output in MVCs were found to hold true for non-fatigued but not for

Journal

of

Physiology

(1990),

423,

pp.

1-14

With

7figure8

Printed

in

Great

Britain

TONIC

VIBRATION

REFLEXES

ELICITED

DURING

FATIGUE

FROM

MAXIMAL

VOLUNTARY

CONTRACTIONS

IN

MAN

BY

L.

G.

BONGIOVANNI*

AND

K.-E.

HAGBARTHt

From

the

Department

of

Clinical

Neurophysiology,

University

Hospital,

S-751

85

Uppsala,

Sweden

(Received

27

April

1989)

SUMMARY

1.

In

the

present

study

on

human

foot

dorsiflexor

muscles

we

have

examined

the

effects

of

high-frequency

(150

Hz)

muscle

vibration

on

weak

or

moderate

voluntary

contractions

(maintained

by

constant

effort)

and

on

maximal

voluntary

contractions

(MVCs)

of

(i)

non-fatigued

muscles,

(ii)

muscles

fatigued

by

sustained

MVCs

and

(iii)

muscles

deprived

of

y-fibre

innervation

by

partial

anaesthetic

nerve

block.

The

motor

outcome

of

the

voluntary

dorsiflexion

efforts

was

assessed

by

measuring

the

firing

rates

of

single

motor

units

in

the

anterior

tibial

(TA)

muscle,

the

mean

voltage

EMG

activity

from

the

pretibial

muscles

and

foot

dorsiflexion

force.

2.

With

the

subject

instructed

to

exert

constant

effort

in

maintaining

a

weak

or

moderate

contraction,

superimposed

vibration

caused

an

enhancement

of

EMG

activity

and

contraction

force.

3.

Previous

claims

that

muscle

vibration

has

no

facilitatory

effect

on

motor

output

in

MVCs

were

found

to

hold

true

for

non-fatigued

but

not

for

fatigued

muscles.

Thus,

the

fatigue-induced

decline

in

EMG

activity

and

motor

unit

firing

rates

was

counteracted

by

short

periods

(<

10-20

s)

of

superimposed

vibration.

However,

with

longer

vibration

periods

it

seemed

as

if

the

initial

facilitation

converted

into

an

opposite

effect

which

accentuated

the

fatigue-induced

decline

in

motor

output

and

contraction

force.

4.

Like

muscle

fatigue,

a

partial

anaesthetic

block

of

the

deep

peroneal

nerve,

supposedly

interrupting

transmission

in

y-motor

fibres,

caused

a

reduction

of

MVC

motor

unit

firing

rates

which

could

be

counteracted

by

muscle

vibration.

In

prolonged

MVCs

performed

during

the

block,

motor

unit

firing

rates

did

not

show

the

normal

progressive

decline

from

an

initially

high

level,

but

stayed

at

a

relatively

constant

low

level

throughout

the

contraction

period.

5.

Even

though

alternative

interpretations

are

possible,

the

results

agree

with

the

hypotheses

(i)

that

in

sustained

MVCs,

fatigue

processes

occur

not

only

in

extrafusal

but

also

in

intrafusal

muscle

fibres,

(ii)

that

the

intrafusal

fatigue

leads

to

a

reduction

of

the

voluntary

drive

conveyed

to

the

ac-motoneurones

via

the

y-loop

and

(iii)

that

vibration-induced

activity

in

group

Ia

afferents

can

act

as

a

substitute

for

the

diminished

fusimotor

drive.

*

Present

address:

Istituto

di

Neurologia,

Universita

degli

Studi

di

Verona,

37126

Verona,

Italy.

t

To

whom

correspondence

and

reprint

requests

should

be

sent.

MS

7658

1

PHY

423

L.

G.

BONGIOVANNI

AND

K.-E.

HAGBARTH

INTRODUCTION

It

is

well

established

that

motor

unit

firing

rates

decline

as

muscle

fatigue

develops

during

sustained

maximal

voluntary

contractions

(Marsden,

Meadows

&

Merton,

1971;

Grimby,

Hannerz

&

Hedman,

1981;

Bigland-Ritchie,

Johansson,

Lippold,

Smith

&

Woods,

1983).

As

emphasized

by

Bigland-Ritchie

and

co-workers,

this

decline

is

advantageous

in

that

it

helps

to

protect

peripheral

neuromuscular

structures

from

excessive

exhaustion

and

to

prevent

impulse

frequencies

higher

than

those

needed

for

full

tetanic

activation

of

the

fatiguing

muscle

fibres

(Bigland-

Ritchie,

Kukulka,

Lippold

&

Woods,

1982;

Bigland-Ritchie

et

al.

1983;

Bigland-

Ritchie

&

Woods,

1984).

There

is

strong

evidence

that

the

decline

depends

not

only

on

motoneurone

adaptation

processes

(Kernell

&

Monster,

1982

a,

b)

but

also

on

some

changes-in

afferent

inflow

from

the

contracting

muscle

which

reduce

the

net

amount

of

excitation

received

by

the

cz-motoneurones

(Bigland-Ritchie,

Dawson,

Johansson

&

Lippold,

1986;

Woods,

Furbush

&

Bigland-Ritchie,

1987;

Garland,

Garner

&

McComas,

1988).

The

precise

nature

of

these

changes

is

still

unknown.

It

has

been

proposed

that

a

fatigue-induced

inflow

of

autogenetic

inhibitory

impulses

in

group

III

and

IV

muscle

afferents

may

contribute

to

the

fall

in

motoneurone

firing

rate

(Bigland-Ritchie

et

al.

1986;

Garland

et

al.

1988),

but

it

is

also

possible

that

muscle

fatigue

is

associated

with

a

decreased

inflow

of

autogenetic

excitatory

impulses

mediated

to

the

a-motoneurones

via

the

y-loop.

As

reported

in

a

previous

study,

a

partial

anaesthetic

muscle

nerve

block,

preferentially

affecting

small-diameter

fibres,

makes

the

subject

unable

to

generate

those

high

motor

unit

firing

rates

which

are

normally

seen

in

the

initial

phase

of

maximal

voluntary

contractions

(Hagbarth,

Kunesch,

Nordin,

Schmidt

&

Wallin,

1986).

It

was

inferred

that

the

block

affected

the

small

y-motor

fibres

and

thereby

deprived

the

a-motoneurones

of

an

excitatory

inflow

via

the

y-loop

which

they

require

in

order

to

generate

optimal

firing

rates.

This

inference

was

supported

by

the

observation

that

the

motor

disability

was

partly

overcome

by

muscle

vibration,

which

is

known

to

be

a

potent

stimulus

for

primary

muscle

spindle

endings

and

can

act as

a

substitute

for

a

diminished

fusimotor

drive.

If

the

decline

in

z-motor

output

during

a

sustained

maximal

voluntary

contraction

(MVC)

in

part

depends

on

a

reduction

in

the

fusimotor-driven

I

a

afferent

inflow

from

the

spindles,

one

would

expect

that

-

in

a

similar

way

as

during

a

y-fibre

block

-

vibration-induced

activation

of

primary

spindle

endings

can

compensate

for

the

diminished

fusimotor

drive

and

restore

a

higher

level

of

a-motor

output.

On

the

above

premises,

one

would

also

expect

an

anaesthetic

block

of

y-motor

fibres

to

result

not

only

in

an

inability

to

generate

high

motor

unit

firing

rates

in

the

initial

phase

of

MVCs,

but

also

in

a

less

pronounced

decline

in

motor

unit

firing

rates

as

contraction

continues.

The

present

experiments

were

undertaken

to

test

the

validity

of

these

expectations.

METHODS

Subject

Repeated

experiments

were

performed

on

five

healthy

subjects

(aged

33-63

years)

including

the

authors.

All

of

these

subjects

were

experienced

in

maintaining

maximal

voluntary

contraction

for

2

TONIC

VIBRATION

REFLEX

IN

MUSCLE

FATIGUE

the

time

required.

Twenty

other

subjects

participated

in

some

of

the

tests.

All

single-motor-unit

recordings

were

made

on

one

of

the

authors

(K.-E.

H.).

The

subjects

gave

their

informed

consent

as

requested

by

the

local

Research

Ethics

Committee.

General

procedures

The

subject

was

comfortably

seated

in

a

semireclining

position

and

the

examined

right

leg

was

fixed

with

the

knee

at

120

deg

and

the

ankle

at

90

deg.

The

foot

was

strapped

to

a

plate

to

which

a

strain

gauge

was

attached

10

cm

from

the

ankle

rotation

axis.

Before

starting

an

experiment,

it

was

checked

that

the

strapping

did

not

cause

any

painful

sensation

from

the

foot

during

maximal

isometric

dorsiflexor

contractions.

Three

types

of

tests

were

designed

to

investigate

the

effect

of

muscle

vibration

on

non-fatigued

and

fatigued

MVCs

of

the

ankle

dorsiflexor

muscles:

(1)

in

a

series

of

brief

(3-4

s)

non-fatigued

MVCs,

control

contractions

alternated

with

contractions

performed

during

concurrent

brief

periods

of

muscle

vibration;

(2)

the

same

type

of

test

was

repeated

after

the

dorsiflexor

muscles

had

been

fatigued

by

a

prolonged

MVC;

(3)

vibration

was

applied

for

20-25

s

while

muscle

fatigue

developed

during

a

sustained

(1

min)

MVC.

Beside

the

vibration-induced

effects

on

MVCs

we

also

studied

the

motor

responses

evoked

when

vibration

was

applied

during

relaxation

and

during

voluntary

dorsiflexor

contractions

of

weak

or

moderate

strength.

The

motor

responses

were

assessed

by

surface

EMG

recordings,

measurements

of

single-motor-unit

firing

rates

and

dorsiflexion

force.

Nerve

block

In

one

experiment,

the

subject

performed

a

series

of

sustained

(1

min)

MVCs

while

he

slowly

recovered

from

a

complete

ankle

dorsiflexor

paresis

induced

by

a

peroneal

nerve

block.

The

block

was

produced

by

injection

of

prilocain

(Citanest

5

mg/ml

+

adrenaline)

around

the

peroneal

nerve

behind

the

fibular

head.

Vibrators

Vibration

was

applied

over

the

tendons

of

the

ankle

dorsiflexor

muscles

using

one

of

two

vibrators

which

were

adjusted

so

that

the

amplitude

of

vibration

was

approximately

1-5

mm

and

the

vibration

frequency

150

Hz.

These

vibrators

were:

(i)

a

commercially

available

electrical

'TVR-vibrator'

(Heiwa

Electronic

Industrial

Co.)

and

(ii)

a

pneumatic

vibrator

powered

by

compressed

air

(to

avoid

electric

artifacts

in

the

electromyograms).

As

in

previous

studies

of

vibration-induced

responses

of

human

muscle

spindle

afferents

(Burke,

Hagbarth,

Lbfstedt

&

Wallin,

1976a,

b)

the

vibrators

were

held

manually

with

a

constant

force

of

application

(20-25

N).

Manual

application

was

superior

to

strapping

the

vibrator

to

the

limb

because

the

strap

could

facilitate

the

spread

of

vibration

to

other

muscles.

Force

measurements

The

strain

gauge

attached

to

the

foot

plate

measured

the

force

resulting

from

contraction

of

the

foot

dorsiflexor

muscles.

Unless

otherwise

stated,

the

subjects

were

not

allowed

to

see

the

signal

from

the

force

transducer

during

the

experiments.

Surface

EMG

This

was

recorded

with

a

pair

of

surface

electrodes

(diameter

0

7

cm)

placed

3

cm

apart

on

the

skin

overlying

the

anterior

tibial

(TA)

muscle

about

15

cm

below

the

knee.

The

signals

were

amplified

(frequency

band

10-100

Hz),

rectified

and

passed

through

a

leaking

integrator

with

a

time

constant

of

0-5

s.

Single-unit

potentials

For

assessment

of

motor

unit

firing

rates

in

the

tibialis

anterior

(TA)

muscle

during

brief

and

sustained

isometric

voluntary

contractions

we

used

electrodes

of

the

type

commonly

used

for

microneurography

(Vallbo,

Hagbarth,

Torebjork

&

Wallin,

1979):

coated

tungsten

electrodes

with

a

shaft

diameter

of

02

mm,

a

tip

diameter

of

5-10

him

and

an

impedance

of

>

100

kQ.

With

a

subcutaneous

reference

needle

electrode

placed

over

the

tibial

bone,

the

microelectrode

was

slowly

advanced

in

the

contracting

muscle

while

searching

for

single-unit

discharges

with

a

high

signal-

to-noise

ratio

and

minor

contamination

from

signals

in

neighbouring

units.

Only

such

recordings

1-2

3

L.

G.

BONGIOVANNI

AND

K.-E.

HAGBARTH

were

accepted

in

which

it

proved

possible

to

follow

the

firing

rates

of

single

identified

units

both

during

brief

and

sustained

MVCs.

Sometimes

two

or

three

units

with

different

spike

amplitudes,

recruitment

thresholds

and

firing

rates

could

be

identified

in

the

same

recording

(Fig.

4).

The

single-unit

data

presented

in

this

and

in

a

succeeding

study

(Bongiovanni,

Hagbarth

&

Stjernberg,

1990)

are

based

on

technically

acceptable

recordings

from

at

least

twenty

motor

units.

Signal

displays

and

analysis

The

signals

were

monitored

on

a

four-channel

storage

oscilloscope

(Tektronix

549)

or

on

a

video

display

monitor

(Gould

V

1000)

and

recorded

on

paper

by

an

electrostatic

recorder

(Gould

ES

1000).

The

plots

showing

single-motor-unit

firing

rates

during

sustained

contractions

were

obtained

by

counting

the

number

of

unitary

spikes/s

with

5

s

intervals

between

each

count.

RESULTS

The

tonic

vibration

reflex

and

its

effect

on

unfatigued

and

fatigued

voluntary

contractions

It

is

well

known

that

sustained

vibration

applied

to

an

initially

relaxed

skeletal

muscle

or

its

tendon

normally

induces

a

tonic

reflex

contraction

in

the

muscle

exposed

to

the

vibration

waves

(Eklund

&

Hagbarth,

1966;

Lance,

De

Gail

&

Neilson,

1966).

Figure

1A

illustrates

a

typical

example

of

such

a

tonic

vibration

reflex

in

the

TA

muscle.

As

shown

by

the

EMG

and

force

traces,

a

weak

contraction

develops

slowly

as

vibration

continues,

and

when

vibration

stops

the

contraction

fades

away

within

a

few

seconds.

EMG

A

Force

20

N

Vibration

EMG

B

--

Force

40

N

a_

I

Vibration

Fig.

1.

TA

surface

EMG

and

force

records

showing

typical

examples

of

the

slow

development

of

the

tonic

vibration

reflex

in

a

resting

subject

(A)

and

the

abrupt

onset

of

the

reflex

in

a

subject

asked

to

exert

constant

effort

in

the

maintenance

of

a

weak

voluntary

background

contraction

(B).

In

this,

as

in

the

succeeding

figures,

filled

bars

indicate

vibration

at

150

Hz

applied

over

the

TA

tendon.

It

is

also

known

from

previous

reports

that

when

vibration

is

applied

to

a

muscle

engaged

in

a

weak

or

moderate

voluntary

contraction

(maintained

by

constant

effort),

the

vibration

reflex

produces

an

involuntary

enhancement

of

a-motor

output

(EMG)

and

contraction

strength

(Hagbarth

&

Eklund,

1966;

McCloskey,

Ebeling

&

Goodwin,

1974).

We

observed

such

vibration-induced

enhancements

of

weak

or

moderate

voluntary

contractions

in

all

five

subjects

exposed

to

this

test,

and

an

example

is

shown

in

Fig.

1B

(same

subject

as

in

Fig.

1A).

In

comparison

with

the

4

TONIC

VIBRATION

REFLEX

IN

MUSCLE

FATIGUE

reflex

elicited

in

an

initially

relaxed

muscle,

the

response

to

vibration

was

stronger

and

had

a

more

abrupt

onset

when

displayed

against

the

background

of

a

weak

voluntary

contraction

(note

different

force

scales

in

Fig.

1A

and

B).

Once

a

tonic

reflex

response

had

reached

its

plateau

level,

this

level

stayed

constant

during

the

rest

of

the

vibration

period

(longest

vibration

period

30

s).

A

B

EMG

4

min

of

MWC

ForceJJJJJJ

LL

~~

)

~

~

1111

ll

I

200

N

SLA~~~iN

I

I

I

I

I

I

I

20

s

Fig.

2.

EMG

activity

and

force

developed

by

foot

dorsiflexor

muscles

during

brief

MVCs

repeated

with

rest

intervals

of

about

20

s

and

with

vibration

applied

to

the

TA

tendon

during

every

second

contraction.

A,

in

the

non-fatigued

subject,

the

EMG

and

force

traces

are

similar

in

contractions

with

and

without

vibration.

B,

with

the

subject

fatigued

by

a

preceding

prolonged

MVC,

vibration

has

a

facilitatory

effect

on

the

brief

MVCs

and

counteracts

the

fatigue-induced

decline

in

EMG

activity

and

force.

See

text.

According

to

previous

reports,

muscle

vibration

does

not

normally

enhance

motor

output

in

maximal

voluntary

contractions

(Hagbarth

&

Eklund,

1969;

Hagbarth

et

al.

1986).

In

the

present

study,

this

was

found

to

hold

true

for

unfatigued

but

not

for

fatigued

MVCs.

The

procedure

illustrated

in

Fig.

2A

was

adopted

to

test

the

effect

of

muscle

vibration

on

EMG

activity

and

force

in

unfatigued

MVCs.

After

a

period

of

relaxation,

lasting

for

at

least

3

min,

the

subject

initiated

a

series

of

brief

(3-4

s)

MVCs,

separated

by

rest

periods

of

20

s.

Control

contractions

(without

vibration)

were

alternated

with

contractions

performed

while

vibration

was

applied

to

the

TA

tendon.

No

sign

of

a

tonic

vibration

reflex

could

be

detected

in

any

of

the

twenty-

five

subjects

exposed

to

this

test,

i.e.

vibration

had

no

significant

influence

on

ax-motor

output

(EMG)

and

contraction

force

(example

shown

in

Fig.

2A).

In

the

experiment

illustrated

in

Fig.

2,

the

series

of

intermittent

MVCs

was

temporarily

interrupted

by

a

long-lasting

(4

min),

fatiguing

MVC.

Following

this

manoeuvre,

there

was

a

marked

reduction

of

the

EMG

activity

recorded

during

the

intermittent

MVCs

(mean:

-18

%),

and

this

fatigue-induced

decline

in

motor

output

was

to

a

large

extent

compensated

for

by

vibration.

In

the

sequence

shown

in

Fig.

2B,

the

EMG

peaks

were

on

average

16

%

higher

in

the

vibration-exposed

than

in

the

interspersed

control

contractions,

whereas

the

vibration-induced

enhancement

of

contraction

force

did

not

amount

to

more

than

4

%.

Four

experiments

of

this

type

were

performed

(on

two

subjects)

and

they

all

showed

that

vibration

effectively

counteracted

the

fatigue-induced

decline

in

EMG.

activity

with

little

or

no

corresponding

effect

on

the

force.

5

L.

G.

BONGIOVANNI

AND

K.-E.

HAGBARTH

More

complex

responses

were

seen

when

vibration

was

applied

during

sustained

MVCs.

Figure

3A

shows

the

well-known

progressive

decline

in

EMG

activity

and

force,

normally

occurring

during

a

sustained

MVC.

In

five

subjects,

the

TA

tendon

was

exposed

to

vibration

for

about

25

s

during

the

course

of

such

a

sustained

MVC,

EMG

A

Force

200

N

20

s

EMG

Force

200

N

20

s

Vibration

Fig.

3.

A,

a

sustained

(60

s)

MVC

of

the

foot

dorsiflexor

muscles

showing

the

typical

progressive

decline

of

EMG

activity

and

force.

B,

effects

of

20

s

vibration

during

a

similar

contraction

performed

by

the

same

subject.

Note

the

initial

facilitatory

effect

(most

prominent

in

the

EMG

trace)

with

succeeding

rapid

decline

and

post-vibratory

recovery.

See

text.

and

Fig.

3B

shows

a

representative

example

of

the

resulting

changes

in

EMG

activity

and

force.

The

EMG

activity

rose

during

the

initial

phase

of

vibration,

but

as

vibration

continued

this

initial

increase

was

followed

by

a

rapid

decline.

Cessation

of

vibration

was

followed

by

post-vibratory

enhancement

of

EMG

activity.

In

the

example

illustrated,

the

initial

increase

in

EMG

activity

had

no

distinct

counterpart

in

the

force

trace,

whereas

the

down-going

component

of

the

response

and

the

post-

vibratory

recovery

was

also

observed

in

this

trace.

A

vibration-induced

motor

response

of

similar

shape

as

seen

in

the

surface

EMG

records

was

observed

also

when

studying

the

firing

rates

of

individual

TA

motor

units

during

sustained

MVCs.

However,

it

was

noticed

that

different

motor

units

were

not

affected

to

the

same

degree

by

vibration.

The

units

which

were

most

susceptible

to

the

influence

of

muscle

vibration

in

these

tests

were

those

which

were

characterized

by

(1)

a

high

recruitment

threshold

in

voluntary

isometric

contrac-

tions,

(2)

a

high

firing

rate

during

the

initial

phase

of

MVCs

and

(3)

a

rapid

decline

in

firing

rate

during

sustained

MVCs.

These

high-threshold

units

were

not

activated

by

vibration

alone,

i.e.

they

were

not

recruited

when

the

tonic

vibration

reflex

was

elicited

in

an

initially

relaxed

muscle.

By

contrast,

low-threshold

units,

which

were

recruited

both

by

the

vibration

reflex

alone

and

by

weak

voluntary

contractions,

were

relatively

more

resistant

to

the

influence

of

vibration

while

fatigue

developed

during

sustained

MVCs.

Figure

4

illustrates

our

way

of

classifying

'low-threshold'

and

'high-threshold'

units,

and

Fig.

5

presents

an

example

of

how

the

two

extreme

6

TONIC

VIBRATION

REFLEX

IN

MUSCLE

FATIGUE

types

of

units

responded

to

vibration

as

muscle

force

declined

during

a

sustained

MVC.

Both

units

responded

with

a

transient

initial

increase

in

firing

rate,

more

pronounced

for

the

high-threshold

than

for

the

low-threshold

unit,

and

in

this

case

also

the

force

record

showed

an

initial

up-going

deflection.

However,

as

vibration

continued,

the

initial

facilitatory

effect

vanished

and

seemed

to

be

followed

by

an

effect

which

acted

in

the

opposite

direction

and

which

was

followed

by

a

post-

vibratory

rebound.

I

I

II

I

li

ii

ii

iii

II

II

/>

~~-~~~-~~=

-

I20

N

A~~~~~~~~~~~~~~

is

F

T

15

B~~~~~~~~~~~~~~~~~~~~~~~

1

50

N

is

Fig.

4.

Differentiation

between

'low-threshold'

and

'high-threshold'

motor

units

in

the

TA

muscle.

A,

example

of

a

'low-threshold'

unit

being

recruited

by

the

tonic

vibration

reflex

elicited

in

a

resting

subject.

Firing

starts

at

a

minimal

dorsiflexion

force

(

<

3

N).

B,

the

same

unit

is

recruited

at

a

similar

low

dorsiflexion

force

during

a

slowly

rising

voluntary

isometric

contraction.

A

second

unit

comes

into

play

at

about

40

N

and

a

third

unit

at

about

100

N.

Units

of

the

latter

type,

firing

only

when

force

exceeds

50%

of

(non-

fatigued)

maximal

contraction

strength,

are

in

this

and

the

succeeding

study

(Bongiovanni,

Hagbarth

&

Stjernberg,

1990)

classified

as

'high-threshold'

units.

(Low

background

noise

eliminated

by

window

discriminator.)

Figure

6

shows

another

example

of

a

high-threshold

motor

unit

with

a

rapid

fall

in

firing

rate

during

a

sustained

MVC.

In

this

case,

vibration

was

applied

at

a

stage

when

the

unit

had

ceased

firing

to

the

voluntary

drive.

The

vibration

reflex

brought

the

unit

back

into

activity,

and

this

improvement

in

motor

performance

was

reflected

also

in

the

force

trace.

It

should

be

noticed

that

whenever

vibration

was

applied

during

the

course

of

a

sustained

MVC

the

initial

facilitatory

effect

of

vibration

was

never

potent

enough

to

fully

compensate

for

the

fatigue-induced

decline

in

motor

unit

firing

rates.

It

should

also

be

pointed

out

that the

high

motor

unit

firing

rates

seen

in

the

unfatigued

muscle

during

brief

MVCs

or

at

the

very

beginning

of

a

sustained

MVC

could

not

be

enhanced

further

by

vibration.

Nerve

block

experiment

After

injection

of

the

anaesthetic

drug

there

was

a

total

paresis

of

the

foot

dorsiflexor

muscles

lasting

for

about

3

h.

Then,

it

took

about

65

min

from

the

moment

when

the

first

EMG

signs

of

motor

unit

activity

reappeared

in

the

TA

muscle

until

the

subject

regained

full

contraction

strength.

While

the

subject

slowly

7

L.

G.

BONGIOVANNI

AND

K.-E.

HAGBARTH

N

I

4)

40

CD

._

0.

.

&P

L-

0

0

30-

20

10

*

High-threshold

motor

unit

o

Low-threshold

motor

unit

0

i

I

.

.

.

.

.

.

.

I

*

I

.

.

.

.

.

100

S

Vibration

Fig.

5.

Example

showing

that

the

vibration

reflex

temporarily

counteracts

the

progressive

decline

in

firing

rates

of

a

high-

and

a

low-threshold

TA

motor

unit

during

a

sustained

MVC.

Note

that

the

initial

facilitatory

effect

of

vibration

-

more

pronounced

for

the

high-

threshold

unit

-

is

succeeded

by

a

rapid

fall

in

firing

rate

and

a

post-vibratory

rebound.

Similar

biphasic

responses

to

vibration

are

seen

also

in

the

force

trace.

N

I

4)

40

._

0)

.

tr_

L-

0

LL

40

-

30*

20

3001

250

200

150

Vibration

-I

10os

Fig.

6.

High-threshold

TA

motor

units

with

a

high

initial

firing

rate

which

rapidly

declines

during

a

sustained

MVC.

The

unit

stops

discharging

after

55

s,

but

is

brought

back

into

action

when

vibration

is

applied

to

the

TA

tendon.

Note

also

concomitant

rise

in

force.

8

TONIC

VIBRATION

REFLEX

IN

MUSCLE

FATIGUE

recovered

from

the

nerve

block

we

examined

several

times

his

ability

to

maintain

maximal

voluntary

dorsiflexor

contractions

for

1

min.

Figure

7A

shows

the

way

in

which

the

firing

rate

of

a

single

motor

unit

in

the

TA

muscle

changed

from

one

contraction

to

the

next

as

the

recovery

proceeded.

During

the

first

contraction,

0

20

min

a

25

min

*29

min

A

A

65

min

-W

40-

co

E

30

00:

It3

j B|

8

0

30

60s

30

-0

4-.

o

CD

I

20

0

4

z

eoo

o

ii

aN

Hliuai

|I

,

20

s

Vibration

Fig.

7.

MVCs

performed

during

65

min

of

recovery

from

a

complete

peroneal

nerve

block.

A,

firing

patterns

of

a

single

TA

motor

unit

during

four

sustained

(60

s)

MVCs

performed

at

different

stages

of

recovery.

Note

that

in

the

early

recovery

phase

(20

min)

the

firing

rate

stays

at

about

the

same

low

level

throughout

the

contraction

period,

but

as

recovery

proceeds

and

the

initial

firing

rate

rises,

the

frequency

drop,

normally

associated

with

fatigue,

becomes

progressively

more

pronounced.

B,

recordings

from

another

TA

motor

unit

obtained

after

7

min

of

recovery.

Upper

diagram

depicts

the

peak

firing

rate

of

this

unit

during

recurrent

brief

(3-4

s)

MVCs

separated

by

rest

intervals

of

20

s.

Besides

showing

a

gradual

increase

in

firing

rate

and

force

as

recovery proceeds

(during

5

min),

the

diagram

illustrates

the

facilitatory

effect

of

the

vibration

reflex.

initiated

after

20

min

of

recovery,

the

firing

rate

varied

within

the

range

of

20-24

Hz

and

did

not

show

any

obvious

decline.

As

time

passed,

there

was

a

progressive

increase

in

the

firing

rates

during

the

initial

phases

of

the

MVCs,

and

at

the

same

time

the

decline

in

firing

rate

during

the

sustained

contractions

became

more

pronounced.

Hence,

the

discharge

rates

at

the

end

of

the

contraction

periods

were

relatively

similar

and

independent

of

the

initial

firing

levels.

Also

the

accompanying

force

trace

showed

that

the

downward

slopes

became

steeper

as

the

initial

peak

values

rose

during

the

period

of

recovery

(not

illustrated).

The

effect

of

vibration

on

motor

performance

was

examined

during

the

first

20

min

of

recovery

(i.e.

before

the

sequence

illustrated

in

Fig.

7A).

During

this

early

period

of

recovery

the

subject

was

instructed

to

make

brief

(3-4

s)

intermittent

MVCs,

separated

by

rest

periods

of

20

s.

As

long

as

maximal

dorsiflexion

force

was

less

than

10

%

of

normal

values,

vibration

applied

over

the

TA

tendon

had

no

apparent

effect

I

9

L.

G.

BONGIOVANNIVI

AND

K.-E.

HAGBARTH

on

motor

performance,

but

a

facilitatory

effect

appeared

at

the

stage

of

recovery

when

the

subject

had

regained

about

20%

of

his

normal

dorsiflexion

force.

Such

a

vibration-induced

improvement

of

motor

performance

is

illustrated

in

Fig.

7B

where

the

peak

dorsiflexion

force

and

the

firing

rate

of

a

single

TA

motor

unit

are

depicted

for

each

of

eighteen

successive

contractions.

DISCUSSION

Even

though

alternative

interpretations

cannot

be

definitely

excluded,

the

results

are

for

the

most

part

in

accordance

with

the

hypothesis

that

the

decline

in

motor

unit

firing

rates

during

sustained

MVCs

in

part

depends

on

a

reduction

in

fusimotor-

driven

I

a

afferent

inflow

from

the

spindles.

From

previous

microneurographic

recordings

in

man

it

is

known

that

muscle

vibration

of

the

type

used

in

the

present

study

(150

Hz,

amplitude

1f5

mm)

gives

rise

to

an

intense,

sustained

discharge

in

group

Ia

afferents

(Burke

et

al.

1976a,

b),

which

resembles

the

discharge

which

can

be

evoked

by

fusimotor

activation

of

primary

spindle

endings

during

isometric

voluntary

contractions

(Vallbo,

1973;

Vallbo

et

al.

1979).

With

increasing

strength

of

a

voluntary

isometric

contraction,

the

afferent

feedback

from

the

muscle

spindles

in

the

contracting

muscle

grows

as

an

increasing

number

of

I

a

afferents

are

recruited

into

action

(Burke,

Hagbarth

&

Skuse,

1978)

and

the

firing

rate

of

individual

I

a

units

is

enhanced

(Vallbo,

1974).

The

upper

limit

for

the

I

a

firing

rate

in

MVCs

has

for

technical

reasons

been

difficult

to

assess

(neurogram

contaminated

by

EMG

signals),

but

firing

rates

close

to

100

Hz

have

been

observed

in

voluntary

contractions

of

moderate

strength

(Vallbo,

1973)

and

this

approaches

the

highest

steady

firing

rates

observed

in

response

to

vibration

(Burke

et

al.

1976

a

b).

In

the

present

study,

we

used

an

indirect

way

of

assessing

changes

in

afferent

inflow

from

the

primary

spindle

endings

as

muscle

fatigue

developed.

The

technique

is

based

on

the

presumption

that

by

studying

the

facilitatory

effects

of

muscle

vibration

on

a-motor

output

in

voluntary

contractions

of

different

strength

it

is

possible

to

make

an

appraisal

of

the

background

fusimotor-driven

I

a

discharge

in

these

contractions.

The

fact

that

vibration

enhances

the

motor

output

in

weak

or

moderate

contractions

(Fig.

1

B)

may

be

taken

as

an

indication

that

vibration

induces

a

I

a

afferent

inflow

which

exceeds

the

pre-existing

fusimotor-driven

discharge

and

thereby

allows

the

tonic

vibration

reflex

to

exert

its

autogenetic

excitatory

effect

on

the

a-motoneurones.

As

the

fusimotor-driven

discharge

increases

with

increasing

contraction

strength,

a

stage

will

probably

be

reached

when

vibration

can

cause

little

or

no

further

enhancement

of the

I

a

inflow.

Such

a

state

of

'saturation'

may

well

account

for

the

fact

that

vibration

has

no

facilitatory

effect

on

EMG

activity

and

motor

unit

firing

rates

in

unfatigued

MVCs.

However,

as

shown

in

the

present

study

vibration

regains

its

autogenetic

excitatory

effect

on

the

motor

output

when

muscle

fatigue

develops

during

intermittent

or

maintained

MVCs

(Figs

2B,

3B,

5

and

6).

The

simplest

explanation

of

this

finding

is

that

muscle

fatigue

from

MVCs

is

associated

with

such

a

decline

in

the

fusimotor-driven

I

a

discharge

that

the

vibration

response

is

no

longer

occluded.

The

present

results

provided

no

definite

clue

regarding

the

mechanisms

responsible

for

the

deduced

decline

in

Ia

afferent

activity.

It

is

possible

that

in

sustained

MVCs

to

TONIC

VIBRATION

REFLEX

IN

MUSCLE

FATIGUE

fatigue

processes

occur

not

only

in

extrafusal

but

also

in

intrafusal

muscle

fibres,

and

that

a

fatigue-induced

decline

in

intrafusal

contraction

force

leads

to

a

reduction

in

the

fusimotor-driven

afferent

discharge.

Signs

of

such

intrafusal

fatigue

have

been

observed

following

prolonged

stimulation

of

static

y-axons

in

the

cat,

and

there

is

evidence

that

reduction

of

muscle

blood

flow

(which

occurs

during

sustained

MVCs)

enhances

muscle

spindle

fatigue

(Barker,

Emonet-Denand,

Harker,

Jami

&

Laporte,

1976;

Emonet-Denand

&

Laporte,

1978;

Decorte,

Emonet-Denand,

Harker,

Jami

&

Laporte,

1984).

An

alternative

possibility

is

that

muscle

fatigue

gives

rise

to

an

inhibitory

inflow

in

group

III

and

IV

muscle

afferents

(Bigland-Ritchie

et

al.

1986;

Garland

et

al.

1988)

which

lowers

the

discharge

rates

not

only

in

a-

but

also

in

y-motoneurones

and

thereby

reduces

the

fusimotor

activation

of

the

spindle

endings

(cf.

comments

below

regarding

the

outcome

of

the

present

nerve

block

experiment).

During

sustained

MVCs,

the

amount

of

excitation

that

the

motoneurones

receive

from

their

own

muscle

may

be

reduced

not

only

by

intrafusal

fatigue

but

also

by

such

mechanisms

as

presynaptic

inhibition

of

Ia

terminals

or

'transmitter

depletion'

at

Ia

synapses

(Hagbarth

&

Eklund,

1966;

De

Gail,

Lance

&

Neilson,

1966;

Delwaide,

1973;

Desmedt

&

Godaux,

1978;

Hultborn,

Meunier,

Morin

&

Pierrot-Deseilligny,

1987

a).

According

to

Hultborn,

Meunier,

Pierrot-Deseilligny

&

Shindo

(1987b)

there

is

at

the

onset

of

a

voluntary

contraction

a

decrease

in

presynaptic

inhibition

of

I

a

terminals

on

the

motoneurones

of

the

contracting

muscle.

If

this

'opening'

of

I

a

transmission

subsides

as

contraction

continues,

the

motoneurone

firing

rate

will

decline.

Motoneurone

adaptation

is

probably

another

factor

contributing

to

the

progressive

fall

in

motoneurone

firing

rates

(Kernell

&

Monster,

1982

a,

b)

and

Renshaw

inhibition

may

also

be

involved

in

this

process.

In

agreement

with

previous

observations

by

Grimby

et

al.

(1981)

we

noted

that

high-threshold

motor

units

with

high

initial

firing

rates

during

MVCs

show

a

faster

frequency

drop

during

fatigue

than

low-threshold

units.

This

seems

to

accord

with

findings

in

the

cat

that

late

adaptation

is

more

prominent

in

large

motoneurones

than

in

small

ones,

and

that

for

one

and

the

same

cell

adaptation

is

more

pronounced

at

high

than

at

lower

initial

firing

rates

(Kernell

&

Monster,

1982a,

b).

However,

it

is

also

to

be

expected

that

the

last

recruited

motor

units

are

the

first

to

show

a

frequency

drop

and

to

be

de-recruited

as

the

excitatory

drive

on

the

motoneurone

pool

declines.

In

similar

terms,

it

is

also

possible

to

explain

why

the

facilitatory

effect

of

vibration

was

more

pronounced

on

the

high-threshold

than

on

the

low-threshold

units

(Fig.

5).

Merton

(1954)

and

Bigland-Ritchie,

Jones

&

Woods

(1979)

have

reported

that

during

sustained

MVCs,

performed

by

well-trained

and

motivated

subjects,

superimposed

electrical

tetanization

of

the

muscle

nerve

increases

EMG

activity

but

not

tension,

indicating

that

the

reduction

in

motor

unit

firing

rate

is

not

responsible

for

loss

of

force.

However,

less

well

trained

or

motivated

subjects

may

have

considerable

difficulty

in

maintaining

a

voluntary

drive

sufficient

to

prevent

supramaximal

nerve

stimuli

from

causing

an

enhancement

of

contraction

strength

(Grimby

et

al.

1981;

Woods

et

al.

1987).

Different

degrees

of

motivation

in

the

maximal

force

tasks

may

well

account

for

the

fact

that

the

vibration-induced

enhancement

of

motor

output

during

sustained

MVCs

was

sometimes

but

not

always

accompanied

by

a

distinct

increase

in

contraction

force

(cf.

Figs

3B

and

6).

If

a

reflex

inhibition

of

a-motoneurones

from

group

III

and

IV

muscle

afferents

is

11

L.

G.

BONGIOVANNI

AND

K.-E.

HAGBARTH

a

prime

cause

of

the

decline

in

motor

unit

firing

rates

during

sustained

MVCs

(Bigland-Ritchie

et

al.

1986;

Garland

et

al.

1988),

one

would

expect

an

anaesthetic

block

of

these

small-diameter

fibres

to

enhance

the

subject's

ability

to

maintain

high

motor

unit

firing

rates.

This

did

not

happen

in

the

nerve

block

experiment.

The

outcome

of

this

experiment

indicates

that

a

block

of

small-diameter

fibres

in

the

muscle

nerve

removes

an

excitatory

inflow

to

the

a-motoneurones

which

is

needed

for

the

generation

of

the

high

initial

firing

rates

in

MVCs,

and

which

fades

away

as

muscle

fatigue

develops.

Without

ascribing

all

the

effects

of

the

local

anaesthetic

as

seen

in

the

EMG

to

a

y-fibre

block,

our

tentative

interpretation

of the

results

presented

in

Fig.

7A

is

that

an

anaesthetic

block

affecting

the

efferent

link

of

the

y-loop

results

in

a

similar

disability

to

generate

high

motor

unit

firing

rates

as

is

normally

encountered

when

y-loop

support

has

faded

away,

partly

because

of

muscle

spindle

fatigue,

at

the

end

of

a

long-lasting

MVC.

However,

the

results

do

not

exclude

the

possibility

that

a

reflex

inhibition

of

y-motoneurones

by

small

diameter

muscle

afferents

contributes

to

the

fatigue-induced

decline

in

y-loop

support.

At

any

rate,

the

observations

indicate

that

the

y-loop

serves

an

important

function

in

adjusting

motor

unit

firing

rates

to

the

changes

in

the

contractile

characteristics

of

fatiguing

extrafusal

muscle

fibres.

It

is

of

interest

to

note,

that

a

similar

disability

to

generate

high

initial

motor

unit

firing

rates,

as

illustrated

by

the

bottom

traces

in

Fig.

7A,

was

observed

by

Burke,

Gandevia,

Macefield

&

McKenzie

(1988)

who

recorded

from

motor

axons

proximal

to

a

complete

nerve

block

during

prolonged

MCVs.

An

unexpected

finding

in

the

present

study

was

that,

with

vibration

periods

lasting

more

than

10-20

s

during

MVCs,

the

initial

facilitatory

effect

of

vibration

often

turned

into

an

opposite

effect,

which

seemed

to

accentuate

the

fatigue-induced

decline

in

EMG

activity

and

motor

unit

firing

rates

(Figs

3B

and

5).

This

late

effect

of

prolonged

muscle

vibration

will

be

further

dealt

with

in

a

separate

report

(Bongiovanni

et

al.

1990).

This

work

was

supported

by

the

Swedish

Medical

Research

Council,

grant

No.

B89-14X-02881-

20C.

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