| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
1 Department of Neurophysiology, Ruhr-University Bochum, 44780 Bochum, Germany
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionReferences |
|---|
(Received 3 March 2005;
accepted after revision 19 May 2005;
first published online 26 May 2005)
Corresponding author K. Funke: Department of Neurophysiology, Medical Faculty, Ruhr-University Bochum, 44780 Bochum, Germany. Email: funke{at}neurop.ruhr-uni-bochum.de
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
A clear SICI is present only if CS is low (60–80% of TS). Increasing the CS strength to that of TS, or combining a supra-threshold CS with a slightly subthreshold TS, also leads to ICF at short ISIs (Ziemann et al. 1998; Di Lazzaro et al. 1999b; Ilic et al. 2002). Based on the assumption that TMS preferentially stimulates horizontally orientated intracortical neuronal elements and related to the finding that ICF generally needs a stronger CS to occur than SICI (> 80%, Kujirai et al. 1993; Ziemann et al. 1996; Chen et al. 1998; Awiszus et al. 1999), Ilic et al. (2002) proposed a model, composed of a short low-threshold inhibitory pathway and a high-threshold polysynaptic excitatory intracortical pathway.
Recently, we have shown that it is possible to record cortical single-unit spike activity at the centre peak of the magnetic field induced by a figure-of-8 coil (Moliadze et al. 2003). In a first attempt, we analysed the interaction of single TMS pulses with visually evoked responses in the primary visual cortex of anaesthetized cats by varying the strength of TMS and the interval between magnetic and visual stimulation. In the present study, we systematically tested the effect of pairing a conditioning stimulus of different strength at different intervals with a test stimulus which either facilitates or inhibits visually evoked activity. In this way, we attempted to obtain a better insight into the cellular and network activities elicited by distinct TMS protocols which could be used in future in vivo studies concerned with the effect of TMS on sensory processing.
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
All experimental procedures were permitted under the local government guidelines for animal welfare (No. 50.8735/81.6), and in addition conformed to legal requirements in the EU, UK and the US.
Surgical and electrophysiological procedures were in principle the same as in the previous study (Moliadze et al. 2003). In brief, all surgical procedures allowing the maintenance of the experimental cats in terms of artificial ventilation, relaxation and nutrition during the 5 day recording sessions were performed under deep anaesthesia with a combination of ketamine (20 mg kg–1 I.M., Ketanest, Parke-Davies, Germany) and xylazine (2 mg kg–1 I.M., Rompun, Bayer, Germany). All incisions and pressure points were also locally anaesthetized by xylocaine (2%, Astra Chemicals, Germany). The level of anaesthesia before and during surgery was tested with the toe-pinch and pinna reflex. Absence of motor reactions and stable blood pressure were taken as signs of sufficient anaesthesia. The relaxation and hydration of cats was achieved by continuous infusion of alcuronium chloride (0.15 mg kg–1 h–1, Alloferin 10, Hoffmann-La Roche, Germany) in 1% glucose-Ringer solution through the femoral artery at a rate of 6 ml h–1. The degree of neuromuscular blockade sufficient to avoid active respiration by the animal was assessed by monitoring the time course of expiratory CO2 change during artificial respiration (Datex Normocap 200, Hoyer, Bremen, Germany). The femoral catheter also allowed the measurement of heart rate and arterial blood pressure. Rectal body temperature was measured and kept at about 38.5°C by the aid of a heat blanket. Continuous anaesthesia during recording sessions was guaranteed by artificial respiration with N2O–O2 (70%: 30%) and halothane (0.6–2.5% Fluothane, ICI-Pharma, Germany) through a catheter introduced into the trachea. Adequate ventilation and anaesthesia of the animal was assured via analysis of the spectral composition of the EEG (presence of alpha and delta waves) and via the level and time course of blood pressure, heart rate and end-expiratory CO2. Body temperature, blood pressure, heart rate, end-expiratory CO2, and the inspiratory levels of O2 and N2O were continuously measured and stored by a supervision monitor. For each of these parameters, upper and lower limits could be set for absolute values, rate of change and for the forecast of a critical state by trend analysis. The crossing of one of these limits triggered an alarm in the laboratory which enabled fast-as-possible emergency actions around the clock. EEG recordings were also monitored and stored on hard disk simultaneously with the single-unit recordings.
The optics were corrected for a viewing distance of 56 cm with contact lenses of 5–7D. Atropine sulphate (1%, Atropin-Pos, Ursapharm, Germany) and phenylephrine hydrochloride (5%, Neosynephrin-Pos, Ursapharm, Germany) were applied topically for mydriasis and retraction of the nictitating membranes. Isoptomax (Alcon Pharma, Germany) was topically applied to the cornea to prevent infections. Craniotomies provided access to area 17 of the right hemisphere for single-unit recording, and to area 18 of the left hemisphere for epidural EEG recording via a 0.5 mm silver ball electrode. Recordings were continued as long as the animal could be maintained in a physiological state, with blood pressure above 80 mmHg, end-expiratory CO2 between 3.8 and 5.5%, body temperature around 38.5°C and the EEG showing a normal pattern with episodic changes in spectral composition due to brainstem activity. At the end of each experiment, the animal was deeply anaesthetized by maximal halothane concentration (4 vol.%) and perfused with cold (4°C) Ringer solution followed by 4% paraformaldehyde, to enable further histological studies on the brain tissue.
Recordings and visual stimulation
Electrophysiological procedures and visual stimulation were also the same as in the previous study. Extracellular recordings of single-unit activity were made within area 17 at the top of the gyrus, corresponding to visual field positions around 5 deg lower and 5 deg lateral to area centralis. Visual stimulation of the receptive fields of individual neurones was achieved by moving an optimally sized and orientated (preferred orientation) bright bar, presented monocularly, forth and back across the receptive field within 3 s. Visual stimuli were generated by a PC-based visual stimulator (‘Leonardo’, Lohmann Research Equipment, Germany) and presented on a 21 inch CRT monitor at a refresh rate of 100 Hz. For further details, see Methods section of the previous paper (Moliadze et al. 2003).
TMS protocols
Paired magnetic pulses were generated by two MagStim 200 and a BiStim module (The Magstim Company, Whitland, Dyfed, UK) and applied to the occipital cortex of cats via a figure-of-eight coil (2 mm x 70 mm in one plane, monophasic pulse, The Magstim Company). As one difference to the previous study we tested a special version of the 2 mm x 70 mm figure-of-8 coil in two of the four cat experiments. The coil built by the MagStim Company on our request is identical to the conventional 2 mm x 70 mm coil except for a central guiding tube of 5 mm in diameter at the junction of the two coils to enable a microelectrode to be lowered through the coil into the brain at the centre peak of the magnetic field. When using the conventional figure-of-8 coil, the electrode was lowered to the cortex by moving it tangentially to the lower surface of the coil with the coil tilted by 45 deg towards the neck of the cat. The coil was centred above area 17/18 of the right hemisphere with the handle pointing to the left hemisphere, thereby inducing a mediolateral current in the dorsally exposed area 17/18 of the right hemisphere. We could not find any significant differences in the threshold for inducing excitatory or inhibitory effects on visually evoked activity for opposite current directions.
Prior to the paired pulse protocols, for each new recording site we determined the strength of the test stimulus (TS) needed to achieve a reliable change in visually evoked activity. Therefore, the TMS pulse was delivered shortly before (20–40 ms) the onset of a visual response (see Fig. 1A), so that the maximum visually evoked activity was close to 100 ms after TMS, an episode that was found in the previous study (Moliadze et al. 2003) to be most likely to lead to facilitation of visual (and spontaneous) activity, but also inhibition in some cases. As in the former study, trials with three different stimulus conditions were interleaved and each repeated 20 times: one trial with visual stimulation only (moving bar), one trial with combined visual and magnetic stimulation, and one trial with TMS only. Different strengths of TMS were tested and the stimulation strength changing the rate of activity by about 10–30% in two sets of recordings using the same stimulation protocol was taken as the test stimulus (TS) strength for ppTMS. TS strength was within 30–50% of maximal stimulator output. The TS had a facilitatory effect on visual activity in about two-thirds (n = 26) of the 42 cells analysed; in the remainder it was suppressive.
|
Data analysis
Quantitative analysis of the ppTMS effect was carried out in the following way: first, the effect of the TS itself was checked by subtracting the activity with visual stimulation only from the activity obtained with combined visual and magnetic stimulation, yielding both the amount and the polarity of change (facilitation or suppression) with TS. Next, the additional effect of the CS was determined – as shown in Fig. 1B
– by subtracting the activity evoked by TS + visual stimulation (curve 1) from the activity evoked with ppTMS + visual stimulation (curve 2) resulting in curve 3. This additional change in visual activity caused by the CS (ppTMS) was set in relation to the effect of TS only (e.g. see Fig. 2). In addition, we checked whether the ppTMS effect is the linear sum of the individual effects of CS and TS by subtracting the sum of the changes in visual activity obtained with CS and TS from the change in visual activity achieved with ppTMS (Dpp
=
vis,ppTMS
– (vis,CS
+
vis,TS)). Since the effects of TMS in the cortical network are likely to change with the delay after the test pulse, e.g. by switching between facilitation and suppression (Moliadze et al. 2003), we calculated mean rate of spike activity in three different time windows following TMS: 30–100 ms, 100–200 ms and 200–500 ms (indicated in Fig. 1B). Time 0–30 ms after onset of TMS was excluded from the analysis because of possible contamination by the TMS artefact. Statistical significance (P < 0.05) of mean changes in activity achieved with ppTMS as compared to TS were determined with Student's paired t test. The paired version of the test was chosen because ppTMS data are coupled to TS control data via the rate of visually evoked activity which varies from cell to cell. Accordingly, the error bars given in Fig. 4 refer to the standard deviation of differences between ppTMS and TS effects.
|
|
|
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
The experimental conditions for ppTMS in our study are somewhat different from those in human motor cortex. In the motor system, TS (or a single TMS pulse in general) always results in increased motor output, the efferent activity is artificially induced and is the result of the concerted and almost synchronous action of many hundreds or thousands of pyramidal cells and the amplitude of the motor response can be more precisely adjusted by TMS strength. The situation is different in our approach: here, visual activity evoked by a moving bright bar interacts with an artificially evoked volley of activity within the cortical network. Moreover, we do not measure the summed output activity of cortical columns but a single cell's activity within the column. Accordingly, we are confronted with highly variable activities, both in response to visual stimulation and as a result of TMS (see also Moliadze et al. 2003).
In our first attempt, we therefore analysed the relationship between ppTMS and TS effects on visually evoked activity at the single-cell level by plotting the additional change in visual activity resulting from the combination of CS with TS (ppTMS) versus the change in activity caused by the TS alone. Thus, activity with ppTMS minus the activity with TS is plotted on the ordinate of the diagrams in Figs 2 and 3A, and activity with TS minus sole visual activity (without TMS) is plotted along the abscissa. This was done separately for each of the five CS strength ranges (15–30%, 40–50%, 60–90%, 100% and 110–130%) and the 12 ISIs tested, resulting in 60 scatter plots. In Fig. 2, plots are shown only for the CS strength range 60–90%, but for each of the 12 ISIs. The distribution of data points in these diagrams indicates a positive correlation between ppTMS and TS effects: the stronger the TS effect, the stronger also the effect of adding the CS, both for facilitation and for suppression of visual activity by the TS. The distribution of data points did not vary much with changing ISI and this also holds for the other four ranges of CS strength tested. Therefore in Fig. 3A, five different CS strength ranges are compared for only one interstimulus interval (ISI 3 ms). A comparison of the five diagrams in Fig. 3A clearly shows that the correlation between ppTMS effect and TS effect depends on CS strength: for the lowest range of CS (15–30%) the correlation is negative, indicating that the conditioning stimulus had weakened the TS effect, in both facilitation and suppression. With increasing CS strength, the correlation between ppTMS and TS effect became positive and facilitation of the TS effect by the CS increased up to saturation at CS 100–130%. The correlation between the effects of ppTMS and TS was quantitatively analysed by calculating the slope of the regression lines and Pearson's correlation coefficients. For each stimulus condition these two values are given in the diagrams of Fig. 3B by plotting slope and correlation coefficient versus ISI for each of the five CS ranges. The slope of the regression line continuously increases with increasing CS strength but also saturates around 100%. The effect is relatively independent of the ISI; only for high CS strengths (100% and 110–130%) is the slope clearly higher with short ISIs (2–6 ms). Pearson's correlation coefficients are less dependent on the ISI for all cases of CS strength and reach statistical significance in all cases except for the CS range 40–50% for which the slope of the regression lines was very low (about 0.1, 
< 0.01 for all ISIs in CS range 15–30%, < 0.001 for all ISIs in CS ranges 60–90%, 100% and 110–130%, < 0.05 only for ISI 4 ms in the CS range 40–50%, with values taken from statistic reference tables).
|
To test whether the changes in visual activity achieved with ppTMS resemble the (linear) sum of the individual effects of the two stimuli (CS + TS), we carried out the following calculation:
|
|
|
|
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
The results of this study reveal that a conditioning stimulus (CS) applied at different intensity and time prior to a supra-threshold TMS test stimulus (TS) modifies the effect of the TS on visually evoked activity in a distinct way. Contrary to the effects of ppTMS described for the human motor cortex, we found no dependence of the ppTMS effect on interstimulus interval (ISI). A moderately subthreshold CS (range 60–90% of TS) caused, on average, an augmentation of the TS effect: either an increased facilitation of visual activity by the TS or strengthened suppression of visual activity if the TS by itself had a suppressive effect. The ppTMS effect, however, varied with the strength of the CS. A facilitation of the TS effect by the CS was found only for CS strength 60–130%. Weaker CS (15–30%) resulted in an ISI-independent reduction of the TS effect, e.g. facilitation of visual activity by the TS was weakened. Furthermore, the ppTMS effect was not equal to the algebraic sum of the individual CS and TS effects. It was lower than the sum of CS and TS effects for low CS strength but stronger for peri-threshold CS.
One aspect of our results was somewhat surprising and needs further discussion: a strengthening of the suppression of visual activity by the TS appeared with CS strength ranges 40–50%, 60–90% and 110–130%, but not with a CS of 100%. Why do we see no change in the amount of inhibition when the conditioning pulse is of the same strength as the test stimulus? This phenomenon could be explained as follows: if two identical supra-threshold stimuli are applied one after the other, the same population of neurones will be stimulated but the effect will be different at excitatory and inhibitory synapses. In the likely case of shunting inhibition caused by activation of GABAA receptors, the first inhibitory volley may maximally suppress nearby excitatory postsynaptic potentials and a second volley acting at the same synapse may not add much effect (no temporal summation). A different population of neurones (axons) will be activated if CS and TS differ in strength, leading to a spatially different pattern of inhibition, and additional excitatory inputs may be depressed. On the contrary, excitatory postsynaptic potentials more likely show temporal summation – in part due to NMDA-mediated potentials – and will sum up even when the same inputs are activated by identical stimuli.
Although these effects of ppTMS on single-unit activity in cat visual cortex are different from those observed for motor activity evoked in human M1 with ppTMS, our findings are in accordance with the model proposed by Ilic et al. (2002), which is composed of a low-threshold inhibitory pathway and a high-threshold excitatory pathway. A weak CS might have preferentially activated or pre-depolarized the inhibitory network which might then be potentiated by the following TS prior to the activation of excitatory connections. With increasing CS strength more and more excitatory neurones might be pre-activated. Although most studies using ppTMS were concerned with the human motor system, it is difficult to compare the findings obtained in these studies with those found in cat visual cortex. In human motor cortex, intracortical inhibitory and excitatory activity elicited first by the CS and then by the TS interacts at the corticospinal output neurones and determines the amount of population activity. In the visual cortex, this population activity interacts with afferent sensory input which by itself activates excitatory and inhibitory network activity. The driving effect of the afferent input might have shifted the ratio of excitatory and inhibitory network activity towards excitation. Indeed, we found in this and the previous study (Moliadze et al. 2003) that the combination of TMS with visually evoked activity causes a 2–3 times stronger facilitation of activity than when applied during spontaneous activity, indicating that the TMS pulse mainly pushed subthreshold, visually pre-activated inputs. Thus, the effect of ppTMS in the visual cortex during visual stimulation seems to be more comparable with results obtained in human motor cortex during voluntary contraction of target muscles. Indeed, short interval cortical inhibition (SICI) is reduced during a voluntary contraction (Ridding et al. 1995; Fisher et al. 2002; Roshan et al. 2003), or replaced by cortical facilitation (ICF) (Di Lazzaro et al. 1998; Ilic et al. 2002).
One problem was that we could not analyse the first 30 ms after TMS because of the huge stimulus artefact. With the ‘Cyberamp 380’ amplifier (Axon Instruments, CA, USA) we could reduce but not eliminate the TMS artefact and even an amplifier equipped with a circuit for blanking out artefacts (CED 1902/4, Cambridge Electronic Design, UK) did not work sufficiently for single-unit recordings. Thus, we could not analyse the direct effects of a TMS pulse on the activity of the recorded cells but the intracortically evoked trans-synaptic effects thought to dominate with TMS should last for up to 100 ms due to the duration of EPSPs and interactions of polysynaptic, repetitive inputs.
On the other hand, our data are in accordance with data obtained from human visual cortex by Ray et al. (1998) and Dambeck et al. (2003). Neither reported increased phosphene thresholds with paired-pulse TMS at short ISIs (1–5 ms). The threshold was either stable up to 100 ms ISI and then increased (Ray et al. 1998), or a general facilitation of phosphene sensation was observed at all ISIs when using a CS of 90% (Dambeck et al. 2003). Paired-pulse TMS applied to human parietal cortex revealed an ISI-dependent effect somewhat similar to motor cortex (Oliveri et al. 2000): the threshold for detecting a weak electrical cutaneous stimulus was increased with short ISIs of 1 or 3 ms, but decreased for an interval of 5 ms compared to the situation with a single TS. However, the TS itself caused an increase in detection threshold, and detection with ppTMS of 5 ms ISI was close to control levels without TMS. This result is similar to our finding of increased suppression by the TS with a slightly subthreshold CS.
Possible cellular mechanisms
What could be the cellular mechanisms that cause the paired-pulse facilitation or suppression of sensory activity? As already mentioned above, a stimulus-dependent ratio of excitatory and inhibitory synapses might be activated. However, the monosynaptic or heterosynaptic activation of purely excitatory inputs can also explain these effects. Using in vivo intracellular recordings in anaesthetized cats, Fuentealba et al. (2004) tested the effects of paired-pulse electrical stimulation of thalamic and cortical inputs to neocortical neurones. Heterosynaptic pairing of cortical and thalamic inputs primarily induced a depression of the second response in a pair, while monosynaptic pairing (either cortical or thalamic inputs) also caused facilitation of the conditioned second input, first of all with thalamic pairing. One may speculate that in our study a weak TMS CS might have primarily activated cortical inputs which resulted in a depression of subsequent thalamic inputs while stronger CS caused facilitation by also stimulating the thalamocortical axons in the white matter. The effective time window of paired-pulse interactions in the study of Fuentealba et al. (2004) is sufficiently long to fit not only to the pairing of TMS but also to the interaction with the visual input. A maximum effect was found with an ISI of about 10–20 ms, which is close to the maximum at 3–4 ms in our study. ISIs shorter than 5 ms were not investigated by Fuentealba et al. (2004).
Another possible cellular reason for depression and even facilitation of the second response in a paired-pulse stimulus protocol could be the refractoriness of the neuronal membrane. By applying the paired-pulse electrical stimulation protocol to peripheral nerves Chan et al. (2002) could demonstrate that the evoked volley of axonal population activity showed an ISI dependence very similar to SICI and ICF of human motor cortex: a subthreshold CS applied 1–4 ms prior to the TS reduced the amplitude of the axonal response while it was enhanced with ISIs of 5–20 ms. Chan concluded that the time course of suppression fits the temporal aspects of the relative refractory state of the axonal membrane while response facilitation is due to a following increase in the open probability of voltage-sensitive sodium channels induced by the leading hyperpolarization (rebound). By applying the same stimulus protocol to the H-reflex test, they could further demonstrate that these changes in excitability are even transmitted across an intervening excitatory synapse. Thus, changes in excitability of the axonal membranes may contribute to the effect of conditioning stimuli even for ISIs longer than 1 ms for which synaptic explanations have been postulated.
Effects of anaesthesia
We have to consider further that activity evoked by stimulating the brain depends on the actual state of the neuronal network which can be affected intrinsically by the brainstem arousal systems, and also by pathological states. For example, stimulus protocols usually inducing the suppression of cortical excitability (1 Hz repetitive TMS) do the opposite during migraine states (Fierro et al. 2003). General anaesthetics affect the state of the cortical network by a spectrum of different actions (for review see Rudolph & Antkowiak, 2004). One prominent action is the potentiation of the GABAA receptor, especially with barbiturates, etomidate and propofol. Although to a somewhat lesser extent, the cortical site of action of the volatile anaesthetic halothane also seems to be the GABAA receptor (Hentschke et al. 2005), while in the spinal cord, potentiation of glycinergic actions by halothane supports immobility and the blockade of transmission of nociceptive information (Rudolph & Antkowiak, 2004). The combined cortical and spinal action of halothane might explain the strongly reduced likelihood of evoking motor potentials by electrically stimulating the human motor cortex (Kawaguchi et al. 1996). At the concentration we used in combination with nitrous oxide, halothane has been found to reduce spontaneous activity in vivo by about 50% (Hentschke et al. 2005). Thalamocortical processing of sensory signals may also be reduced but typical patterns of excitatory and inhibitory responses are still preserved during halothane–nitrous oxide anaesthesia, a reason for choosing this kind of anaesthesia when studying sensory processing in higher mammals. In this and the previous study (Moliadze et al. 2003), we could show that a single TMS pulse can induce both facilitatory and suppressive volleys lasting up to one second or even more, indicating that synaptic transmission is only moderately affected by nitrous oxide–halothane anaesthesia. Nevertheless, the balance between excitatory and inhibitory actions in the cortex may be shifted towards a dominance of inhibitory actions.
Conclusions
In summary, our results obtained with single-unit recordings during ppTMS of cat visual cortex reveal that the outcome of ppTMS primarily depends on the strength of the conditioning stimulus but less on the interval between conditioning (CS) and test stimulus (TS). At moderately subthreshold and suprathreshold strength (60–130%), CS amplifies the TS effect: facilitation of subsequent visual activity is improved but also the suppression of visual activity induced by the TS is slightly strengthened. A weak CS (15–30%), however, diminishes facilitation of visual activity by the TS. Our findings are in agreement with the idea that inhibitory connections may have a lower activation threshold than excitatory connections. A weak CS would thus pre-activate a relatively higher number of inhibitory synapses as compared to a stronger CS, leading to a weakening of the following TS, while relatively more and more excitatory inputs are activated with increasing CS strength. Our data are also in accordance with the few data obtained in human visual cortex, but more detailed studies of the ppTMS effect on human visual perception are needed to further elucidate the specific nature of the visual system with respect to TMS.
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Chan
JHL, Lin
CSY, Pierrot-Deseilligny
E
&
Burke
D (2002). Excitability changes in human peripheral nerve axons in a paradigm mimicking paired-pulse transcranial magnetic stimulation. J Physiol
542, 951–961.
Chen
R, Tam
A, Butefisch
C, Corwell
B, Ziemann
U, Rothwell
JC
&
Cohen
LG (1998). Intracortical inhibition and facilitation in different representations of the human motor cortex. J Neurophysiol
80, 2870–2881.
Dambeck N, Stock K, Weidemann J, Meister IG, Foltys H & Boroojerdi B (2003). Investigating phosphene elicitation with the paired-pulse paradigm. Proceedings of the 29th Neurobiology Conference and 5th Conference of the German Neuroscience Society, S528.
Di Lazzaro V, Oliviero A, Profice P, Insola A, Mazzone P, Tonali P & Rothwell JC (1999a). Direct recordings of descending volleys after transcranial magnetic and electrical motor cortex stimulation in conscious humans. Electroencephalogr Clin Neurophysiol Suppl 51, 120–126.[Medline]
Di Lazzaro
V, Restuccia
D, Olivero
A, Profice
P, Ferrara
L, Insola
A, Mazzone
P, Tonali
P
&
Rothwell
JC (1998). Effects of voluntary contraction on descending volleys evoked by transcranial magnetic stimulation in conscious humans. J Physiol
508, 625–633.
Di Lazzaro V, Rothwell JC, Oliviero A, Profice P, Insola A, Massone P & Tonali P (1999b). Intracortical origin of the short latency facilitation produced by pairs of threshold magnetic stimuli applied to human motor cortex. Exp Brain Res 129, 494–499.[CrossRef][Medline]
Fierro
B, Ricci
R, Piazza
A, Scalia
S, Giglia
G, Vitello
G
&
Brighina
F (2003). 1 Hz rTMS enhances extrastriate cortex activity in migraine – Evidence of a reduced inhibition?
Neurology
61, 1446–1448.
Fisher R, Nakamura Y, Bestmann S, Rothwell JC & Bostock H (2002). Two phases of intracortical inhibition explored by transcranial magnetic threshold tracking. Exp Brain Res 143, 240–248.[CrossRef][Medline]
Fuentealba
P, Crochet
S, Timofeev
I
&
Steriade
M (2004). Synaptic interactions between thalamic and cortical inputs onto cortical neurons in vivo. J Neurophysiol
91, 1990–1998.
Hentschke H, Schwarz C & Antkowiak B (2005). Neocortex is the major target of sedative concentrations of volatile anaesthetics: strong depression of firing rates and increase of GABAA receptor-mediated inhibition. Eur J Neurosci 21, 93–102.[CrossRef][Medline]
Ilic
TV, Meintzschel
F, Cleff
U, Ruge
D, Kessler
KR
&
Ziemann
U (2002). Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity. J Physiol
545, 153–167.
Kawaguchi M, Shimizu K, Furuya H, Sakamoto T, Ohnishi H & Karasawa J (1996). Effects of isoflurane on motor-evoked potentials induced by direct electrical stimulation of the exposed motor cortex with single, double and triple stimuli in rats. Anaesthesiology 85, 1176–1183.[CrossRef][Medline]
Kujirai
T, Caramia
MD, Rothwell
JC, Day
BL, Thompson
PD, Ferbert
A, Wroe
S, Asselman
P
&
Marsden
CD (1993). Cortico-cortical inhibition in human motor cortex. J Physiol
471, 501–519.
Moliadze
V, Zhao
Y, Eysel
U
&
Funke
K (2003). Effect of transcranial magnetic stimulation on single-unit activity in the cat primary visual cortex. J Physiol
553, 665–679.
Nakamura H, Kitagawa H, Kawaguchi Y & Tsuji I (1997). Intracortical facilitation and inhibition after transcranial magnetic stimulation in conscious humans. J Physiol 498, 817–823.[Medline]
Oliveri
M, Caltagirone
C, Filippi
MM, Traversa
R, Cicinelli
P, Pasqualetti
P
&
Rossini
PM (2000). Paired transcranial magnetic stimulation protocols reveal a pattern of inhibition and facilitation in the human parietal cortex. J Physiol
529, 461–468.
Ray PG, Meador KJ, Epstein CM, Loring DW & Day LJ (1998). Magnetic stimulation of visual cortex: factors influencing the perception of phosphenes. J Clin Neurophysiol 15, 351–357.[CrossRef][Medline]
Ridding MC, Taylor JL & Rothwell JC (1995). The effect of voluntary contraction on cortico-cortical inhibition in human motor cortex. J Physiol 487, 541–548.[Medline]
Roshan L, Paradiso GO & Chen R (2003). Two phases of short-interval intracortical inhibition. Exp Brain Res 151, 330–337.[CrossRef][Medline]
Rudolph U & Antkowiak B (2004). Molecular and neuronal substrates for general anaesthetics. Nat Rev Neurosci 5, 709–720.[CrossRef][Medline]
Sanger
TD, Garg
RR
&
Chen
R (2001). Interactions between two different inhibitory systems in the human motor cortex. J Physiol
530, 307–317.
Tokimura H, Ridding MC, Tokimura Y, Amassian VE & Rothwell JC (1996). Short latency facilitation between pairs of threshold magnetic stimuli applied to human motor cortex. Electroencephalogr Clin Neurophysiol 101, 263–272.[CrossRef][Medline]
Ziemann U, Rothwell JC & Ridding MC (1996). Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol 496, 873–881.[Medline]
Ziemann
U, Tergau
F, Wassermann
EM, Wisher
S, Hilderbandt
J
&
Paulus
W (1998). Demonstration of facilitatory I wave interaction in the human motor cortex by paired transcranial magnetic stimulation. J Physiol
511, 181–190.
|
Acknowledgements |
|---|
This article has been cited by other articles:
|
|
 |
|
  C. de Labra, C. Rivadulla, K. Grieve, J. Marino, N. Espinosa, and J. Cudeiro Changes in Visual Responses in the Feline dLGN: Selective Thalamic Suppression Induced by Transcranial Magnetic Stimulation of V1 Cereb Cortex, June 1, 2007; 17(6): 1376 - 1385. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Aydin-Abidin, V. Moliadze, U. T. Eysel, and K. Funke Effects of repetitive TMS on visually evoked potentials and EEG in the anaesthetized cat: dependence on stimulus frequency and train duration J. Physiol., July 15, 2006; 574(2): 443 - 455. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
