A governing assumption about repetitive transcranial magnetic stimulation (rTMS) has been that it interferes with task-related neuronal activity – in effect, by “injecting noise” into the brain – and thereby disrupts behavior. Recent reports of rTMS-produced behavioral enhancement, however, call this assumption into question. We investigated the neurophysiological effects of rTMS delivered during the delay period of a visual working memory task by simultaneously recording brain activity with electroencephalography (EEG). Subjects performed visual working memory for locations or for shapes, and in half the trials a 10-Hz train of rTMS was delivered to the superior parietal lobule (SPL) or a control brain area. The wide range of individual differences in the effects of rTMS on task accuracy, from improvement to impairment, was predicted by individual differences in the effect of rTMS on power in the alpha-band of the EEG (∼10 Hz): a decrease in alpha-band power corresponded to improved performance, whereas an increase in alpha-band power corresponded to the opposite. The EEG effect was localized to cortical sources encompassing the frontal eye fields and the intraparietal sulcus, and was specific to task (location, but not object memory) and to rTMS target (SPL, not control area). Furthermore, for the same task condition, rTMS-induced changes in cross-frequency phase synchrony between alpha- and gamma-band (>40 Hz) oscillations predicted changes in behavior. These results suggest that alpha-band oscillations play an active role cognitive processes and do not simply reflect absence of processing. Furthermore, this study shows that the complex effects of rTMS on behavior can result from biasing endogenous patterns of network-level oscillations.
Abstract■ Verbal working memory ( VWM), the ability to maintain and manipulate representations of speech sounds over short periods, is held by some influential models to be independent from the systems responsible for language production and comprehension [e.g., Baddeley, A. D. Working memory, thought, and action. New York, NY: Oxford University Press, 2007]. We explore the alternative hypothesis that maintenance in VWM is subserved by temporary activation of the language production system [Acheson, D. J., & MacDonald, M. C. Verbal working memory and language production: Common approaches to the serial ordering of verbal information. Psychological Bulletin, 135, 50-68, 2009b]. Specifically, we hypothesized that for stimuli lacking a semantic representation (e.g., nonwords such as mun), maintenance in VWM can be achieved by cycling information back and forth between the stages of phonological encoding and articulatory planning. First, fMRI was used to identify regions associated with two different stages of language production planning: the posterior superior temporal gyrus (pSTG) for phonological encoding (critical for VWM of nonwords) and the middle temporal gyrus (MTG) for lexical-semantic retrieval (not critical for VWM of nonwords). Next, in the same subjects, these regions were targeted with repetitive transcranial magnetic stimulation (rTMS) during language production and VWM task performance. Results showed that rTMS to the pSTG, but not the MTG, increased error rates on paced reading (a language production task) and on delayed serial recall of nonwords (a test of VWM). Performance on a lexical-semantic retrieval task (picture naming), in contrast, was significantly sensitive to rTMS of the MTG. Because rTMS was guided by language production-related activity, these results provide the first causal evidence that maintenance in VWM directly depends on the long-term representations and processes used in speech production. ■
Abstract& Understanding the contributions of the prefrontal cortex (PFC) to working memory is central to understanding the neural bases of high-level cognition. One question that remains controversial is whether the same areas of the dorsolateral PFC (dlPFC) that participate in the manipulation of information in working memory also contribute to its short-term retention (STR). We evaluated this question by first identifying, with functional magnetic resonance imaging (fMRI), brain areas involved in manipulation. Next, these areas were targeted with repetitive transcranial magnetic stimulation (rTMS) while subjects performed tasks requiring only the STR or the STR plus manipulation of information in working memory. fMRI indicated that manipulation-related activity was independent of retention-related activity in both the PFC and superior parietal lobule (SPL). rTMS, however, yielded a different pattern of results. Although rTMS of the dlPFC selectively disrupted manipulation, rTMS of the SPL disrupted manipulation and STR to the same extent. rTMS of the postcentral gyrus (a control region) had no effect on performance. The implications of these results are twofold. In the PFC, they are consistent with the view that this region contributes more importantly to the control of information in working memory than to its STR. In the SPL, they illustrate the importance of supplementing the fundamentally correlational data from neuroimaging with a disruptive method, which affords stronger inference about structure-function relations. &
Functional neuroimaging studies have produced contradictory data about the extent to which specific regions of the frontal and the posterior parietal cortices contribute to the retention of information in spatial working memory. We used high frequency repetitive transcranial magnetic stimulation (rTMS) to assess the necessity for the short-term retention of spatial information of brain areas identified by previous functional imaging studies: dorsolateral prefrontal cortex (dlPFC), frontal eye fields (FEF), superior parietal lobule (SPL) and intraparietal sulcus (IPS). 10 Hz rTMS spanned the 3-sec delay period of a spatial delayed-recognition task. The postcentral gyrus (PCG) was included to control for any regionally nonspecific effects of rTMS. The only regionally specific effect was a significant decrease in reaction time when rTMS was applied to SPL. Additionally, rTMS lowered accuracy to a greater extent when applied to left than to right hemisphere, and was more disruptive when applied contralaterally vs. ipsilaterally to the visual field in which the memory probe was presented. Although seemingly paradoxical, the finding of rTMS-induced improvement in task performance has a precedent, and is consistent with the idea that regions associated with spatial sensory-motor processing make necessary contributions to the short-term retention of this information. Possible factors underlying rTMS-induced behavioral facilitation are considered.
Background-Many recent studies have employed repetitive transcranial magnetic stimulation (rTMS) to study brain-behavior relationships. However, the pulse-to-pulse neural effects of rapid delivery of multiple TMS pulses are unknown largely because of TMS-evoked electrical artifacts limiting recording of brain activity.
The dorsolateral prefrontal cortex (dlPFC) plays an important role in working memory, including the control of memory-guided response. In this study, with 24 subjects, we used high frequency repetitive transcranial magnetic stimulation (rTMS) to evaluate the role of the dlPFC in memory-guided response to two different types of spatial working memory tasks: one requiring a recognition decision about a probe stimulus (operationalized with a yes/no button press), another requiring direct recall of the memory stimulus by moving a cursor to the remembered location. In half the trials, randomly distributed, rTMS was applied to the dlPFC and in a separate session, the superior parietal lobule (SPL), a brain area implicated in spatial working memory storage. A 10-Hz (3 sec., 110% of motor threshold) train of TMS was delivered at the onset of the response period. We found that only dlPFC rTMS significantly affected performance, with rTMS of right dlPFC decreasing accuracy on delayed-recall trials, and rTMS of left and right dlPFC decreasing and enhancing accuracy, respectively, on delayed-recognition trials. These findings confirm that the dlPFC plays an important role in memory-guided response, and suggest that the nature of this role varies depending on the processes required for making a response.
A commonly held view is that repetitive TMS (rTMS) influences behavior by producing transient "virtual lesions" in targeted tissue. However, findings of rTMS-related improvements in performance are difficult to reconcile with this assumption. With regard to the the mechanism of rTMS, a combined rTMS/EEG study conducted in our lab has revealed a complex set of relations between rTMS, EEG activity, and behavioral performance, with the effects of rTMS on power in the alpha band and on alpha:gamma phase synchrony each predicting its effect on behavior. These findings suggest that rTMS influences performance by biasing endogenous task-related oscillatory dynamics, rather than creating a "virtual lesion". To further differentiate these two alternatives, in the present study we compared the effects of 10 Hz rTMS on neural activity with the results of an experiment in which rTMS was replaced with 10 Hz luminance flicker. We reasoned that 10 Hz flicker would produce widespread entrainment of neural activity to the flicker frequency, and comparison of these EEG results with those from the rTMS study would shed light on whether the latter also reflected entrainment to an exogenous stimulus. Results revealed pronounced evidence for "entrainment noise" produced by 10 Hz flicker -increased oscillatory power and inter-trial coherence (ITC) at the driving frequency, and increased alpha:gamma phase synchronization --that were nonetheless largely uncorrelated with behavior. This contrasts markedly with 10-Hz rTMS, for which the only evidence for stimulation-induced noise, elevated ITC at 30 Hz, differed qualitatively from the flicker results. Simultaneous recording of the EEG thus offers an important means of directly testing assumptions about how rTMS exerts its effects on behavior.
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