Journal of Physiology

Training involving repetitive movements against a large

resistance is known to enhance muscular strength, and the

intramuscular adaptations that occur in response to this

'resistance training' have been well described (for reviews

see Timson, 1990; Abernethy et al. 1994; Baldwin & Haddad,

2001).

Although it has long been suspected that resistance

training is also accompanied by adaptations in the CNS

that play an important role in the development of strength,

the precise nature of the neural responses to resistance

training is unknown (e.g. Sale, 1988; Moritani, 1993; Enoka,

1997; Carroll et al. 2001a; Gandevia, 2001). Since it is now

well established that motor learning is accompanied by

changes in the functional organisation of the cerebral

cortex (e.g. Martin & Morris, 2001), it seems reasonable to

presume that resistance training may induce changes in

the organisation of the cortex. However, it has recently

been shown that the repetitive execution of a simple

movement does not induce substantial adaptation in the

motor cortex in monkeys (Plautz et al. 2000). Furthermore,

Remple et al. (2001) reported that repetition of a difficult

task that requires a new movement technique to be learned

and refined induces a similar degree of cortical adaptation,

regardless of whether the training movements are performed

against high or low resistance in rats. These studies suggest

that the systematic repetition of simple movements with

low force and velocity requirements does not cause

substantial, long-lasting (i.e. beyond a few hours after

exercise) cortical adaptation, and that increasing the force

required to execute a new task during skill learning does

not markedly affect the degree of cortical adaptation that

occurs. The question remains, however, whether training

involving the repetitive execution of a simple movement

against a large resistance has the capacity to cause

adaptations in the motor cortex. In the present experiment,

we investigated whether resistance training induces relatively

long-lasting changes in the functional properties of the

corticospinal pathway in humans.

The sites of neural adaptation induced by resistance training in humans

Timothy J. Carroll, Stephan Riek and Richard G. Carson

Perception and Motor Systems Laboratory, The School of Human Movement Studies, The University of Queensland, Brisbane, Queensland 4072,

Australia Although it has long been supposed that resistance training causes adaptive changes in the CNS, the sites and nature of these adaptations have not previously been identified. In order to determine whether the neural adaptations to resistance training occur to a greater extent at cortical or subcortical sites in the CNS, we compared the effects of resistance training on the electromyographic (EMG) responses to transcranial magnetic (TMS) and electrical (TES) stimulation. Motor evoked potentials (MEPs) were recorded from the first dorsal interosseous muscle of 16 individuals before and after 4 weeks of resistance training for the index finger abductors, or training involving finger abduction-adduction without external resistance was delivered at rest at intensities from 5 % below the passive threshold to the maximal output of the stimulator. TMS and TES were also delivered at the active threshold intensity while the participants exerted torques ranging from 5 to 60 % of their maximum voluntary contraction (MVC) torque.

The average latency of MEPs elicited by TES was significantly shorter than that of TMS MEPs, which indicates that the site of

activation differed between the two forms of stimulation. Training resulted in a significant increase in MVC torque for the resistance-training group, but not the control group. There were no statistically significant changes in the corticospinal properties measured at rest for either group. For

the active trials involving both TMS and TES, however, the slope of the relationship between MEP size and the torque exerted was significantly lower after training for the resistance-training group. Thus, for a specific level of muscle activity, the magnitude of the EMG responses to both

forms of transcranial stimulation were smaller following resistance training. These results suggest that resistance training changes the functional properties of spinal cord circuitry in humans, but does not substantially affect the organisation of the motor cortex. (Received 7 June 2002; accepted after revision19 July 2002; first published online 16 August 2002) Corresponding author T. J. Carroll: Neurophysiology Laboratory, E-427 Van Vliet Centre, Faculty of Physical Education and Recreation, University of Alberta, Edmonton, Canada T6G 2H9. Email: tcarroll@ualberta.ca

Journal of Physiology (2002),

Journal of Physiology

The specific aim of the present experiment was to determine

whether resistance training changes the input-output

properties of the corticospinal pathway at rest and during

muscle activation. In order to investigate whether resistance

training causes adaptations at cortical or subcortical sites

along the corticospinal pathway, we determined the effect

of training on the magnitude of responses to transcranial

magnetic stimulation (TMS) and transcranial electrical

stimulation (TES) during background muscle activation.

The mechanism by which descending corticospinal volleys

are elicited differs between TMS and TES. A large proportion

of the muscular response to TMS of the upper limb

muscles is brought about by trans-synaptic excitation of

corticospinal cells, which results in one or more 'indirect'

descending volleys, or I waves (Mazzochio et al. 1994;

Edgley et al. 1997; Di Lazzaro et al. 1998a,b). Compared

with TMS, a greater proportion of the corticospinal

neurones activated by TES are depolarised directly by the

electrical stimulus, probably at an axonal site two or three

nodes distant to the axon hillock, resulting in a so-called

'direct', or D wave (e.g. Di Lazzaro et al. 1998a, 1999). The

responses to TES are therefore less strongly influenced by

the excitability state of the motor cortex than those to

TMS. It was anticipated that the present experiment,

which investigated changes in the evoked responses to

both TES and TMS, would allow us to determine whether

the adaptations to resistance training occur to a greater

extent at cortical or subcortical sites in the CNS.

Methods

Participants, Sixteen individuals (aged 22-36 years; 15 male, 1 female) volunteered for this experiment. The participants were randomly allocated to either a resistance-training condition or to a condition involving unresisted movement. All of the participants were right handed according to the Edinburgh Handedness

Inventory (Oldfield, 1971). Each individual gave written,

informed consent to participate in the study, the procedures for which conformed to the Declaration of Helsinki and were

approved by the University of Queensland Medical Research

Ethics Committee.

General procedure

Twelve training sessions were performed by the participants over a 4 week training period (three sessions per week). Before and after the training period, each volunteer participated in an experimental session involving transcranial and peripheral nerve stimulation. The final experimental session was conducted between 48 and 96 h after the last training session. Participants were seated in a dentist's chair, with their forearm and hand supported by a custom-built device (Fig. 1A). The device restricted movement of the wrist and hand, and allowed measurement of abduction torque about the second metacarpo-phalangeal joint

via a torque transducer aligned co-axially with the joint. Motor

evoked potentials (MEPs) were recorded from the first dorsal

interosseous muscle (FDI) at rest and during background

contraction. During the resting trials, TMS was applied at a range of stimulation intensities from just below the threshold intensity for eliciting a response at rest to the maximal output of the stimulator. During the active trials, TMS and TES were applied at the active threshold intensity while the participants exerted finger abduction torque at a range of levels from 5 to 60 % of their maximum capacity.

Training Programme

The experimental device used during the stimulation sessions was also used to apply resistance during training. The

second metacarpo-phalangeal joint was aligned co-axially with

the main shaft of a pulley system. Weights were attached to the terminal pulley in a manner that applied a resistance to abduction movements of the index finger at a point 5 cm from the axis of joint rotation. Thus, in order to rotate the device shaft at a steady pace, the subjects were required to perform shortening and lengthening muscle actions with index finger abductors. A potentiometer was attached in series with the main shaft of the

training device in order to record the joint position during

training. The calibrated output of the potentiometer was amplified

and displayed in real time to provide visual feedback to the

participants. They were required to move their fingers between

20 deg of finger abduction and 15 deg of finger adduction. The

participants were instructed to move steadily throughout the

prescribed range, so that they controlled the load at all times. Four

trials, each consisting of six complete finger abduction-adduction cycles, were completed in each training session. All training loads were scaled to each individual's maximal dynamic strength (as determined prior to training); the load was increased from 70 % of maximum in steps of 5 % whenever three sessions had been completed with the previous load. Participants in the unresisted training group performed the same number of movements, through the same range, but without external resistance.

Maximal voluntary contraction

The peak torque recorded in either of two trials was taken as the maximal voluntary contraction (MVC). Participants were instructed to increase torque steadily for 2 s and then to exert maximal torque for 3 s. Verbal encouragement and visual feedback of the torque exerted were provided.

EMG recordings and peripheral nerve stimulation

The surface EMG was recorded from the FDI via Ag/AgCl

electrodes (1 cm in diameter) positioned respectively over the

motor point of the muscle and the metacarpo-phalangeal joint of the index finger. The reference electrode was attached over a bony prominence on the distal part of the radius. Signals were band pass filtered (30-1000 Hz), and amplified (gain w 200-1000) by a Grass (P511) amplifier. EMG data were sampled at 5000 Hz by a 12 bit National Instruments board and saved to disk.

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