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Cortical Stimulation Consolidates and Reactivates Visual OPEN Cortical stimulation consolidates and SUBJECT AREAS: reactivates visual experience: neural PERCEPTION CONSCIOUSNESS plasticity from magnetic entrainment of PSYCHOLOGY VISUAL SYSTEM visual activity Hsin-I Liao1,3, Daw-An Wu1, Neil Halelamien2 & Shinsuke Shimojo1,2 Received 15 March 2013 1Division of Biology, California Institute of Technology, USA, 2Computation and Neural Systems, California Institute of Technology, Accepted USA, 3NTT Communication Science Laboratories, NTT Corporation, Japan. 2 July 2013 Published Delivering transcranial magnetic stimulation (TMS) shortly after the end of a visual stimulus can cause a 18 July 2013 TMS-induced ‘replay’ or ‘visual echo’ of the visual percept. In the current study, we find an entrainment effect that after repeated elicitations of TMS-induced replay with the same visual stimulus, the replay can be induced by TMS alone, without the need for the physical visual stimulus. In Experiment 1, we used a subjective rating task to examine the phenomenal aspects of TMS-entrained replays. In Experiment 2, we Correspondence and used an objective masking paradigm to quantitatively validate the phenomenon and to examine the requests for materials involvement of low-level mechanisms. Results showed that the TMS-entrained replay was not only should be addressed to phenomenally experienced (Exp.1), but also able to hamper letter identification (Exp.2). The findings have H.I.L. (liao.hsini@lab. implications in several directions: (1) the visual cortical representation and iconic memory, (2) ntt.co.jp) experience-based plasticity in the visual cortex, and (3) their relationship to visual awareness. ranscranial Magnetic Stimulation (TMS) is a non-invasive technique for stimulating the human brain. TMS is able to suppress or activate neural processes in cortex, depending on the functional context, state of the brain, and parameters of stimulation1. TMS can be used to stimulate visual cortex, inducing perception of T 2 brief flashes of light, termed phosphenes . TMS-induced phosphenes are generally perceived to be colorless or palely colored flashes of light, shaped as blobs, radial wedges, or quadrantic fills. However, the visual experiences induced by TMS can differ when visual cortex is already at a non-baseline state at the time of stimulation. For example, if the participant has been pre- adapted using colored light, then TMS elicits a phosphene that is tinted with the adapted color3,4. This visual percept reflects the altered activity and excitability states across neurons in the adapted cortex. It is hypothesized that the subset of neurons stimulated by the adapting color becomes more easily activated by TMS following the adaptation period3,4. The perceptual content of cortical states can be revealed in an even more vivid fashion when probed imme- diately following the offset of a brief visual stimulus. When TMS is delivered to visual cortex shortly after a visual stimulus has been seen, the participant can re-perceive a portion of the preceding visual stimulus, a phenomenon termed a ‘‘replay’’5–8 or ‘‘visual echo’’9. This effect is optimal with TMS following the visual stimulus by 200– 400 ms, though lesser effects can be seen using somewhat larger delays. Phenomenology varies across conditions and observers. In the strongest instances of replay, the percept has been described as appearing to be ‘‘cut out’’ from the preceding visual stimulus. In weaker cases, the participant perceives something resembling a typical formless phosphene, except embedded with contours or colors from the preceding visual stimulus. These per- ceptual effects likely reflect organized activity and excitability states left in the wake of the visual stimulus. As in the simpler color adaptation example, visual cortical circuits may remain in perceptually organized excitability states for some time following the conclusion of visual stimulation3,4. In the course of conducting our research into TMS-induced replay, it was occasionally noted that TMS alone would sometimes elicit a replay-like effect. The participant would see features of visual stimuli from preceding trials, even though the TMS delay to the visual stimulus (6–10 seconds) were much longer than the usual effective periods which are within 400 ms. These events tended to occur after extended testing of the replay effect, especially if the same visual stimulus was used repeatedly. This suggested that organized cortical excitability SCIENTIFIC REPORTS | 3 : 2228 | DOI: 10.1038/srep02228 1 www.nature.com/scientificreports states were persisting longer than usual, as if the cortical states were the subjective strength and its timecourse of the entrainment effect becoming entrained due to repeated pairings of TMS with a visual following the learning phase. stimulus. An experimental run consisted of 15 trials (illustrated in Fig. 1a). In the current study, we examine this entrainment phenomenon The first ten were replay learning trials, where a visual stimulus was directly. Experiment 1 characterizes the subjective experience of an followed by TMS with a 300 ms stimulus onset asynchrony (SOA). entrained TMS replay based on subjective strength ratings, and The last five trials were test trials, containing only TMS. Inter-trial examines the conditions necessary to induce entrainment. Experi- intervals were 6 seconds, to allow the TMS units to recharge. ment 2 validates the phenomenon by measuring performance levels Following each trial, the participant gave integer ratings ranging on an objective target discrimination task, where the TMS-entrained from 1–9 for the vividness of TMS-induced replay percepts. A rating replay operated as a masker to suppress visibility of a target. This of 9 would mean that TMS caused them to see a vivid duplication of functional measure of the effect also tests the hypothesis about the the visual stimulus. When they perceived a TMS-induced phosphene underlying neural mechanism that the replay and ordinary percepts but not the replay, they were instructed to give the rating number as share early visual cortical circuits. 0. The basic structure of the experiments included two types of trials. Because the visual effect of TMS varies across participants (some In learning trials, a visual stimulus is followed by TMS, causing a participants see no effects at all in response to TMS, not even a replay effect each time. These trials are repeated back-to-back in such phosphene), we performed a preliminary screening to determine a paired fashion of visual stimulus and TMS in order to induce an the proportion of participants who saw phosphenes, replay and entraining effect. In subsequent test trials, TMS is delivered without a entrainment (see Methods for details). Among 19 participants visual stimulus. While TMS in isolation normally results only in a recruited in the preliminary screening, 17 participants reported see- phosphene, some participants would see a replay of the visual stimu- ing phosphenes in response to TMS. Of those 17, 14 reported a replay lus used during these test trials, which we define as a ‘‘TMS entrain- percept. Finally, among the 14 participants who perceived replays, 10 ment effect’’. reported perceiving entrainment. That is, in the test phase of the experiment, they continued to report seeing a replayed visual stimu- Results lus in response to TMS (i.e., the rating score of the test phase was higher than zero, t(9) 5 4.09, P 5 .003, two-tailed). A timecourse of Experiment 1: timecourse of subjective experience, and conditions their reports and the average scores across participants, are shown in necessary for entrainment. To examine the subjective experiences of Figure 2 (in red). A replotting of the figure to include all the parti- the TMS entrainment effect, we asked the participants to rate the cipants who perceived replays regardless whether or not perceiving vividness of replay percepts throughout the learning and test phases. entrainment (n 5 14) in the average, compared to the participants This produced ratings of standard replay percepts and the entrained who perceived entrainment (n 5 10) is shown in Supplementary replay percepts on a common explicit scale, and allowed us to trace Figure 1. It shows, that for all the participants who reported a replay percept, the average result still indicated the entrainment effect [11th– 15th trials’ mean6SEM5 1.64 6 0.49; the Student’s one-sample t- Test showed that the mean was significant higher than 0, t(13) 5 3.44, P 5 .004, two-tailed]. To examine the conditions necessary for inducing entrainment, we ran a control version of the learning phase (Fig. 1b) in which the visual stimuli and TMS were presented out of phase, separated by 3 seconds. This counter-phase presentation exposed the participant to the same number of TMS pulses and visual stimuli, but did not allow the two types of stimuli to interact to cause a replay. It tested the Figure 1 | Procedure of Experiment 1. The vertical black lines represent the timing of visual stimulus appearing on the monitor; the red lines represent the timing of the paired-pulse TMS (50 ms between the pulses) to visual cortex. (a) In the perceptual entrainment condition, the visual stimulus was followed by the TMS with 300 ms delay in the learning phase. Figure 2 | Results of Experiment 1. Individual (cross symbols) and Trials were separated by 6-second intervals. After 10 trials repetition, only average (solid lines) rating scores as a function of trial numbers in the TMS was delivered to examine whether replay or phosphene was perceived. perceptual entrainment condition (red) and the control condition (blue). (b) In the control condition, a phase offset between the two types of stimuli The data were from the participants who saw both TMS-induced replay was introduced, increasing the delay between visual stimulus and TMS to and TMS-entrained replay (n 5 10). For the data including all the 3 secs, while preserving the 6-second presentation rate for each stimulus participants who saw TMS-induced replay, regardless of whether or not type.
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