Elsevier

NeuroImage

Volume 40, Issue 4, 1 May 2008, Pages 1841-1848
NeuroImage

Testing the validity of the TMS state-dependency approach: Targeting functionally distinct motion-selective neural populations in visual areas V1/V2 and V5/MT+

https://doi.org/10.1016/j.neuroimage.2008.02.002Get rights and content

Abstract

By making use of the phenomenon that the effects of transcranial magnetic stimulation (TMS) are dependent on the initial cortical excitability, we show that TMS can reveal the properties of distinct neural populations within the stimulated region. Visual adaptation to either simple translational or radial motion was used to manipulate the initial activity state of neural populations of different tunings prior to application of TMS. After adaptation to either leftward or rightward motion, phosphenes induced from V1/V2 and the V5/MT+ complex took on the motion properties of the adapting stimulus, consistent with evidence that both regions contain direction-selective neurons. In contrast, after adaptation to radial motion, only phosphenes induced from the V5/MT+ complex took on the motion qualities of the adapting stimulus, consistent with findings that V5/MT+ but not V1/V2 contains neurons tuned to radial motion. That phosphenes induced from the V5/MT+ complex can appear containing either simple or radial motion demonstrates that the state dependency of TMS can be used to target specific neural populations within the affected region.

Introduction

Transcranial magnetic stimulation (TMS), a technique for transiently modulating neural activity, has become a widely used tool in cognitive neuroscience. Its usefulness lies in its ability to reveal the necessity of cortical regions in cognitive functions, complementing neuroimaging techniques such as functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) that cannot assess causality (see Walsh and Pascual-Leone, 2003, Cowey, 2005 for reviews). Its spatial resolution, estimated to be approximately 1–2 cm in the visual cortex depending on stimulation parameters (Kammer, 1999), enables TMS to differentially stimulate nearby cortical regions, and it has been used to demonstrate functional dissociations between visual areas such as primary visual cortex and V5/MT (e.g., Matthews et al., 2001), occipital face area and the lateral occipital cortex (Pitcher et al., 2007), as well as the frontal eye fields and V5/MT (e.g., Campana et al., 2006, Campana et al., 2007).

Although TMS has been useful in establishing the necessity of cortical regions in cognitive functions, there are some questions that TMS has not been able to address. For instance, so far TMS has been silent regarding the properties and functions of the different neural populations within the stimulated region. Addressing such issues requires a technique that can differentially stimulate functionally distinct neural populations within a cortical area, specificity that noninvasive brain stimulation techniques such as TMS which are thought to stimulate all neural populations non-discriminately cannot seemingly offer.

It is potentially possible however to improve the functional specificity of TMS by making use of the phenomenon that the perceptual and behavioral effects of TMS depend on the relative activity state of functionally distinct neural populations within the stimulated region (Silvanto et al., 2007; cf. Silvanto and Muggleton, 2008a, Silvanto and Muggleton, 2008b). In a recent study it was shown that single-pulse TMS behaviorally and perceptually facilitates the attributes encoded by the less active/excitable neural populations (Silvanto et al., 2007). Specifically, it was shown that after adaptation to a colored stimulus, phosphenes induced from the visual cortex take on the color of the adapting stimulus (Silvanto et al., 2007); a similar result was found in a psychophysical color detection task in which TMS was applied at an intensity subthreshold for inducing phosphenes.

In the present study, we investigated whether this TMS-adaptation paradigm can be used to target specific neural populations within the stimulated region by differentially modulating the excitability of distinct neural populations prior to application of TMS. We made use of neuroimaging evidence that neurons in the human V5/MT+ complex (consisting of V5/MT and MST; cf. Huk et al., 2002) contain neural populations tuned to translational motion, as well as other neural populations tuned to radial motion (Tootell et al., 1995, Rutschmann et al., 2000, Morrone et al., 2000). By using visual adaptation to manipulate the excitability of neurons tuned to either simple translational or radial motion, we investigated whether one can systematically modulate the perceptual consequence of visual cortical TMS to reflect the properties of neurons of different tunings. The logic was that if TMS perceptually facilitates the attributes encoded by the less active/excitable neural populations, the perceptual content of TMS-induced phosphenes should reflect the receptive field properties of neurons that had been made less excitable by adaptation. Our results show that phosphenes induced from V5/MT+ can contain either radial or translational motion depending on the adapting stimulus, consistent with findings that the V5/MT+ complex contains neurons tuned to different types of motion stimuli (Tootell et al., 1995, Rutschmann et al., 2000, Morrone et al., 2000). In contrast, only adaptation to translational motion influenced the perceptual content of phosphenes induced from V1/V2, consistent with evidence that these regions contain neurons selective for translational but not for radial motion (e.g., Tootell et al., 1995, Singh et al., 2000).

Section snippets

Subjects

Twelve subjects (8 males and 4 females, aged 21 to 37, including the author J.S.) were recruited for the study (four of whom were excluded after screening due to inability to perceive moving phosphenes). All subjects gave informed consent before participating in the study which had been approved by the local ethics committee and were treated in accordance with the declaration of Helsinki.

TMS stimulation and site localization

TMS was delivered by means of a Magstim Super Rapid machine (Magstim, UK) via a 70 mm figure-of-eight shaped

Results

Prior to the adaptation experiment, subjects’ phosphene appearance was investigated in order to obtain a baseline to which the phosphenes induced after adaptation could be compared. Fig. 2 (panels A–C) depict the appearance of phosphenes induced from the left and right V1/V2 (all the figures are based on subjects’ own drawings) in three subjects. Triple-pulse TMS (30% above phosphene threshold) induced a large static phosphene in the contralateral visual field that in some subjects (see Fig. 2

Discussion

Our results show that the perceptual effects of TMS can reveal the receptive field properties of functionally distinct neural populations within the stimulated region. Consistent with evidence that V1/V2 and the V5/MT+ complex contain direction-selective neurons (e.g., Tootell et al., 1995), phosphenes induced from both regions were affected by adaptation to simple translational motion. After adaptation, phosphenes induced from V1/V2 (that normally appear static) contained the motion direction

Acknowledgments

We thank Glenn Mcgrath and Graeme Hick for their comments on the manuscript.

References (31)

  • HukA.C. et al.

    Retinotopy and functional subdivision of human areas MT and MST

    J. Neurosci.

    (2002)
  • LivingstoneM.S. et al.

    Anatomy and physiology of a color system in the primate visual cortex

    J. Neurosci.

    (1984)
  • KammerT.

    Phosphenes and transient scotomas induced by magnetic stimulation of the occipital lobe: their topographic relationship

    Neuropsychologia

    (1999)
  • MatthewsN. et al.

    Transcranial magnetic stimulation differentially affects speed and direction judgments

    Exp. Brain Res.

    (2001)
  • MazzochioR. et al.

    Effect of tonic voluntary activity on the excitability of human motor cortex

    J. Physiol.

    (1994)
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