Il ruolo della propriocezione nel controllo del

movimento volontario

Marco Bove
Department of Experimental Medicine, Section of Human Physiology
University of Genoa, ITALY

marco.bove@unige.it
 “You can only control what you sense”

Arthur Prochazka: “Proprioceptive feedback and movement regulation”

Chapter 3, in Handbook of Physiology 1998
Proprioception is the Kinaesthetic Sense

The proprioceptive, or kinaesthetic sense, is related to the

capacity to sense position of joints, to sense their direction and
velocity of movements, and to determine the effort need to grasp
and lift and object.

Proprioception is closely associated with motor system.

The sense of limb position at rest and the sense of limb

movement are the products of inputs from cutaneous
mechanoreceptors, joint receptors, and two specialised
proprioceptors - muscle spindles and Golgi tendon organs.
The sensory innervation
of the spindle is through
primary (Ia) spindle
afferents that innervate
both nuclear bag and
nuclear chain intrafusal
muscle fibers and
secondary (II) afferents
that innervate nuclear
chain fibers.
Motor innervation of the
spindle is supplied by
static and dynamic γ
motor neurons (γs and γδ)
which control the overall
sensitivity of the muscle
spindle.
Static
Dynamic

S
T
R
E
T
C
H
 Responses of cat primary and secondary afferents to linear stretch
(A), tap (B), vibration (C), and release from stretch (D)

Primary spindle endings

sensitive to:
- muscle length and rate of
change of length

Secondary spindle endings

sensitive to:
- muscle length

Matthews PB. Muscle spindles and their motor control. Physiol Rev. 1964 Apr;44:219-88.
Burke, D., Hagbarth, K.E., Lofstedt, L. & Wallin, B.G. (1976). The responses of human muscle spindle endings to
vibration of non-contracting muscles. Journal of Physiology 261, 673-693.
How the movement direction is coded by muscle spindles?
 Primary motor cortex

•The contralateral precentral

gyrus (area 4) is the area in
which the lowest-intensity
stimulation elicited movements.
•Simple movements of single
joints (twitch)
•Activation of neurons near the
electrode
Single M1 Cell Activity Vectors
Recording during movement

Individual neurons encode general directional information

involved in motor neuron pool activation during limb
movement.
Population Vectors

Outputs of individual cells are

summed to give a “population”
vector
Population Vectors and Direction
Specific directions of movement correspond to unique population vectors:
-many motor cortex cells fire with each movement
-cell activity is summed to get population vector
Activity

Activity
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

Neuron Neuron
Is it possible to modulate the muscle spindles activity?

Muscle tendon vibration

 Spinal effect: the Tonic Vibration Reflex (TVR)

Surface recording
electrodes over the
wrist flexor and
extensor.
Cylindrical vibrator,
driven at 80-100 Hz
with displacements
of 1.0 to 2.0 mm by
an electric motor
connected to an
eccentric load,
placed on the volar
surface of the wrist
(vibration of the
flexor tendon).
 flessori mano dx
150.000

uVolts
The Tonic Vibration Reflex (TVR) 100.000
50.0000
0.00000
mano dx
150.000

uVolts
100.000
estensori
dxdx

50.0000
0.00000
flessori mano

150.000

uVoltsuVolts
dx avambraccio

100.000
150.000
50.0000
200 µV Wrist flexor
0.00000
100.000
dx

50.0000
mano

150.000
flessori
dx

0.00000

uVolts
avambraccio
dx mano

100.000
150.000
estensori

uVolts
100.000
150.000
50.0000

uVolts
flessori

50.0000
0.00000
100.000
Wrist extensor
0.00000
y avambraccio
mano dx

50.0000
estensori

150.000
150.000

uVolts
0.00000

uVoltsuVolts
100.000
100.000
13417.2
estensori

50.0000
dx dx
flessori

50.0000
8944.84
0.00000
acc
avambraccio

0.00000
4472.42
dx avambraccio

150.000
0.00000
150.000

uVolts
uVolts
100.000
0.0000 30.000 60.000 90.000 100.000
seconds 50.0000
estensori

50.0000
0.00000
acc y flessori

0.00000
acc y estensori avambraccio

13417.2
150.000

uVolts
8944.84

uVolts
100.000
4472.42
0.00000 50.0000
Vibration
0.0000
of a muscle
30.000
tendon (80-100
60.000
Hz) produces
90.000
a reflex contraction,
0.00000

sustained throughout the period of vibration, called Tonic Vibration

seconds 13417.2
Reflex

uVolts
8944.84
(TVR). 4472.42
0.00000
0.0000 30.000 60.000 90.000
seconds
 flessori mano dx

150.000

uVolts
100.000

50.0000

Wrist
0.00000 flexor
estensori mano dx

150.000

uVolts
100.000

50.0000

Wrist
0.00000extensor

16800.8

uVolts
acc y

8400.42

0.00000

-8400.42
0.0000 30.000 60.000 90.000
seconds
Vibration of the agonist muscle (wrist flexor) induces the TVR in the vibrated
muscle; furthermore, the vibration is able to suppress the voluntary tonic EMG
activity in the antagonist muscle (extensor carpi) (reciprocal inhibition).
The neural pathway
of the TVR is
represented by the
monosynaptic reflex
arc.

TVR is strongly influenced by cerebral structures

Central effect
Ascending somatosensory paths:
(A) Organization of the dorsal
column medial lemniscal system
from entry of large-diameter
afferents into the spinal cord to
the termination of thalamocortical
axons in the primary
somatosensory area of the
cerebral cortex.
(B) Organization of the spinothalamic
tract and the remainder of the
anterolateral system. Primary axons
terminate the spinal cord itself.
Second-order axons cross the
midline and ascend through the
spinal cord and brain stem to
terminate in VPL and other nuclei of
the thalamus. Collaterals of these
axons terminate in the reticular
formation of the pons and medulla.
All relevant information reaches
the ventrobasal complex and
most is relayed to the areas of SI.
From there, by steps through SII
and the posterior parietal areas,
somatosensory information
reaches
(1) the motor system (primary
and supplementary motor cortex),
where the continuous sensory
feedback onto motor system
occurs;
(2) the polysensory association
cortex in the superior temporal
gyrus, in which creation of a
complete and abstract sensory
map of the external world is
thought to occur;
(3) the limbic system (e.g.,
entorhinal cortex and
hippocampus, amygdala).
Secondary & Association Somatosensory Cortex
•Secondary somatosensory cortex -
bilateral info (both sides of the body)
•Damage = complex effects;
•Asterognosia – inability to recognize
objects by touch
•Asomatognosia – the failure to
recognize parts of one’s own body

• Parietal lobe = association cortex:

– Apraxia=difficulty making specific
movements when requested to do
so
– Contralateral neglect =inability to
respond to stimuli on one side of
the body opposite the lesion
 Proprioceptive illusions induced by muscle tendon vibration (MTV)

Goodwin GM, McCloskey DI, Matthews PB. Proprioceptive

illusions induced by muscle vibration: contribution by muscle
spindles to perception? Science. 1972;175:1382-4.
 Movement illusions induced by MTV:
the neural correlates
Activation of pre/motor areas, Activation of pre/motor areas and
and primary somatosensory area associative parietal areas

Naito E, Ehrsson HH, Geyer S, Zilles K, Roland PE (1999)

Illusory arm movements activate cortical motor areas: a positron
emission tomography study. J Neurosci 19:6134–6144.
Romaiguère P, Anton J-L, Roth M, Casini L, Roll J-P (2003)
Naito E, Ehrsson HH (2001) Kinesthetic illusion of wrist
Motor and parietal cortical areas both underlie kinaesthesia.
movement activates motor-related areas.Neuroreport 12:3805–
Cogn Brain Res 16:74–82.
3809.
How is important the proprioception in motor control?
Neuroplasticity

Neuroplasticity can be defined as the intrinsic ability of the

brain to change itself in response to experience through the
functional and/or structural reorganization of its neuronal
connections.
Neuroplasticity occurs during brain and behaviour
development, motor learning, and also after brain damage.
The reorganization of neuronal connections in the brain can
be either beneficial or detrimental to behavioral functions.
When brain changes are associated with improvements in
behavioural capacity, neural plasticity is referred to as
adaptive. On the other hand, when changes are linked to
behavioural deterioration or adverse consequences to the
individual, neural plasticity is referred to as maladaptive.
Neural Plasticity

Primary motor cortex (M1) can exhibit considerable plasticity due to:

i) everyday experience, including motor skill learning and cognitive motor actions (i.e.,
limb use and overuse)

ii) pathological or traumatic changes (i.e., limb disuse)

Cortical motor representation
The representation of a particular body part in the motor cortex may be
thought of as a reflection of the individual’s motor capacity with that body
part.
Non-invasive brain stimulation

Barker et al., 1985

Transcranial Magnetic Stimulation (TMS)
 Transcranial Magnetic Stimulation

TMS is a non invasive neurophysiological

technique that allows to:

1. study both conductivity and excitability of the

corticospinal system in humans

2. study plasticity of M1

3. modulate excitability and plasticity

 Motor Evoked Potential (MEP) size

MEP size
• is a measure of the portion of the spinal motoneurones
discharged by TMS and of its synchronization

EMG signal of the target muscle

 MEP Size

• Is a function of the
intensity of stimulation

• Should be referred to the

whole motoneuronal pool
(M wave)

• Is negatively influenced
by GABA-A agonists
 Input-Output (IO) curve or recruitment
curve
• The increase in motor output that occurs with
increasing intensity of stimulation

• A measure of the distribution of excitability in the

corticospinal system
+
excitability

- excitability
 MEP latency

MEP latency: MEP onset (expressed in milliseconds) is a rough

measure of the conduction of descending impulses
 Central Motor Conduction Time

Time taken by impulses, following activation of pyramidal neurons in the

cortex, to travel along the central pathways
Motor maps
Short-term immobilization protocols on
healthy subjects (6 ÷ 12 hours)
 1° DAY 2° DAY
6 pm: PRE 8 am-6 pm:NON-USE 6 pm: POST
FDI
AG AF CG FR GP IO LC
SB
PR
E
POS
T
 Structural plasticity

10 right-handed
subjects with
injury of the
right upper
extremity that
required at least
14 days of limb
immobilization.
Short-term upper limb disuse can induce platic modifications in the
contralateral and ipsilateral primary motor cortices resulting in an
hemispheric unbalance.
Experimental protocol

Avanzino L, Pelosin E, Abbruzzese G, Bassolino M, Pozzo T, Bove M. Shaping Motor Cortex

Plasticity Through Proprioception. Cereb Cortex. 2014;24:2807-14.
Results
We found that the muscle vibration of the right immobilized
arm was able to cope with neuroplastic changes induced
by limb disuse:
i. reducing the inhibitory effect on left M1 excitability
ii. re-establishing the correct transcallosal control from left
to right M1
iii. preventing the excitability increase of the corticospinal
and transcallosal neurons of right M1 due to left arm
overuse
 Technoconcept – Vibramoov

https://www.youtube.com/watch?v=CM7JWYJUZ30

https://www.youtube.com/watch?v=ulNnPF8xTL4

https://technoconcept.com/vibramoov/