could be modulated by states of neural circuitry in the occipital cortex. Supporting the abovementioned findings and speculations, several studies have reported that the structures of the neural circuits in the occipital region are altered during childhood. Specifically, decreased synaptic density in the human visual cortex has been shown to take place during development (Courchesne, 1990; Huttenlocher, 1990). Additionally, recent neuroimaging techniques (such as MRI) demonstrated that the occipital poles lose gray matter during early childhood (Gogtay et al., 2004). These developmental changes in the occipital cortex could contribute to developmental changes in the P1 component. In addition to the developmental change in P1 amplitude, we also observed a stimulus effect in the 7-year-old group. This suggests that, even in the early stages of processing, the human figure implicit in point-lights motion can modulate neural activities at an early stage of childhood. In previous ERP studies of body perception, the P1 amplitude was significantly different in responses to stick figures, objects and faces (Thierry et al., 2006). In face processing, the P1 amplitude was larger for inverted and upright faces than for negative faces (Itier and Taylor, 2004). Based on these ERP studies, the P1 component might be thought to reflect the processing of a visual stimulus category. However, in the present study, a significant difference was observed in the 7-year-olds group; thus, this processing might also be changed by development. The finding is in contrast to the results of a previous ERP-based study of body perception (Gliga and DehaeneLambertz, 2005), and difficult to interpret without further study. The larger P1 responses obtained for the PLW

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stimulus in 7-year-olds might imply that the P1 component is sensitive to the implicit form of the human figure from the initial alignment of point-lights specifically of this age. It has also been reported that the component can be modulated by the demands of tasks (Taylor, 2002), thus our task might selectively affect P1 amplitude at this age in children. However, such interpretations are only speculative and further study of how the P1 component is developmentally modulated by stimulus category is needed. With regard to latency, although previous BM studies have not focused on the P1 latency, the present study showed that the P1 latency was modulated by the stimulus category; the P1 latency of the response to the sPLW stimulus was significantly longer than that of the response to the PLW stimulus at O1/O2. In previous ERP studies of face (Itier and Taylor, 2004; Taylor et al., 2004) and body (Thierry et al., 2006) perception, the P1 latency was modulated by the stimulus category: inverted faces elicited longer P1 latencies than upright faces (Itier and Taylor, 2004) and the P1 elicited by objects was significantly delayed relative to faces and bodies (Thierry et al., 2006). In the present study, subjects could perceive a human figure from the alignment of point-lights at the initial frame of the PLW stimulus, but not from the alignment of point-lights at the initial frame of the control scrambled version of a PLW. Such a differential initial alignment might affect the P1 latency. The shortened latency in the P1 component may reflect that the neural system is specialized for the detection of the implicit human form. As a result, the system might respond more rapidly to the PLW stimulus than to the sPLW stimulus. The regression analysis did not reveal a significant effect of age on the P1 latency. Consistent with results from the present group analysis, an ERP study reported that latency of responses to facial stimuli was not altered by development (Itier and Taylor, 2004). In sum, although the P1 amplitude changed linearly during development, the latency was not significantly changed. This implies that the intensity of populational neural activities (the P1 component) in the early visual processing of PLW stimuli is linearly modulated by development, but that the timing of populational neural activities is not modulated by development at the occipital electrodes. With regard to the developmental changes in the conditional difference, the P1 amplitude was modulated only in 7-year-olds, but the P1 latency was modulated by stimulus condition in all age groups. The shortened latency of the P1 component might reflect the expertise for the visual processing of the PLW stimulus. N1 component For the N1 component, the latency was decreased linearly with development; however, the amplitude was not changed monotonically. Moreover, the differential neural response to the PLW and sPLW stimuli depended on the electrode; N1 amplitude was modulated by the category of stimulus at the occipitotemporal electrodes (T5=/T6=) and N1 latency was modulated by stimulus at both the occipital (O1/O2) and occipitotemporal (T5=/T6=) electrodes. Consistent with previous ERP studies (Hirai et al., 2003;

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Jokisch et al., 2005), the N1 amplitude induced by PLW stimulus was significantly larger in all age groups than that induced by the sPLW stimulus. However, contrary to the previous findings, the N1 latency in response to the PLW stimulus was significantly longer than that in response to the sPLW stimulus at the O1/O2 and T5=/T6= electrodes. This would be because the N1 amplitude was larger for the PLW stimulus than sPLW stimulus, thus the latency to reach the peak of the component would be prolonged. In the present study, the amplitudes of both N1 and N2 components were still positive (Figs. 5 and 6) in some groups; however, this could be due to the effect of the deflection of the P1 component, or positive trends that were superimposed on the ERP waveforms as mentioned before. Consistent with the results for the N1 component, the peak-to-peak (P1-N1) amplitude induced by the PLW stimulus was significantly larger than that induced by the sPLW stimulus. However, age-related differences were found not only at the occipital electrodes, but also at the occipitotemporal electrodes (T5=/T6=). This suggests that the developmental effect also manifested in the occipitotemporal region. Although interpretation of the N1 component is still controversial, the present study suggests that N1 reflects the motion onset response (local motion processing), or the processing of the familiar human form from the alignment of point-lights (i.e. visual processing of the human figure from the alignment of point-lights). This interpretation is based on previous ERP studies of PLW perception (Hirai et al., 2003; Jokisch et al., 2005; Hirai and Kakigi, 2008), motion perception (Probst et al., 1993; Bach and Ullrich, 1994; Kubova et al., 1995; Hoffmann et al., 1999; Heinrich et al., 2004) and body perception (Stekelenburg and de Gelder, 2004; Thierry et al., 2006). That is, it has been demonstrated that a negative deflection with a latency of around 150 –200 ms at the occipitotemporal electrodes reflects cortical motion processing in humans. Moreover, a recent study demonstrated the N1 component to be sensitive to local motion information at the T5=/T6= electrodes by using an adaptation paradigm (Hirai and Kakigi, 2008). Among studies of PLW perception, Jokisch et al. (2005) reported that the N1 component was observed at around 200 ms, and that the amplitude was more pronounced in the upright PLW condition than in the invertedor scrambled-PLW stimulus condition. This pronounced effect of the upright PLW stimulus probably reflects the processing by the PLW of the human figure in a familiar orientation. Related to this view, in a study on body perception, the N1 component was observed at around 194 ms at the occipitotemporal electrode when the visual stimulus of a human body was presented (Thierry et al., 2006). According to these findings, N1 may reflect the motion onset response or the processing of the human form from the alignment of the point-lights. Several cross-sectional ERP studies have investigated developmental changes of the N1 component that are related to the processing of motion, color (Mitchell and Neville, 2004; Coch et al., 2005), face (Taylor et al., 2001, 2004), or body (Gliga and Dehaene-Lambertz, 2005) stim-

uli. In the present study, we did not observe developmental changes in N1 amplitude, but observed changes in the peak-to-peak (P1-N1) analysis at the T5=/T6= electrodes. It is possible that the N1 component is affected by development, however, the preceding P1 component varied extensively across age groups, thus we did not observe a significant developmental effect in the N1 analysis, but observed it in the peak-to-peak (P1-N1) analysis. That is, P1-N1 amplitude was significantly larger in the 10-yearolds than in the adults at the occipitotemporal electrodes. Age-related changes of the N1 component have been reported in ERP-based studies on face perception: with upright faces (Taylor et al., 1999) and inverted faces (Taylor et al., 2001). Moreover, another study reported an age-related change in N170 amplitude when the adult group was included (Itier and Taylor, 2004). The observed age-related alteration of P1-N1 amplitude at occipitotemporal electrodes in the present study implies that the neural processing related to visual processing of the PLW stimulus has developed by the age of 10. Consistent with the present findings, a previous study reported that the N1 latency decreases linearly with age (Mitchell and Neville, 2004). By using unidirectional linear motion stimuli, an age-related change in N1 latency was reported (Langrova et al., 2006). Even when using the face-specific N170 component, developmental changes were also reported (Taylor et al., 2001; Itier and Taylor, 2004). Consistent with these findings, the regression analysis performed in the present study showed that N1 latency was significantly decreased with age at all electrodes except for PLW stimulus at T5= electrode. One explanation for the developmental change showing a decrease in N1 latency might be increased expertise for the visual processing of the PLW stimulus. Such a specialization might also be addressed by measuring reaction time to detect the BM stimulus. N2 component Concurrent with previous ERP studies (Hirai et al., 2003; Jokisch et al., 2005; Hirai and Kakigi, 2008), N2 amplitude was modulated by stimulus at the T5=/T6= electrodes. A previous study showed that amplitudes induced by PLW stimulus were significantly larger than those induced by sPLW stimulus, with no conditional differences in N2 latency (Hirai et al., 2003). Although functional interpretation has not been determined, it has been proposed that the N2 component reflects processing of biologically relevant information (Hirai et al., 2003; Jokisch et al., 2005) or human shape from point-light motion patterns (Hirai and Kakigi, 2008). This interpretation is based on the fact that the amplitude of the N2 component did not differ significantly between responses to inverted and upright PLW stimuli, but was less pronounced in response to SM, indicating similar processing for upright and inverted BM conditions in later processing stages (Jokisch et al., 2005). Thus, this finding suggests that the later evoked responses can reflect the fine analysis of motion patterns, which provide biologically relevant information. Furthermore, Jokisch et al. (2005) reported that the N2 component was generated

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from the FG, anterior cingulate gyrus, medial frontal gyrus, and superior temporal gyrus (STG). Supporting this, many fMRI studies have indicated that the pSTS and FG play important roles in BM processing (see, for example, Bonda et al., 1996; Grossman et al., 2000; Grossman and Blake, 2002). In the present study, a consistent age-related difference in the N2 component was not observed. This might be due to maturation of cortical structures within the vicinity of STS and FG regions. Longitudinal studies of human cortical gray matter density have revealed that the small area in the posterior section of the STG undergoes early maturation (Gogtay et al., 2004). Perhaps due to early maturation of the posterior STG, it is not possible to observe developmental effects on the amplitudes of the N2 components. Contrary to the present findings, a recent neuroimaging study suggested that the differential activation pattern in STS and fusiform face area (FFA), FG, or occipital face area (OFA) to face stimulus was observed between a 5– 8-year old group and a 11–14-year old group (Passarotti et al., 2003; Scherf et al., 2007). Another fMRI study investigated developmental changes in the neural responses to a BM stimulus in school-aged children, 7–10 years old (Passarotti et al., 2003; Carter and Pelphrey, 2006), although point-light motion technique was not employed, but rather a biological figure (a walking human), as well as the following: BM by a non-biological figure (a walking robot); disorganized, non-BM by a disjointed mechanical figure; and organized, non-BM by a grandfather clock. They found that a network of brain regions, including the STS region, responded more strongly to biological stimuli than to non-BM stimuli. They also identified a developmental change that suggested increased specificity for BM with age in the STS region (Carter and Pelphrey, 2006). It is difficult to directly compare fMRI findings with the present ERP results, due to (1) differences of visual stimuli (not point-light motion stimulus, but textured stimulus), and (2) methodological differences between fMRI and ERP studies (see, for example; Foucher et al., 2003) and (3) the different numbers of participants in different study designs. Nevertheless, the STS neural response to the BM stimulus was enhanced, compared with the non-BM stimulus, and this was observed in both studies. However, contrary to their findings, we did not observe an agerelated change in the amplitudes of N2 components. Further studies should be performed to address developmental changes in these late components, which could be involved in the processing of PLW stimuli.

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detected BM without masking noise (Pavlova et al., 2001; Jordan et al., 2002; Blake et al., 2003; Freire et al., 2006). However, a separate behavioral study suggested that “sensitivity” to BM (detecting BM from the masking noise dots) in 6-year-olds was significantly poorer than that in adults (Freire et al., 2006). To verify developmental changes in electrophysiological responses to BM stimulus, further studies are needed to investigate the relationship between behavioral performance and electrophysiological responses, and to clarify how masking noise affects each component, as well as how these components are modulated by development. As Freire et al. (2006) pointed out, BM processing involves the visual processing of global motion and formfrom-motion. Thus, in addition to the masking paradigm for BM detection, the relationship between BM processing and other forms of visual processing, such as visual processing of global motion and form-from-motion, should also be elucidated. It has been demonstrated that sensitivity to global motion reaches adult levels by the age of 4 years (Parrish et al., 2005); however, the degree of sensitivity to global motion varied with speed and direction of stimulus (Ellemberg et al., 2004). When testing form-from-motion processing, 7– 8-year-old children reached an adult level when asked to identify letters or shapes defined by dots that moved coherently in opposite directions (Giaschi and Regan, 1997; Parrish et al., 2005). Furthermore, other studies suggest that development of form-from-motion processing matures by 10 –11 years of age (Gunn et al., 2002). Based on these behavioral findings, the relationship between developmental changes in electrophysiological responses to both global motion processing and formfrom-motion processing, as well as responses to BM processing, should be further explored.

CONCLUSION In the present study, we measured ERPs during perception of PLW stimulus in 50 children, between 7 and 14 years of age. The results demonstrated that P1 amplitude and N1 latency decrease linearly during development, as revealed by regression analysis, and that P1-N1 amplitude changes with development, although the amplitudes of N2 components are not coherently altered by development. This provides the direct electrophysiological evidence for developmental changes of PLW processing.

Developmental changes for BM processing during childhood

Acknowledgments—We gratefully thank all the children and parents for their participation. We thank Mr. Y. Takeshima, and Ms. M. Teruya for technical support. M.H. was supported by a Grantin-Aid for JSPS Fellows No. 18-11826 from the Ministry of Education, Science, Sports and Culture, Japan.

Similar ERP components were observed in the present study as previously reported in adult ERP studies (Hirai et al., 2003; Jokisch et al., 2005; Hirai and Kakigi, 2008). The electrophysiological responses of N1 and N2 components to a PLW stimulus were enhanced compared with their responses to an sPLW stimulus in all age groups. In agreement with the present ERP results, several behavioral studies reported that children as young as 5 years of age

Allison T, Puce A, McCarthy G (2000) Social perception from visual cues: role of the STS region. Trends Cogn Sci 4:267–278. Allison T, Puce A, Spencer DD, McCarthy G (1999) Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli. Cereb Cortex 9:415– 430.

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(Accepted 12 March 2009) (Available online 20 March 2009)