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The Functional Effect of Transcranial Magnetic Stimulation: Signal Suppression Or Neural Noise Generation?

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The Functional Effect of Transcranial Magnetic Stimulation: Signal Suppression Or Neural Noise Generation? The Functional Effect of Transcranial Magnetic Stimulation: Signal Suppression or Neural Noise Generation? Justin A. Harris1, Colin W. G. Clifford1, and Carlo Miniussi2,3 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/20/4/734/1759438/jocn.2008.20048.pdf by guest on 18 May 2021 Abstract & Transcranial magnetic stimulation (TMS) is a popular tool cortex and measured its effect on a simple visual discrimina- for mapping perceptual and cognitive processes in the human tion task, while concurrently manipulating the level of image brain. It uses a magnetic field to stimulate the brain, modifying noise in the visual stimulus itself. TMS increased thresholds ongoing activity in neural tissue under the stimulating coil, overall; and increasing the amount of image noise systemati- producing an effect that has been likened to a ‘‘virtual lesion.’’ cally increased discrimination thresholds. However, these two However, research into the functional basis of this effect, essen- effects were not independent. Rather, TMS interacted multipli- tial for the interpretation of findings, lags behind its appli- catively with the image noise, consistent with a reduction in cation. Acutely, TMS may disable neuronal function, thereby the strength of the visual signal. Indeed, in this paradigm, there interrupting ongoing neural processes. Alternatively, the ef- was no evidence that TMS independently added noise to the fects of TMS have been attributed to an injection of ‘‘neural visual process. Thus, our findings indicate that the ‘‘virtual le- noise,’’ consistent with its immediate and effectively random sion’’ produced by TMS can take the form of a loss of signal depolarization of neurons. Here we apply an added-noise para- strength which may reflect a momentary interruption to on- digm to test these alternatives. We delivered TMS to the visual going neural processing. & INTRODUCTION is uncorrelated with the ongoing task-related activity of Transcranial magnetic stimulation (TMS) is a technique those neurons. According to this account, the signal is that uses a magnetic field to produce indirect electrical not reduced but is masked by an increase in background stimulation of the brain (Barker, Jalinous, & Freeston, noise. In either case, however, the behavioral effect will 1985). The induced stimulation modifies ongoing activ- be the same—a decline in performance. ity in the neural tissue under the stimulating coil, with Available evidence concerning the physiological re- the effect that TMS can impair performance on a wide sponse to TMS is equivocal. Moliadze, Zhao, Eysel, and range of perceptual and cognitive tasks (Cowey, 2005; Funke (2003) recorded single-unit neuronal activity in the Hallett, 2000; Pascual-Leone, Walsh, & Rothwell, 2000; cat visual cortex during presentations of single pulses of Walsh & Cowey, 2000). As such, TMS has often been TMS. They observed a pattern of excitation and inhibition described as creating a ‘‘virtual lesion’’ (Hallett, 2000; that lasted up to 500 msec after the pulse, as well as a Pascual-Leone et al., 2000), but this description can be depression of spontaneous activity lasting one or more interpreted in different ways (Walsh & Cowey, 2000). seconds. Conceptually, the induced pattern of discharge One way to describe the functional impact of TMS is that and suppression could erase whatever information was it temporarily disables neuronal function, thereby inter- carried by the precise firing pattern of the afflicted neu- rupting processing of the information (signal) carried by rons at the time of the TMS. Alternatively, the random the activity of the afflicted neurons. Thus, for example, if activity induced by the TMS could simply sum with the a target area accumulates information about a sensory neurons’ ongoing firing pattern. In other words, the ob- event, then TMS would abort that process and effectively served impact of TMS on neuronal activity could be reduce the net strength of the perceptual signal. An al- interpreted as a loss of signal strength or simply the ad- ternative view is that TMS introduces random noise dition of noise to signal processing. in neural processing by inducing neuronal activity that The present study seeks to identify the functional im- pact of TMS, and in particular, to test whether TMS adds noise to signal processing or reduces signal strength. We 1The University of Sydney, Australia, 2University of Brescia, Brescia, adopt a formal statistical definition of noise that allows Italy, 3Cognitive Neuroscience, IRCCS, Brescia, Italy us to describe how signal information and noise interact D 2008 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 20:4, pp. 734–740 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.2008.20048 by guest on 30 September 2021 and therefore derive distinct testable predictions about the effect of TMS. We measured the effect of TMS de- livered to the visual cortex of human subjects while they performed a simple visual discrimination task. We con- currently manipulated the level of image noise in the visual stimulus itself (Figure 1). Threshold contrast pow- er, T2, is a direct linear function of the variance of the noise added to the image (Green & Swets, 1966; see Analysis section under the Methods section below for a 2 detailed description of the relationship between T and Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/20/4/734/1759438/jocn.2008.20048.pdf by guest on 18 May 2021 image noise). Therefore, if TMS adds further noise, this will produce an overall increase in T2, observable as a leftward shift in the line relating T2 to the variance of image noise. Indeed, if TMS noise and image noise have Figure 2. Graphical illustrations of three hypothesized effects of equivalent effects on signal processing, then TMS should TMS on squared detection thresholds as plotted against variance 2 cause a fixed increase in T , and thus, produce a parallel of image noise. (A) shows a parallel leftward shift induced by the shift in the relation between T2 and image noise (as il- simple addition of noise from TMS; (B) shows a leftward shift and lustrated in Figure 2A). However, the shift may not be increase in slope created by TMS-induced noise added downstream parallel if the response of the visual system to the image of a gain control process operating on the signal and image noise; (C) shows an increase in slope (without leftward shift) created by (including noise present in the image) is subject to non- a TMS-induced decrease in signal strength (relative to noise). Note linear gain control (e.g., Heeger, 1993) operating ‘‘up- that an increase in threshold indicates a decrease in sensitivity, and stream’’ from the site of TMS. A gain control process therefore lower threshold2 values reflect better performance. would moderate the response of the visual system as the overall contrast of the stimulus increases, keeping the gain in the system constant, and therefore, increasing the signal and increasing the slope of the line relating T2 to amount of image noise would cause a proportional reduc- image noise (Figure 2C; see Pelli & Farell, 1999). For tion in signal strength. If TMS affects neurons ‘‘down- example, with a spatially periodic pattern, such as the stream’’ of this gain control, the amount of noise added sine wave grating we have used here, information about by TMS would increase relative to the signal strength as the visual image requires the integration of activity the image noise increased, even though the amount of across a distributed population of cortical neurons. In random neuronal activity induced by TMS would be con- this case, the total signal strength would increase ap- stant. As a result, there would be an interaction between proximately linearly with an increase in the number of the effects of TMS and image noise (see Dao, Lu, & neurons responding to the stimulus. In contrast, uncor- Dosher, 2006), such that TMS would increase the slope related noise (both internally generated neural noise of the line relating to T2 to the variance of image noise, and image noise) would increase with the square root of as well as shifting that line to the left (Figure 2B). the number of neurons because the variances of un- Alternatively, TMS may reduce the efficiency of visual correlated sources of noise combine additively, and processing without adding noise, and therefore, without thus, the standard deviation increases as the square root inducing a leftward shift in the line relating T2 to image of the summed variances. Therefore, if TMS interrupted noise. This could occur if TMS interrupts visual process- ongoing activity in half of these cortical neurons, this ing, thereby reducing the effective strength of the visual would reduce the strength of the signal representing the Figure 1. (A) The target stimulus was presented on a mid-gray background in the lower right visual field (at the perceived location of phosphenes induced beforehand by TMS pulses), and the contrast was varied to measure the participant’s detection threshold. (B, C) Image noise was added by superimposing spatial white noise, drawn from a uniform distribution, onto the grating. These examples show noise variances of 0.0033 (B) and 0.0133 (C). Harris, Clifford, and Miniussi 735 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.2008.20048 by guest on 30 September 2021 grating by 50% but reduce the uncorrelated noise by (approximately 1 cm above and to the left of the inion). only 30%. That is, the efficiency of the visual system The position of the coil, and amplitude of stimulation would be reduced. It should be noted that the degree of output, was varied to find the location and lowest inten- reduction would depend on the noise correlation be- sity that could reliably induce phosphenes (with the tween neurons. If noise is positively correlated between participant’s eyes closed and ambient illumination kept neurons, this will increase the sum of the variance across low).
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