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Frontal non-invasive neurostimulation modulates antisaccade preparation in non-human primates.

Valero-Cabre A, Wattiez N, Monfort M, François C, Rivaud-Péchoux S, Gaymard B, Pouget P - PLoS ONE (2012)

Bottom Line: We show that online single pulse TMS significantly modulated antisaccade latencies.Such effects proved dependent on TMS site (effects on FEF but not on an actively stimulated control site), TMS modality (present under active but not sham TMS on the FEF area), TMS intensity (intensities of at least 40% of the TMS machine maximal output required), TMS timing (more robust for pulses delivered at 150 ms than at 100 post target onset) and visual hemifield (relative latency decreases mainly for ipsilateral AS).Our results demonstrate the feasibility of using TMS to causally modulate antisaccade-associated computations in the non-human primate brain and support the use of this approach in monkeys to study brain function and its non-invasive neuromodulation for exploratory and therapeutic purposes.

View Article: PubMed Central - PubMed

Affiliation: Université Pierre et Marie Curie, CNRS UMR 7225, INSERM UMRS 975, Institut du Cerveau et la Möelle (ICM), Paris, France. antoni.valerocabre@upmc.fr

ABSTRACT
A combination of oculometric measurements, invasive electrophysiological recordings and microstimulation have proven instrumental to study the role of the Frontal Eye Field (FEF) in saccadic activity. We hereby gauged the ability of a non-invasive neurostimulation technology, Transcranial Magnetic Stimulation (TMS), to causally interfere with frontal activity in two macaque rhesus monkeys trained to perform a saccadic antisaccade task. We show that online single pulse TMS significantly modulated antisaccade latencies. Such effects proved dependent on TMS site (effects on FEF but not on an actively stimulated control site), TMS modality (present under active but not sham TMS on the FEF area), TMS intensity (intensities of at least 40% of the TMS machine maximal output required), TMS timing (more robust for pulses delivered at 150 ms than at 100 post target onset) and visual hemifield (relative latency decreases mainly for ipsilateral AS). Our results demonstrate the feasibility of using TMS to causally modulate antisaccade-associated computations in the non-human primate brain and support the use of this approach in monkeys to study brain function and its non-invasive neuromodulation for exploratory and therapeutic purposes.

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Estimate of discomfort induced by TMS.Estimation of discomfort based on the interaction between percent of initiated trials (used as an indirect correlate of the level of discomfort; the higher the discomfort the lower the number of initiated trials) and TMS intensity (% of machine maximal output). (Upper panel) Note that below 50% intensity, low discomfort is inferred from the high percent of initiated trials (grey and black lines) respectively for monkey ‘C’ and ‘Y’, for the TMS condition (dotted lines) as compared to the sham TMS condition (solid lines). (Bottom panel) Representative traces of eye movement with/without TMS (respectively grey, black lines) at 50% intensity for one of the monkeys. At least for the two SOAs used in the study (100 and 150 ms) eye movement metrics were not affected by TMS. Furthermore, no saccades were elicited by the stimulation.
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pone-0038674-g004: Estimate of discomfort induced by TMS.Estimation of discomfort based on the interaction between percent of initiated trials (used as an indirect correlate of the level of discomfort; the higher the discomfort the lower the number of initiated trials) and TMS intensity (% of machine maximal output). (Upper panel) Note that below 50% intensity, low discomfort is inferred from the high percent of initiated trials (grey and black lines) respectively for monkey ‘C’ and ‘Y’, for the TMS condition (dotted lines) as compared to the sham TMS condition (solid lines). (Bottom panel) Representative traces of eye movement with/without TMS (respectively grey, black lines) at 50% intensity for one of the monkeys. At least for the two SOAs used in the study (100 and 150 ms) eye movement metrics were not affected by TMS. Furthermore, no saccades were elicited by the stimulation.

Mentions: Trials with blinking responses interfering with eye recordings or incomplete AS were eliminated from the data set. Such trials represented less than 2% in the No TMS condition, 5% for low level and 20% in high TMS stimulation, respectively (see Figure 4). The AS latency for each individual trial was calculated as the time between stimulus presentation and the onset derivative of the eye saccade velocity reaching a speed of 30 deg/s. Individual AS latency values were averaged for trials under TMS (TMS-trials) and compared to those without stimulation (no-TMS trials), for each session and experimental condition explored in the study on each monkey (see Supplementary Table S1 for average antisaccade raw latency values for each monkey and experimental condition in milliseconds). Sets of saccade latencies under active/sham and no-TMS trials for each experimental condition were statistically compared by means of non-parametric signed Rank-Sum Wilcoxon tests.


Frontal non-invasive neurostimulation modulates antisaccade preparation in non-human primates.

Valero-Cabre A, Wattiez N, Monfort M, François C, Rivaud-Péchoux S, Gaymard B, Pouget P - PLoS ONE (2012)

Estimate of discomfort induced by TMS.Estimation of discomfort based on the interaction between percent of initiated trials (used as an indirect correlate of the level of discomfort; the higher the discomfort the lower the number of initiated trials) and TMS intensity (% of machine maximal output). (Upper panel) Note that below 50% intensity, low discomfort is inferred from the high percent of initiated trials (grey and black lines) respectively for monkey ‘C’ and ‘Y’, for the TMS condition (dotted lines) as compared to the sham TMS condition (solid lines). (Bottom panel) Representative traces of eye movement with/without TMS (respectively grey, black lines) at 50% intensity for one of the monkeys. At least for the two SOAs used in the study (100 and 150 ms) eye movement metrics were not affected by TMS. Furthermore, no saccades were elicited by the stimulation.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3368878&req=5

pone-0038674-g004: Estimate of discomfort induced by TMS.Estimation of discomfort based on the interaction between percent of initiated trials (used as an indirect correlate of the level of discomfort; the higher the discomfort the lower the number of initiated trials) and TMS intensity (% of machine maximal output). (Upper panel) Note that below 50% intensity, low discomfort is inferred from the high percent of initiated trials (grey and black lines) respectively for monkey ‘C’ and ‘Y’, for the TMS condition (dotted lines) as compared to the sham TMS condition (solid lines). (Bottom panel) Representative traces of eye movement with/without TMS (respectively grey, black lines) at 50% intensity for one of the monkeys. At least for the two SOAs used in the study (100 and 150 ms) eye movement metrics were not affected by TMS. Furthermore, no saccades were elicited by the stimulation.
Mentions: Trials with blinking responses interfering with eye recordings or incomplete AS were eliminated from the data set. Such trials represented less than 2% in the No TMS condition, 5% for low level and 20% in high TMS stimulation, respectively (see Figure 4). The AS latency for each individual trial was calculated as the time between stimulus presentation and the onset derivative of the eye saccade velocity reaching a speed of 30 deg/s. Individual AS latency values were averaged for trials under TMS (TMS-trials) and compared to those without stimulation (no-TMS trials), for each session and experimental condition explored in the study on each monkey (see Supplementary Table S1 for average antisaccade raw latency values for each monkey and experimental condition in milliseconds). Sets of saccade latencies under active/sham and no-TMS trials for each experimental condition were statistically compared by means of non-parametric signed Rank-Sum Wilcoxon tests.

Bottom Line: We show that online single pulse TMS significantly modulated antisaccade latencies.Such effects proved dependent on TMS site (effects on FEF but not on an actively stimulated control site), TMS modality (present under active but not sham TMS on the FEF area), TMS intensity (intensities of at least 40% of the TMS machine maximal output required), TMS timing (more robust for pulses delivered at 150 ms than at 100 post target onset) and visual hemifield (relative latency decreases mainly for ipsilateral AS).Our results demonstrate the feasibility of using TMS to causally modulate antisaccade-associated computations in the non-human primate brain and support the use of this approach in monkeys to study brain function and its non-invasive neuromodulation for exploratory and therapeutic purposes.

View Article: PubMed Central - PubMed

Affiliation: Université Pierre et Marie Curie, CNRS UMR 7225, INSERM UMRS 975, Institut du Cerveau et la Möelle (ICM), Paris, France. antoni.valerocabre@upmc.fr

ABSTRACT
A combination of oculometric measurements, invasive electrophysiological recordings and microstimulation have proven instrumental to study the role of the Frontal Eye Field (FEF) in saccadic activity. We hereby gauged the ability of a non-invasive neurostimulation technology, Transcranial Magnetic Stimulation (TMS), to causally interfere with frontal activity in two macaque rhesus monkeys trained to perform a saccadic antisaccade task. We show that online single pulse TMS significantly modulated antisaccade latencies. Such effects proved dependent on TMS site (effects on FEF but not on an actively stimulated control site), TMS modality (present under active but not sham TMS on the FEF area), TMS intensity (intensities of at least 40% of the TMS machine maximal output required), TMS timing (more robust for pulses delivered at 150 ms than at 100 post target onset) and visual hemifield (relative latency decreases mainly for ipsilateral AS). Our results demonstrate the feasibility of using TMS to causally modulate antisaccade-associated computations in the non-human primate brain and support the use of this approach in monkeys to study brain function and its non-invasive neuromodulation for exploratory and therapeutic purposes.

Show MeSH
Related in: MedlinePlus