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Motor properties of peripersonal space in humans.

Serino A, Annella L, Avenanti A - PLoS ONE (2009)

Bottom Line: In monkeys, fronto-parietal networks are involved both in integrating multisensory information within a limited space surrounding the body (i.e. peripersonal space, PPS) and in action planning and execution, suggesting an overlap between sensory representations of space and motor representations of action.Such auditory modulation of hand motor representation was specific to a hand-centred, and not a body-centred reference frame.This pattern of corticospinal modulation highlights the relation between space and time in the pps representation: an early facilitation for near stimuli may reflect immediate motor preparation, whereas, at later time intervals, motor preparation relates to distant stimuli potentially approaching the body.

View Article: PubMed Central - PubMed

Affiliation: Dipartimento di Psicologia, Università degli Studi di Bologna, Bologna, Italy. andrea.serino@unibo.it

ABSTRACT

Background: A stimulus approaching the body requires fast processing and appropriate motor reactions. In monkeys, fronto-parietal networks are involved both in integrating multisensory information within a limited space surrounding the body (i.e. peripersonal space, PPS) and in action planning and execution, suggesting an overlap between sensory representations of space and motor representations of action. In the present study we investigate whether these overlapping representations also exist in the human brain.

Methodology/principal findings: We recorded from hand muscles motor-evoked potentials (MEPs) induced by single-pulse of transcranial magnetic stimulation (TMS) after presenting an auditory stimulus either near the hand or in far space. MEPs recorded 50 ms after the near-sound onset were enhanced compared to MEPs evoked after far sounds. This near-far modulation faded at longer inter-stimulus intervals, and reversed completely for MEPs recorded 300 ms after the sound onset. At that time point, higher motor excitability was associated with far sounds. Such auditory modulation of hand motor representation was specific to a hand-centred, and not a body-centred reference frame.

Conclusions/significance: This pattern of corticospinal modulation highlights the relation between space and time in the pps representation: an early facilitation for near stimuli may reflect immediate motor preparation, whereas, at later time intervals, motor preparation relates to distant stimuli potentially approaching the body.

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Related in: MedlinePlus

Raw MEPs amplitudes recorded from the FDI (top) and the ADM muscle (bottom) in one representative subject from Experiment 1 (only 120% rMT blocks are shown).
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pone-0006582-g003: Raw MEPs amplitudes recorded from the FDI (top) and the ADM muscle (bottom) in one representative subject from Experiment 1 (only 120% rMT blocks are shown).

Mentions: Baseline MEPs were averaged and used to compute an index of MEP modulation (MEPi) during the experimental session with auditory stimulation. The ANOVA on MEPis revealed a significant four-way interaction between Space, Intensity, Delay and Experiment (F3,66 = 2.76, p<.05). To further analyze this interaction, two separate Muscle × Space × Intensity × Delay ANOVAs were performed for each Experiment. The ANOVA run on Experiment 1 data revealed a triple Space × Intensity × Delay interaction (F3,33 = 7.40, p<.0008); thus we run two separate Muscle × Space × Delay ANOVAs for each Intensity. ANOVA on MEPi recorded with the lower TMS intensity (120% rMT) revealed a significant main effect of Space (F1,11 = 5.81, p<.04) and Time (F3,33 = 5.05, p<.01) and most importantly, a highly significant Space × Delay interaction (F3,33 = 7.56, p<.003; see Figure 2A). Post-hoc comparisons (Newman-Keuls Test) showed that MEPis recorded 50 ms after sounds occurrence were significantly enhanced when sounds were administered in the NEAR (mean MEPi±s.e.m.: 113%±9) rather than in the FAR (97%±7; p<.03) space. This effect disappeared when TMS pulses were administered 100 and 200 ms after sound presentations, and MEPis were not-significantly higher when FAR (122%±9 and 124%±10 for 100 ms and 200 ms of Delay respectively) rather than NEAR (116%±11 and 113%±10) sounds were presented (ps>.46). At a delay of 300 ms from sound presentation, the MEPi modulation found at 50 ms was completely reversed: at the long delay, the MEPis were significantly higher when FAR (117%±8) rather than NEAR (92%±9; p<.005) sounds were presented. Thus, MEPs were modulated by the presentation of NEAR and FAR sounds, and the direction of the effect depended on the time delay between MEP recording and sounds presentation. The interaction Muscle × Space × Delay was not significant (F3,33 = 0.52, p = .64), indicating that the two muscles were similarly modulated as a function of space and time. Examples of raw MEPs recorded from the FDI and ADM muscle in these conditions (Experiment 1, 120% rMT) are shown in Figure 3.


Motor properties of peripersonal space in humans.

Serino A, Annella L, Avenanti A - PLoS ONE (2009)

Raw MEPs amplitudes recorded from the FDI (top) and the ADM muscle (bottom) in one representative subject from Experiment 1 (only 120% rMT blocks are shown).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2719059&req=5

pone-0006582-g003: Raw MEPs amplitudes recorded from the FDI (top) and the ADM muscle (bottom) in one representative subject from Experiment 1 (only 120% rMT blocks are shown).
Mentions: Baseline MEPs were averaged and used to compute an index of MEP modulation (MEPi) during the experimental session with auditory stimulation. The ANOVA on MEPis revealed a significant four-way interaction between Space, Intensity, Delay and Experiment (F3,66 = 2.76, p<.05). To further analyze this interaction, two separate Muscle × Space × Intensity × Delay ANOVAs were performed for each Experiment. The ANOVA run on Experiment 1 data revealed a triple Space × Intensity × Delay interaction (F3,33 = 7.40, p<.0008); thus we run two separate Muscle × Space × Delay ANOVAs for each Intensity. ANOVA on MEPi recorded with the lower TMS intensity (120% rMT) revealed a significant main effect of Space (F1,11 = 5.81, p<.04) and Time (F3,33 = 5.05, p<.01) and most importantly, a highly significant Space × Delay interaction (F3,33 = 7.56, p<.003; see Figure 2A). Post-hoc comparisons (Newman-Keuls Test) showed that MEPis recorded 50 ms after sounds occurrence were significantly enhanced when sounds were administered in the NEAR (mean MEPi±s.e.m.: 113%±9) rather than in the FAR (97%±7; p<.03) space. This effect disappeared when TMS pulses were administered 100 and 200 ms after sound presentations, and MEPis were not-significantly higher when FAR (122%±9 and 124%±10 for 100 ms and 200 ms of Delay respectively) rather than NEAR (116%±11 and 113%±10) sounds were presented (ps>.46). At a delay of 300 ms from sound presentation, the MEPi modulation found at 50 ms was completely reversed: at the long delay, the MEPis were significantly higher when FAR (117%±8) rather than NEAR (92%±9; p<.005) sounds were presented. Thus, MEPs were modulated by the presentation of NEAR and FAR sounds, and the direction of the effect depended on the time delay between MEP recording and sounds presentation. The interaction Muscle × Space × Delay was not significant (F3,33 = 0.52, p = .64), indicating that the two muscles were similarly modulated as a function of space and time. Examples of raw MEPs recorded from the FDI and ADM muscle in these conditions (Experiment 1, 120% rMT) are shown in Figure 3.

Bottom Line: In monkeys, fronto-parietal networks are involved both in integrating multisensory information within a limited space surrounding the body (i.e. peripersonal space, PPS) and in action planning and execution, suggesting an overlap between sensory representations of space and motor representations of action.Such auditory modulation of hand motor representation was specific to a hand-centred, and not a body-centred reference frame.This pattern of corticospinal modulation highlights the relation between space and time in the pps representation: an early facilitation for near stimuli may reflect immediate motor preparation, whereas, at later time intervals, motor preparation relates to distant stimuli potentially approaching the body.

View Article: PubMed Central - PubMed

Affiliation: Dipartimento di Psicologia, Università degli Studi di Bologna, Bologna, Italy. andrea.serino@unibo.it

ABSTRACT

Background: A stimulus approaching the body requires fast processing and appropriate motor reactions. In monkeys, fronto-parietal networks are involved both in integrating multisensory information within a limited space surrounding the body (i.e. peripersonal space, PPS) and in action planning and execution, suggesting an overlap between sensory representations of space and motor representations of action. In the present study we investigate whether these overlapping representations also exist in the human brain.

Methodology/principal findings: We recorded from hand muscles motor-evoked potentials (MEPs) induced by single-pulse of transcranial magnetic stimulation (TMS) after presenting an auditory stimulus either near the hand or in far space. MEPs recorded 50 ms after the near-sound onset were enhanced compared to MEPs evoked after far sounds. This near-far modulation faded at longer inter-stimulus intervals, and reversed completely for MEPs recorded 300 ms after the sound onset. At that time point, higher motor excitability was associated with far sounds. Such auditory modulation of hand motor representation was specific to a hand-centred, and not a body-centred reference frame.

Conclusions/significance: This pattern of corticospinal modulation highlights the relation between space and time in the pps representation: an early facilitation for near stimuli may reflect immediate motor preparation, whereas, at later time intervals, motor preparation relates to distant stimuli potentially approaching the body.

Show MeSH
Related in: MedlinePlus