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Logo of jphysiolThe Journal of Physiology SiteMembershipSubmissionJ Physiol
J Physiol. Jun 1, 2005; 565(Pt 2): 659–665.
Published online Mar 10, 2005. doi:  10.1113/jphysiol.2004.080184
PMCID: PMC1464536

Modulatory effects of low- and high-frequency repetitive transcranial magnetic stimulation on visual cortex of healthy subjects undergoing light deprivation

Abstract

The aim of the present study was to explore further the effects of light deprivation (LD) on visual cortex excitability. Healthy subjects reporting reliable induction of phosphenes by occipital transcranial magnetic stimulation (TMS) underwent 60 min of complete LD. Phosphene threshold (PT) was measured before (T0), after 45 min (T1) and 60 min (T2) of LD, and then every 10 min after light re-exposure until recovery to T0 values. Repetitive TMS (rTMS) (at 1 or 10 Hz) was applied in separate sessions during the last 15 min of LD. PTs significantly decreased after 45 min of LD. rTMS differentially modified the effects of 60 min LD on PTs depending on stimulation frequency. One hertz rTMS did not change the decreasing of PT values as observed in baseline condition, but significantly prolonged the time to recover T0 PT values after light re-exposure. By contrast, 10 Hz rTMS significantly increased PT and the time to recover T0 PT values after light re-exposure was shortened. The results of this study show that the modulatory effects of different rTMS frequencies on visual cortex critically depend on the pre-existing excitability state of inhibitory and facilitatory circuits, and provide novel insights into the neurophysiological changes that take place in the visual cortex following functional visual deafferentation.

Transcranial magnetic stimulation (TMS) has proven to be a safe and valuable tool to investigate cortical excitability (Pascual-Leone et al. 1998). In particular, TMS delivered to the occipital cortex can evoke the perception of flashes or spots of light (phosphenes) in the absence of visual stimuli. The phosphene threshold (PT), i.e. the minimum intensity required to evoke phosphenes, provides a measure of visual cortex excitability in normal subjects and in patients affected by migraine (Afra et al. 1998; Aurora et al. 1998).

Repetitive TMS (rTMS) can modulate cortical excitability beyond the duration of the train itself. Depending on stimulation frequency, rTMS can exert facilitatory or suppressive effects on the stimulated cortex. In healthy subjects, low-frequency rTMS (1 Hz) has been demonstrated to generally induce a lasting decrease in motor (Chen et al. 1997) and visual (Boroojerdi et al. 2000a) cortical excitability, while high-frequency stimulation has been observed to generally increase excitability of the motor cortex (Pascual-Leone et al. 1994) Such rTMS-induced changes in cortical excitability are probably dependent on the pre-existing level of excitability. For example, 1 Hz rTMS delivered to the visual cortex of migraineurs with aura has a paradoxical facilitatory effect (Brighina et al. 2002) (decreased PT that can last for about 30 min). This has been related to the interictal hyperexcitability state of the visual cortex in migraine with aura due to a failure of inhibitory circuits, which are unable to be upregulated by low-frequency TMS. Similar paradoxical effects were found in motor cortex by Ziemann et al. (1998a) who showed that low-frequency (0.1 Hz) rTMS can induce a strong facilitatory influence when delivered in conditions of increased cortical excitability following transient forearm deafferentation.

Deafferentation, i.e. transient or irreversible deprivation of peripheral stimuli, leads to prominent changes in the organization and excitability of the corresponding cortical area (Pettet & Gilbert, 1992; Merzenich & Jenkins, 1993; Ziemann et al. 1998a, b; Werhahn et al. 2002). In blind individuals, visual hallucinations have been interpreted as due to the hyperexcitability of cortical circuits following sensory deprivation (Fernandez et al. 1997; Merabet et al. 2004). Suppression of visual hallucinations in a partially blind subject by means of occipital rTMS, presumably through modulation of cortical excitability, has been recently reported (Merabet et al. 2003). Transient light deprivation (LD) results in physiological and functional changes in the human visual cortex. They consist in a rapid increase of cortical excitability, expressed as a reduction of PT and enhanced activation to incoming visual input on functional magnetic resonance imaging (Boroojerdi et al. 2000b). The aim of the present study was to explore how low- and high-frequency rTMS modulate visual cortical excitability when applied to light-deprived visual cortex, in order to enhance our understanding on the impact of input deprivation on cortical excitability in the adult human brain.

Methods

Subjects

Twelve healthy subjects (eight male, four female; aged 41 ± 10.5 years) were enrolled, but only six with reliable phosphenes participated in the study. None of the subjects had a history of migraine, or any visual abnormalities on neuro-ophthalmological examination. All had normal visual acuity and none were taking any drugs. All were naïve to the experimental purposes. Subjects were instructed on experimental conditions and techniques, and gave their informed consent prior to entering the study, which had been approved by the local ethics committee.

Test–retest reliability of phosphene perception was assessed in a preliminary investigation. Only subjects perceiving phosphenes with high reproducibility participated in the study. The subjects underwent three sessions of complete LD for 60 min on three different days. On one of the days, they received low (1 Hz)-frequency rTMS in the last 15 min of LD. On another day they received high (10 Hz)-frequency rTMS in the last 15 min of LD. On the third day, they were not exposed to any rTMS. The order of these three sessions was randomized and counterbalanced across subjects using a Latin square design. Changes of visual cortex excitability were serially assessed by means of PT.

Magnetic stimulation

PT assessment

All experiments were conducted in a darkened room and the subjects were blindfolded to accomplish total darkness (they did not report any light perception). To avoid nonspecific effect of drowsiness, during LD the examiner monitored subjects' alertness by frequently requesting that the subjects report their sensations. Subjects wore a tight-fitting plastic swimmer's cap marked with a grid of 3 × 3 points, with each point 2 cm apart, centred over Oz (international 10/20 system). A Cadwell high-frequency magnetic stimulator equipped with a 9 cm water-cooled figure-of-eight coil delivering magnetic stimuli with monophasic configuration (pulse width of 200 μs) was used. The coil was placed, with its handle pointing upward, so as to induce a current flowing in a craniocaudal direction. The starting position of the coil was in the midline 2 cm above the inion, and subsequently it was shifted laterally to both sides until the optimum point for induction of phosphenes was found. This point was marked on the swimmer's cap in order to maintain a constant coil position during the experiment. The correct position was monitored by using a small flash light. Paired stimuli with 50 ms interstimulus intervals were used to induce phosphenes. This double pulse stimulation was chosen on the basis of previous experiments (Boroojerdi et al. 2001; Brighina et al. 2002). Magnetic stimulation was started at an intensity of 30% of the maximum stimulator output, and then increased in 2% steps until phosphenes could be elicited, or until a maximum of 100% intensity of stimulation was reached. PT was defined as the minimum intensity required for evoking phosphenes in three of five trials. Average of between six and seven trials were needed for each PT assessment. The intertrial interval was not fixed, but it was not less than 10 s.

rTMS (1 and 10 Hz)

rTMS was applied to the optimal scalp position for induction of phosphenes after 45 min LD, at a PT intensity as assessed before LD. One hertz rTMS (900 stimuli) was delivered continuously for 15 min, and 10 Hz rTMS (900 stimuli) was delivered in trains of 50 stimuli separated by 45 s intervals (15 min).

Phosphene reliability

Only subjects with reliable phosphenes limited to exposure to real TMS were eligible for the study. Phosphenes had to be experienced in the visual field contralateral to the stimulated hemisphere at least 80% of the time upon repeated TMS of the same point. Sham TMS, tilting the coil 90% degree with respect to the scalp, had to fail to induce phosphenes.

Main experiment

Subjects that met the phosphene reliability criteria (four males, two females; mean age: 38 ± 9 years) participated in the experiment. They underwent five experimental sessions with at least 1 day interval between sessions.

Sessions 1–3

Subjects underwent 60 min LD. In session 1, no rTMS was applied (baseline condition). In the other two sessions, rTMS was applied after 45 min LD at low frequency or high frequency.

In all sessions PT was measured before LD (T0), after 45 min (T1) and 60 min of LD (T2), and then every 10 min after light re-exposure until PT came back to baseline value (T0). The time to recover baseline PT (recovery time) was also recorded. Each PT assessment took no more than a few minutes. A time schedule of the overall experiment is summarized in Fig. 1.

Figure 1
Time schedule of the experiments including phosphene threshold (PT) measures and repetitive transcranial magnetic stimulation (rTMS)

Sessions 4–5

Subjects underwent two further control experiments without LD but with exposure to low frequency (session 4) or high-frequency (session 5) rTMS. The order of sessions 4 and 5 was also counterbalanced across subjects. PT was measured just before and after rTMS. Time to recover baseline PT values after rTMS was recorded by measuring PT at 10 min intervals.

The order of the two groups of sessions (1–3; 4–5) was counterbalanced across subjects.

Statistical analysis

Repeated measures ANOVA was used to compare PT values at different times and between different experimental sessions. Intraindividual variability (reproducibility) of PT measures at T0 and T1 in the different sessions was analysed by means of test–retest reliability (Cronbach alpha coefficient).

Recovery times were compared by means of one-way ANOVA.

Results

Phosphene perception and reliability

Eight out of 12 subjects (66%) participating in the study reported phosphenes induced by TMS. Phosphenes met reliability criteria (see above) in six subjects, who went on to complete the experiment.

Main experiment

Experimental sessions 1–3

rTMS was well tolerated and no subjects reported phosphene perception during the trains.

Repeated measures ANOVA with times (T0, T1 and T2) and conditions (baseline, 1 Hz and 10 Hz rTMS) as within subject factors showed a significant interaction main effect (F4,2= 7.70; P < 0.0006). Post-hoc analysis (Duncan) revealed that PT was significantly reduced after 45 min LD (T1versusT0) in sessions 1–3 (baseline: P < 0.001; 1 Hz and 10 Hz rTMS: P < 0.01). Further significant reduction of PT values was observed after 60 min LD (T2versusT1) in the baseline (P < 0.01) and 1 Hz rTMS conditions (P < 0.005); however, 1 Hz rTMS did not change PT level with respect to baseline. Opposite changes were induced by 10 Hz rTMS that significantly increased PT values (T2versusT1: P < 0.01) (Fig. 2A). Figure 2B displays the individual values. Repeated PTs at T0 and T1 showed high test–retest reliability related to the three measurements for each subject (T0: alpha coefficient = 0.966; T1: alpha coefficient = 0.990). Mean time to recover T0 PT values after light re-exposure was about 30 min in the baseline condition. One-way ANOVA for recovery time in the experimental sessions 1–3 (baseline, 1 Hz and 10 Hz rTMS) showed a significant main effect: F2,8= 39.24; P < 0.0001. Duncan post-hoc analysis demonstrated significant opposite effects by the different rTMS frequencies: as compared with the baseline condition, recovery time was increased by 1 Hz (P < 0.01) and decreased by 10 Hz rTMS (P < 0.001) (Fig. 3). Overall PT changes at different times during LD and light re-exposure are displayed in Fig. 4.

Figure 2
PT changes during LD in baseline and after rTMS
Figure 3
PT recovery times after light re-exposure
Figure 4
Overall PT changes during LD and light re-exposure

Control sessions 4–5

In control sessions 4 and 5, repeated measures ANOVA with rTMS frequency (1 Hz and 10 Hz) and times (before and after TMS) as within subject factors showed a significant main effect of the interaction: F2,10= 12.45 P < 0.005. As shown by Duncan post-hoc analysis, PT values were significantly increased by 1 Hz (P < 0.05) and decreased by 10 Hz rTMS (P < 0.05) (Fig. 5). Mean PT recovery time was 30 min for 1 Hz and 15 min for 10 Hz rTMS.

Figure 5
PT changes in control experiments

Discussion

Our results reproduce those of Boroojerdi et al. (2000b) regarding changes in visual cortical excitability with relatively short-lasting light deprivation. Furthermore, we provide novel insights demonstrating that the altered excitability of the visual cortex following LD in normal subjects can be differentially modulated by different rTMS frequencies. The usual effect of 1 Hz rTMS is to decrease cortical excitability while, though to a lesser extent, 10 Hz increases cortical excitability. In our study, opposite modulatory effects of low- and high-frequency rTMS were observed. Following light-deprivation, 1 Hz rTMS sustains the increased sensitivity of visual cortex, prolonging the induced changes in PT. Conversely, 10 Hz frequency rTMS decreases sensitivity of visual cortex, significantly increasing PT values during LD and shortening recovery of baseline excitability soon after light re-exposure.

We hypothesize that the paradoxical effects of rTMS in our study must be related to the LD-induced changes in cortical excitability prior to the exposure to rTMS.

It has been suggested that under normal cicumstances the glutamatergic system is tonically inhibited by GABA (Schroeder et al. 1997). In this condition, low-frequency rTMS generally exerts inhibitory effects, probably upregulating inhibitory circuits (Boroojerdi et al. 2000a), whereas high-frequency rTMS has facilitatory effects likely to be acting on excitatory circuits. The mechanisms underlying plasticity induced by deprivation of sensory inputs are still unclear, but they seem to include the unbalance of cortical inhibition and excitation involving several neurotransmitter circuits such as GABA, NMDA and muscarinic pathways (Ziemann et al. 1998b; Boroojerdi et al. 2001; Philpot et al. 2001). A central role appears to be played by GABA: GABA levels and GAD (glutamic acid decarboxylase, the key enzyme in the synthesis of GABA) are reduced in the deafferentated cortex (Jones, 1993), as are GABAA receptors and synapse efficacy (Kilman et al. 2002). Additionally, synaptic plasticity in the visual cortex requires activation of NMDA receptors and is favoured by reduced GABAergic inhibition (Artola & Singer, 1987).

Pharmacological evidence supports the hypothesis of GABA involvement, together with other neurotransmitters, in plastic changes induced by functional deafferentation in humans. In particular, drugs which enhance GABA function inhibit the effects of sensory deprivation in visual (Boroojerdi et al. 2001) and motor cortex (Ziemann et al. 1998b), while blockade of GABA receptors, enhances plastic changes in deafferentated cortex (Jacobs & Donoghue, 1991; Chowdhury & Rasmusson, 2002, 2003).

Taken together, these findings suggest that the involvement of GABAergic inhibition, NMDA receptor activation and cholinergic transmission are operating in rapid, experience-dependent plasticity in the human visual cortex. These effects are interpreted as secondary to the unmasking of pre-existent excitatory connections, which normally are supposed to be blocked by local inhibitory circuits.

When a failure of inhibitory circuits occurs, i.e. after functional deafferentation, the slight depolarization of postsynaptic membrane, removing Mg2+ ions from NMDA receptors, is able to prime the LTP phenomenon. In this condition, the loss of balance between facilitatory and inhibitory circuits might invert the stimulation frequency-dependent effects of rTMS on cortical excitability. In particular, the functional suppression of inhibitory circuits in the light-deprived visual cortex could allow a facilitatory effect even when low-frequency rTMS is applied. This is in agreement with the effects of rTMS on deafferentated motor cortex (Ziemann et al. 1998a), and seems to further support the hypothesis that the TMS findings in migraineurs with aura may be due to the reduction in interictal inhibition in their visual cortex (Brighina et al. 2002). More recently, Siebner et al. (2004) demonstrated that preconditioning corticospinal excitability with transcranial direct current stimulation over the M1 can modulate the direction of plasticity induced by subsequent administration of 1 Hz rTMS. The authors concluded that the plastic changes induced by 1 Hz rTMS critically depend on the functional state of the stimulated cortex before and at the time of rTMS conditioning.

In the present study, PT values were significantly decreased after 60 min of LD and were not modified by 1 Hz rTMS. This stimulation frequency, however, induced a significant prolongation of the cortical hyperexcitability state induced by the LD as indexed by the longer time needed to recover the baseline PT after light re-exposure. This effect is interpreted as an rTMS-induced potentiation of the impact of LD on cortical excitability and may be due to a strengthening of the excitatory synapses. However, further suppression of inhibitory circuits cannot be excluded. The ability of high-frequency rTMS to restore normal excitability of the visual cortex following LD seems harder to explain. In the setting of LD-induced enhanced excitability, high-frequency rTMS seems to act preferentially by upregulating inhibition. In this respect, it seems worth noting that the effects of 10 Hz rTMS during LD are similar to those induced by light re-exposure. In both conditions, a rapid recovery of GABA function could play a role in restoring PT baseline levels.

The effect of high-frequency rTMS on the silent period (SP), a measure of intracortical inhibition (Berardelli et al. 1999), also supports upregulation of inhibitory circuits. During muscle contraction (a condition of increased motor cortex excitability), high-frequency rTMS potentiates inhibitory circuits, increasing SP duration. A possible explanation is that in a condition of hyperexcitability, when excitatory circuits reach a ceiling of activation and cannot be further upregulated, high-frequency rTMS may paradoxically potentiate inhibitory circuits. Other suggestions of upregulation of inhibitory circuits by high-frequency rTMS in pathological conditions might come from studies in Parkinson's disease (Siebner et al. 2000; Gilio et al. 2002), where a reduced cortical inhibition has been repeatedly reported, along with a reduced cortical activation (Cantello et al. 2002). Here, SP duration is increased during (Gilio et al. 2002) or after (Siebner et al. 2000) 5 Hz rTMS trains arguing in favour of a facilitatory effect of high-frequency rTMS also on intracortical inhibition.

The relationship between TMS-evoked phosphenes and visual function is not fully understood. Indeed we do not know exactly which neuronal elements or mechanisms are involved in phosphene perception. Pascual-Leone & Walsh (2001) suggested that feedback–feedforward loops between secondary and primary visual areas have to be sufficiently activated to generate phosphene perception.

However, we know that after low-frequency rTMS of the occipital cortex, visual evoked potentials are modulated (Thut et al. 2003; Schutter & van Honk, 2003) in a manner similar to the changes induced in PT (Boroojerdi et al. 2000a). Therefore, even though insufficiently studied, the modulatory effects of rTMS on visual cortex excitability may follow similar rules than those that apply to motor cortex rTMS.

We applied rTMS at PT intensity as assessed before LD. Even if lower intensity is needed to elicit phosphenes with paired stimuli (as used for PT assessment) compared to single pulse, PT decreased after 45 min LD. Therefore it cannot be excluded that rTMS was at threshold or slightly suprathreshold to elicit phosphenes. However, subjects did not report any phosphene perception during rTMS, as could be expected in particular with 10 Hz frequency. The lack of the effect might depend on the rapid, paradoxical increasing of PT by high-frequency train during LD, likely to be dependent on upregulation of inhibitory circuits.

In any case, in our experiment, comparison of control sessions 4 and 5 with sessions 2 and 3 demonstrates that the same rTMS parameters can induce significantly different modulations in the face of functional deafferentation of the targeted cortical site of stimulation.

The modulatory effect of different frequencies of rTMS may be facilitatory or inhibitory depending on interindividual variability, duration, intervals and intensity of train stimulation (Maeda et al. 2000a, b). Therefore, one could make the point that the observed facilitatory or inhibitory effects may be attributable to the interindividual variability or to the spurious variation in other parameters (e.g. duration, threshold intensity) rather than to a more fundamental mechanism. We believe that this is highly unlikely since each subject underwent all experimental sessions, and rTMS parameters (threshold intensity and duration of the trains) were kept constant across rTMS frequencies for each subject. In addition, it is worth noting that in our study subjects also exhibited a low intraindividual variability as documented by the very consistent effect of LD on PT across repeated sessions.

Nevertheless, it should be noted that we studied only half of the normal subjects screened, and the selected subjects, with highly reliable phosphenes induced by TMS, may not be representative of a larger population. However, to our knowledge, no peculiar physiological properties of the visual cortex distinguish subjects with reliable phosphenes from those who do not perceive phosphenes induced by TMS.

In conclusion, the present study suggests that the lasting effects of rTMS trains depend on the functional state of cortical inhibitory and facilitatory circuits. Physiological mechanisms underlying rTMS modulation of visual cortex remain at present purely speculative, and direct measures in suitable animal model or with combined application of rTMS and other brain imaging methods are needed. However, it seems that findings in motor cortex parallel our results in the visual cortex, and suggest a fundamental property that may not be limited to rTMS, but one which is applicable to other forms of neuromodulation across brain regions.

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