Title: ProprioceptionRelated Evoked Potentials
1Proprioception-Related Evoked Potentials
2Objectives
- The objectives of this work are
- To introduce Proprioceptive Evoked Potentials
(PEPs) and their stimulation, recording, and
analysis techniques. - To discuss the differences between PEPs and
sensory evoked potentials (SEPs) that are
elicited by electrical nerve stimulation.
3What Are Proprioceptive Evoked Potentials?
- Proprioception is sensing the body,
- i.e. gathering information about
- The bodys position in space
- Active and passive movements
- Force that is applied by the body
- Such data is collected by receptors of the
somatosensory system, named proprioceptors, which
report on stretching of muscles and angles of
joints. For example, muscle spindles and Golgi
tendon organs are proprioceptors. - Due to independent studies of EPs related to
proprioception, a number of different terms have
emerged in this field
Arnfred et al., 2000 Bear et al., 2001
4Termination
- The most common terms are
- Proprioceptive Evoked Potentials (PEPs) are
potentials evoked by addition of weight to a hand
held load. Arnfred, et al., 2000 - Proprioceptive Event Related Potentials (PERPs)
are potentials evoked by a stimulation similar to
the former one, but with an oddball paradigm
Arnfred, 2005 - Proprioception-related evoked potentials are
potentials evoked by passive body movements
Seiss et al., 2002 - For convenience, the term Proprioceptive Evoked
Potentials (PEPs) will be used here to describe
all potentials evoked by stimulation of
proprioceptors, e.g. EPs evoked by active or
passive movements. Notice that this does not
include potentials evoked by electrical
stimulation.
5Example PEPs Related to Finger Movement
- Bötzel et al. 1997 studied potentials evoked by
finger movement in 11 healthy subjects. - Post-movement potentials were evoked by three
stimulation methods - The subject actively moved his right middle
finger to a given position (active movement). - The finger was passively stretched by a
technician that pulled a string that was tapped
to the finger (passive movement). The finger
was extended to the same position as in (1), in a
comparable velocity. - The median nerve was electrically stimulated,
- and the somatosensory evoked potentials
- (SEPs) were recorded.
6Example PEPs Related to Finger Movement
- During stimulation, EEG was recorded from the
scalp using the 10-20 system. - Source analysis was performed using
- the BESA program.
- Results
- The active and passive EPs were very similar, and
both included an N2/P2 complex at about 80ms
after stimulus onset (Fig. 1), with stronger P2
in the passive case. - In the SEPs, N20/P20 complex was identified (data
not shown).
Fig. 1. Thick line recording from electrode 3.
Thin line finger acceleration trace.
7Example PEPs Related to Finger Movement
- The dipoles of the N2/P2 and the N20/P20
complexes were attributed to the same area in the
contralateral hemisphere, but differed in dipole
orientation (Fig. 2) - SEPs N20/P20 dipole pointed anterior-medially.
- Active and passive N2/P2 dipoles pointed
posteriorly.
Fig. 2. Average dipole locations. Back - active
movement N2/P2 dipole. Light grey - passive
movement N2/P2 dipole. Dark grey - median nerve
SEP N20/P20 dipole. The angular part signals the
range of orientations of the positive dipoles
ends.
8Example PEPs Related to Finger Movement
- Discussion Because the EPs of the active and
passive stimuli were very similar, they must be
purely somatosensory (a motor component would
have appeared in the active condition only). - What is the origin of this somatosensory
information? - Cutaneous afferents and joint afferents are ruled
out because they usually do not report joint
position. - Golgi tendon organs are also not an option,
because they are not modulated by passive joint
movements. - Primary muscle spindle afferents of the forearm
are the best candidates. - By contrast, it has been established that the
median nerve SEPs originates in cutaneous and
joint receptors, and has very little contribution
from muscle spindles Seiss et al. 2003.
9Example PEPs Related to Finger Movement
- Conclusion The N2/P2 complex arises from
cerebral processing of proprioceptive information
sent from muscle spindles to the brain.
Therefore, the potentials elicited by passive and
active movements are PEPs. - Interestingly, the dipole analysis indicated that
the proprioceptive information arrives to S1.
This result will later be compared to those of
other researches.
10Example II PEPs Related to Wrist Movement
- Arnfred et al. 1999 studied potentials evoked
by a change of load that the subject held (Fig
3). -
- Stimulation linear increment of the load from
400g to 480g , in steps of 20g in 10ms. The
maximal load (480g) was maintained for 100ms. The
stimulus was described as carrying a basket of
apples when another apply is suddenly thrown into
it.
Fig. 3. Experimental set-up
- EEG was recorded from 10 right-handed subjects
using the 10-20 system
11Example II PEPs Related to Wrist Movement
- Results the major components of the EPs were
(Fig. 4) - Contralateral parietal waves P70\P190 at C3
- Frontal N70 wave at Fz
- P100 wave at Cz
- Discussion
- The pattern of very close frontal and parietal
activation with reverse polarities resembles the
PEPs of passive movements that were recorded by
Bötzel et al. their data is not shown, and is
significantly different from median nerve SEPs.
Fig. 4. Grand average of the EPs. Arrows mark
stimulus onset.
12Example II PEPs Related to Wrist Movement
- Moreover, the stimulus was perceived as applied
force, i.e. neither tactile nor passive movement. - Conclusion A brisk change of hand held load
elicits PEPs with intermediate latency. - In a later work, Arnfred 2005 studied the EPs
elicited by a similar method, using an oddball
paradigm. The subjects had to recognize the type
of stimulus (frequent 40g / rare 100g) and
count the oddball stimuli. - This study showed that P100 of the two stimuli
hardly differed, while later components were
influenced by the context. Since P100 is related
to specific processing in S2 cortex, the author
concluded that the proprioceptive stimulus is
processed within the first 100ms.
13Sensitivity of PEPs to Movement Parameters
- Seiss et al. 2002 studied the influence of
movement parameters on PEPs elicited by passive
movements. - Stimulation was performed by a robot that
imposed four types of passive finger movements
(Fig 5) - Extension to 15mm
- Extension to 25mm
- Flexion to 15mm
- Flexion to 25mm
- During stimulation, EEG was recorded
- using the 10-20 system. Additionally,
- the authors recorded median nerve
- SEPs elicited by electrical stimulation.
Fig. 5. The robot that imposed passive finger
movements. Seiss et al., 2003
14Sensitivity of PEPs to Movement Parameters
- Results
- All PEPs elicited by the four passive movement
stimuli were similar, with a frontal negative
wave measured at electrode FC1 at about 90ms
(denoted N90). - The four PEPs differed only in the wave duration
N90 was about 30ms longer for 25mm stimuli than
for 15mm stimuli. Movement direction did not
matter (Fig. 6). - This prolongation was roughly
- proportional to the difference
- between the movement durations.
- The SEP showed the well known
- N20/P20 pattern.
Fig. 6. PEP grand average. Solid line 15mm
stimulus, dashed line 25mm stimulus.
15Sensitivity of PEPs to Movement Parameters
- Source analysis yielded a single dipole for each
PEP. The dipoles were in close proximity, and
were anterior to the source of the SEP. - Moreover, the analysis showed that the PEPs are
generated in the motor cortex. - Conclusion
- The authors suggested the following longer
movements may give rise to contributions of other
neuronal populations to the PEP, which are not
revealed in PEPs elicited by short movements.
16Conclusion PEPs Features
- Several corollaries can be made from the
described studies - PEPs reflect the arrival and processing of
proprioceptive information at the cortex. - PEPs can be elicited by
- Active movements
- Passive movements
- Weight lifting
- Muscle stretching (which was not discussed here)
- However, electrical stimulation elicits SEPs, not
PEPs. - It has been recently suggested that the first
100ms of PEPs reflects processing of the
proprioceptive stimulus, and later components are
changed by the context.
17Conclusion PEPs Features
- The pattern of PEPs
- Comparing the described studies indicates that
PEPs are usually characterized by a frontal
negative component. The latency of this component
varies between different experiments, probably
due to differences in the stimulation techniques
and the body part that is moving. - Passive and active movements yield PEPs that are
very similar, both in latencies and in
amplitudes. - While a number of studies concluded that PEPs are
generated in the sensory cortex, a recent study
indicated that PEPs also have contributions from
the motor cortex.
18Comparison of PEPs and Electrically Evoked SEPs
- Origin PEPs reflect input from muscle spindle
afferents only. On the contrary, median nerve
SEPs reflect inputs from cutaneous afferents, as
well as negligible inputs from muscle spindle
afferents. Practically, it can be assumed that
PEPs and SEPS reflect different inputs Seiss et
al., 2003. - Pattern The primary component of PEPs has a
frontal-negative distribution, while the N20/P20
component of the median nerve SEP has a
parietal-negative/frontal-positive distribution. - Cortical generator N2/P2 components of PEPs are
generated in the sensorimotor cortrex, and their
source is 7-10 mm anterior to the source of
N20/P20 complex of the median nerve SEPs.
19The Benefit in PEPs Research
- Investigation of PEPs seems to hold promise in
two fields - Movement disorders. analysis of PEPs isolates
information about the proprioceptive feedback
that exists in the sensory-motor loop. Thus, PEPs
investigation may improve our understanding of
movement disorders such as Huntingtons disease
and Parkinsons disease. - Neuropsychiatric disorders. Since the perception
of myself is established on integration of
proprioceptive and sensory information, PEPs can
be utilized for investigating neuropsychiatric
disorders, e.g. schizophrenia.
Arnfred, 2005 Seiss et al., 2003
20References
- Arnfred, S., Chen, A. C., Eder, D., Glenthoj, B.,
Hemmingsen, R. (2000) Proprioceptive evoked
potentials in man cerebral responses to changing
weight loads on the hand. Neurosci Lett, 288,
111-4. - Arnfred, S. M. (2005). Proprioceptive event
related potentials gating and task effects. Clin
Neurophysiol, 116, 849-60. - Bear, M. F., Connors, B. W., Paradiso, M. A.
(2001) Neuroscience Exploring the brain.
Lippincott, Williams, Wilkins, Baltimore MD,
Chapter 13. - Bötzel, K., Eceker, C., Schulze, S. (1997)
Topography and dipole analysis of reafferent
electrical brain activity folllowing the
Breitschaftsponttial. Exp. Brain Res., 114,
352-361. - Seiss, E., Hesse, C.W., Drane, S., Oostenveld,
R., Wing, A.M., Praamstra, P., (2002)
Proprioception-related evoked potentials origin
and sensitivity to movement parameters.
Neuroimage, 17(1) 461-8. - Seiss, E., Praamstra, P., Hesse, C.W., Rickards,
H. (2003). Proprioceptive sensory function in
Parkinsons disease and Huntingtons disease
evidence from proprio-ception-related EEG
potentials. Exp. Brain Res., 148, 308-319.