proprioception-related evoked potentials presented by efrat barak

Proprioception-Related Proprioception-Related Evoked PotentialsEvoked Potentials

Presented byPresented by

Efrat BarakEfrat Barak

ObjectivesObjectives

The objectives of this work are:The objectives of this work are: To introduce Proprioceptive Evoked To introduce Proprioceptive Evoked

Potentials (PEPs) and their stimulation, Potentials (PEPs) and their stimulation, recording, and analysis techniques.recording, and analysis techniques.

To discuss the differences between To discuss the differences between PEPs and sensory evoked potentials PEPs and sensory evoked potentials (SEPs) that are elicited by electrical (SEPs) that are elicited by electrical nerve stimulation.nerve stimulation.

What Are Proprioceptive What Are Proprioceptive Evoked Potentials?Evoked Potentials?

Proprioception Proprioception is “sensing the body”, is “sensing the body”, i.e. gathering information about: i.e. gathering information about: The body’s position in spaceThe body’s position in space Active and passive movementsActive and passive movements Force that is applied by the body Force that is applied by the body

Such data is collected by receptors of the Such data is collected by receptors of the somatosensory system, named somatosensory system, named proprioceptors,proprioceptors, which report on stretching of muscles and angles which report on stretching of muscles and angles of joints. For example, muscle spindles and Golgi of joints. For example, muscle spindles and Golgi tendon organs are proprioceptors.tendon organs are proprioceptors.

Due to independent studies of EPs related to Due to independent studies of EPs related to proprioception, a number of different terms have proprioception, a number of different terms have emerged in this field:emerged in this field:[Arnfred et al., 2000; Bear et al., 2001][Arnfred et al., 2000; Bear et al., 2001]

TerminationTerminationThe most common terms are:The most common terms are: Proprioceptive Evoked PotentialsProprioceptive Evoked Potentials ( (PEPsPEPs) are ) are

potentials evoked by addition of weight to a hand held potentials evoked by addition of weight to a hand held load. [Arnfred, et al., 2000]load. [Arnfred, et al., 2000]

Proprioceptive Event Related PotentialsProprioceptive Event Related Potentials ( (PERPsPERPs) are ) are potentials evoked by a stimulation similar to the former potentials evoked by a stimulation similar to the former one, but with an oddball paradigm [Arnfred, 2005]one, but with an oddball paradigm [Arnfred, 2005]

Proprioception-related evoked potentialsProprioception-related evoked potentials are are potentials evoked by passive body movements [Seiss et potentials evoked by passive body movements [Seiss et al., 2002]al., 2002]

For convenience, the term Proprioceptive Evoked For convenience, the term Proprioceptive Evoked Potentials (Potentials (PEPPEPss)) will be used here to describe all will be used here to describe all potentials evoked by stimulation of proprioceptors, e.g. potentials evoked by stimulation of proprioceptors, e.g. EPs evoked by active or passive movements. EPs evoked by active or passive movements. Notice that Notice that this does not include potentials evoked by electrical this does not include potentials evoked by electrical stimulation.stimulation.

Example: PEPs Related to Example: PEPs Related to Finger MovementFinger Movement

Bötzel et al. [1997] studied potentials evoked by Bötzel et al. [1997] studied potentials evoked by finger movement in 11 healthy subjects. finger movement in 11 healthy subjects. Post-movement potentials were evoked by three Post-movement potentials were evoked by three stimulation methods:stimulation methods:

The subject actively moved his right middle The subject actively moved his right middle finger to a given position (finger to a given position (activeactive movement). movement).

The finger was passively stretched by a The finger was passively stretched by a technician that pulled a string that was tapped technician that pulled a string that was tapped to the finger (to the finger (passivepassive movement). The finger movement). The finger was extended to the same position as in (1), in was extended to the same position as in (1), in a comparable velocity. a comparable velocity.

The median nerve was electrically stimulated, The median nerve was electrically stimulated, and the somatosensory evoked potentialsand the somatosensory evoked potentials((SEPsSEPs) were recorded.) were recorded.


During stimulation, EEG was During stimulation, EEG was recorded from the scalp using recorded from the scalp using the 10-20 system.the 10-20 system.

Source analysis was performed Source analysis was performed using using the BESA program.the BESA program.

Results:Results: The active and passive EPs The active and passive EPs

were very similar, and both were very similar, and both included an N2/P2 complex at included an N2/P2 complex at about 80ms after stimulus onset about 80ms after stimulus onset (Fig. 1), with stronger P2 in the (Fig. 1), with stronger P2 in the passive case.passive case.

In the SEPs, N20/P20 complex In the SEPs, N20/P20 complex was identified (data not shown).was identified (data not shown).

Fig. 1. Thick line – Fig. 1. Thick line – recording from electrode recording from electrode 3. Thin line – finger 3. Thin line – finger acceleration trace. acceleration trace.


Fig. 2. Average dipole locations. Back - active Fig. 2. Average dipole locations. Back - active movement N2/P2 dipole. Light grey - passive movement N2/P2 dipole. Light grey - passive movement N2/P2 dipole. Dark grey - median nerve movement N2/P2 dipole. Dark grey - median nerve SEP N20/P20 dipole. The angular part signals the SEP N20/P20 dipole. The angular part signals the range of orientations of the positive dipoles ends. range of orientations of the positive dipoles ends.

The dipoles of the N2/P2 and The dipoles of the N2/P2 and the N20/P20 complexes were the N20/P20 complexes were attributed to the same area in attributed to the same area in the contralateral hemisphere, the contralateral hemisphere, but differed in dipole but differed in dipole orientation (Fig. 2): orientation (Fig. 2): SEPs N20/P20 dipole pointed SEPs N20/P20 dipole pointed

anterior-medially. anterior-medially. Active and passive N2/P2 Active and passive N2/P2

dipoles pointed posteriorlydipoles pointed posteriorly..


Discussion:Discussion: Because the EPs of the active and passive Because the EPs of the active and passive stimuli were very similar, they must be purely stimuli were very similar, they must be purely somatosensory (a motor component would have somatosensory (a motor component would have appeared in the active condition only). appeared in the active condition only). What is the origin of this somatosensory information?What is the origin of this somatosensory information? Cutaneous afferents and joint afferents are ruled out Cutaneous afferents and joint afferents are ruled out

because they usually do not report joint position.because they usually do not report joint position. Golgi tendon organs are also not an option, because Golgi tendon organs are also not an option, because

they are not modulated by passive joint movements.they are not modulated by passive joint movements. Primary muscle spindle afferents of the forearm are Primary muscle spindle afferents of the forearm are

the best candidates.the best candidates.By contrast, it has been established that the median By contrast, it has been established that the median

nerve SEPs originates in cutaneous and joint nerve SEPs originates in cutaneous and joint receptors, and has very little contribution from receptors, and has very little contribution from muscle spindles [Seiss et al. 2003].muscle spindles [Seiss et al. 2003].


Conclusion:Conclusion: The N2/P2 complex arises from The N2/P2 complex arises from cerebral processing of cerebral processing of proprioceptiveproprioceptive information sent from muscle spindles to the information sent from muscle spindles to the brain. brain. Therefore, the potentials elicited by Therefore, the potentials elicited by passive and active movements are PEPs.passive and active movements are PEPs.

Interestingly, the dipole analysis indicated that Interestingly, the dipole analysis indicated that the proprioceptive information arrives to S1. This the proprioceptive information arrives to S1. This result will later be compared to those of other result will later be compared to those of other researches.researches.

Example II: PEPs Related to Example II: PEPs Related to Wrist MovementWrist Movement

Arnfred et al. [1999] studied potentials evoked by a change of load that Arnfred et al. [1999] studied potentials evoked by a change of load that the subject held (Fig 3).the subject held (Fig 3).

Fig. 3. Experimental set-upFig. 3. Experimental set-up

Stimulation: linear increment Stimulation: linear increment of the load from 400g to 480g , of the load from 400g to 480g , in steps of 20g in 10ms. The in steps of 20g in 10ms. The maximal load (480g) was maximal load (480g) was maintained for 100ms. The maintained for 100ms. The stimulus was described as stimulus was described as ‘carrying a basket of apples ‘carrying a basket of apples when another apply is when another apply is suddenly thrown into it’.suddenly thrown into it’.

EEG was recorded from 10 right-handed EEG was recorded from 10 right-handed subjects using the 10-20 systemsubjects using the 10-20 system


Results:Results: the major components of the EPs were (Fig. 4): the major components of the EPs were (Fig. 4): Contralateral parietal waves P70\P190 at C3’Contralateral parietal waves P70\P190 at C3’ Frontal N70 wave at FzFrontal N70 wave at Fz P100 wave at CzP100 wave at Cz

Discussion:Discussion: The pattern of very close frontal and The pattern of very close frontal and

parietal activation with reverse parietal activation with reverse polarities resembles the PEPs of polarities resembles the PEPs of passive movements that were passive movements that were recorded by Bötzel et al. [their data recorded by Bötzel et al. [their data is not shown], and is significantly is not shown], and is significantly different from median nerve SEPs.different from median nerve SEPs. Fig. 4. Grand average of the EPs. Arrows mark Fig. 4. Grand average of the EPs. Arrows mark

stimulus onset.stimulus onset.


Moreover, the stimulus was perceived as applied Moreover, the stimulus was perceived as applied force, i.e. neither tactile nor passive movementforce, i.e. neither tactile nor passive movement..

Conclusion:Conclusion: A brisk change of hand held load elicits A brisk change of hand held load elicits PEPs with intermediate latency. PEPs with intermediate latency.

In a later work, Arnfred [2005] studied the EPs In a later work, Arnfred [2005] studied the EPs elicited by a similar method, using an oddball elicited by a similar method, using an oddball paradigm. paradigm. The subjects had to recognize the type of The subjects had to recognize the type of stimulus (frequent: +40g / rare: +100g) and count the stimulus (frequent: +40g / rare: +100g) and count the oddball stimuli. oddball stimuli. This study showed that P100 of the two stimuli hardly This study showed that P100 of the two stimuli hardly differed, while later components were influenced by differed, while later components were influenced by the context. Since P100 is related to specific the context. Since P100 is related to specific processing in S2 cortex, the author concluded that processing in S2 cortex, the author concluded that the the proprioceptive stimulus is processed within the first proprioceptive stimulus is processed within the first 100ms100ms..

Sensitivity of PEPs to Sensitivity of PEPs to Movement ParametersMovement Parameters

Seiss et al. [2002] studied the influence of Seiss et al. [2002] studied the influence of movement parameters on PEPs elicited by movement parameters on PEPs elicited by passive movements. passive movements. Stimulation was performed by a robot that imposed Stimulation was performed by a robot that imposed four types of passive finger movements (Fig 5): four types of passive finger movements (Fig 5): Extension to 15mmExtension to 15mm Extension to 25mm Extension to 25mm Flexion to 15mmFlexion to 15mm Flexion to 25mm Flexion to 25mm

During stimulation, EEG was recorded During stimulation, EEG was recorded using the 10-20 system. Additionally, using the 10-20 system. Additionally, the authors recorded median nerve the authors recorded median nerve SEPs elicited by electrical stimulation.SEPs elicited by electrical stimulation.

Fig. 5. The robot that Fig. 5. The robot that imposed passive imposed passive finger movements. finger movements. [Seiss et al., 2003][Seiss et al., 2003]


Results:Results: All PEPs elicited by the four passive movement All PEPs elicited by the four passive movement

stimuli were similar, with a frontal negative wave stimuli were similar, with a frontal negative wave measured at electrode FC1 at about 90ms measured at electrode FC1 at about 90ms (denoted N90).(denoted N90).

The four PEPs differed only in the wave duration: The four PEPs differed only in the wave duration: N90 was about 30ms longer for 25mm stimuli N90 was about 30ms longer for 25mm stimuli than for 15mm stimuli. Movement direction did than for 15mm stimuli. Movement direction did not matter (Fig. 6).not matter (Fig. 6).

This prolongation was roughly This prolongation was roughly proportional to the difference proportional to the difference between the movement durations. between the movement durations.

The SEP showed the well known The SEP showed the well known N20/P20 pattern.N20/P20 pattern.

Fig. 6. PEP grand average. Solid line – 15mm Fig. 6. PEP grand average. Solid line – 15mm stimulus, dashed line – 25mm stimulus. stimulus, dashed line – 25mm stimulus.


Source analysis yielded a single dipole for each Source analysis yielded a single dipole for each PEP. The dipoles were in close proximity, and PEP. The dipoles were in close proximity, and were anterior to the source of the SEP.were anterior to the source of the SEP.

Moreover, the analysis showed that the PEPs are Moreover, the analysis showed that the PEPs are generated in the motor cortex.generated in the motor cortex.

Conclusion:Conclusion:

The authors suggested the following: The authors suggested the following: longer longer movements may give rise to contributions of movements may give rise to contributions of other neuronal populations to the PEP, which are other neuronal populations to the PEP, which are not revealed in PEPs elicited by short not revealed in PEPs elicited by short movements. movements.

Conclusion: PEPs Conclusion: PEPs FeaturesFeatures

Several corollaries can be made from the described studies:Several corollaries can be made from the described studies: PEPs reflect the arrival and processing of proprioceptive PEPs reflect the arrival and processing of proprioceptive

information at the cortex.information at the cortex. PEPs can be elicited by:PEPs can be elicited by:

Active movementsActive movements Passive movementsPassive movements Weight liftingWeight lifting Muscle stretching (which was not discussed here)Muscle stretching (which was not discussed here)

However, electrical stimulation elicits SEPs, not PEPs. However, electrical stimulation elicits SEPs, not PEPs. It has been recently suggested that the first 100ms of It has been recently suggested that the first 100ms of

PEPs reflects processing of the proprioceptive stimulus, PEPs reflects processing of the proprioceptive stimulus, and later components are changed by the context.and later components are changed by the context.

Conclusion: PEPs Conclusion: PEPs FeaturesFeatures

The pattern of PEPs:The pattern of PEPs: Comparing the described studies indicates that PEPs Comparing the described studies indicates that PEPs

are usually characterized by a frontal negative are usually characterized by a frontal negative component. The latency of this component varies component. The latency of this component varies between different experiments, probably due to between different experiments, probably due to differences in the stimulation techniques and the differences in the stimulation techniques and the body part that is moving. body part that is moving.

Passive and active movements yield PEPs that are Passive and active movements yield PEPs that are very similar, both in latencies and in amplitudes.very similar, both in latencies and in amplitudes.

While a number of studies concluded that PEPs are While a number of studies concluded that PEPs are generated in the sensory cortex, a recent study generated in the sensory cortex, a recent study indicated that PEPs also have contributions from the indicated that PEPs also have contributions from the motor cortex. motor cortex.

Comparison of PEPs and Comparison of PEPs and Electrically Evoked SEPsElectrically Evoked SEPs

Origin:Origin: PEPs reflect input from muscle spindle afferents PEPs reflect input from muscle spindle afferents only. On the contrary, median nerve SEPs reflect inputs only. On the contrary, median nerve SEPs reflect inputs from cutaneous afferents, as well as negligible inputs from cutaneous afferents, as well as negligible inputs from muscle spindle afferents. Practically, it can be from muscle spindle afferents. Practically, it can be assumed that PEPs and SEPS reflect different inputs assumed that PEPs and SEPS reflect different inputs [Seiss et al., 2003].[Seiss et al., 2003].

Pattern:Pattern: The primary component of PEPs has a frontal- The primary component of PEPs has a frontal-negative distribution, while the N20/P20 component of negative distribution, while the N20/P20 component of the median nerve SEP has a parietal-negative/frontal-the median nerve SEP has a parietal-negative/frontal-positive distribution. positive distribution.

Cortical generator:Cortical generator: N2/P2 components of PEPs are N2/P2 components of PEPs are generated in the sensorimotor cortrex, and their source generated in the sensorimotor cortrex, and their source is 7-10 mm anterior to the source of N20/P20 complex of is 7-10 mm anterior to the source of N20/P20 complex of the median nerve SEPs.the median nerve SEPs.

The Benefit in PEPs The Benefit in PEPs ResearchResearch

Investigation of PEPs seems to hold promise in two Investigation of PEPs seems to hold promise in two fields:fields:

1.1. Movement disordersMovement disorders. analysis of PEPs isolates . analysis of PEPs isolates information about the proprioceptive feedback information about the proprioceptive feedback that exists in the sensory-motor loop. Thus, PEPs that exists in the sensory-motor loop. Thus, PEPs investigation may improve our understanding of investigation may improve our understanding of movement disorders such as Huntington’s movement disorders such as Huntington’s disease and Parkinson’s disease. disease and Parkinson’s disease.

2.2. Neuropsychiatric disordersNeuropsychiatric disorders. Since the perception . Since the perception of ‘myself’ is established on integration of of ‘myself’ is established on integration of proprioceptive and sensory information, PEPs proprioceptive and sensory information, PEPs can be utilized for investigating neuropsychiatric can be utilized for investigating neuropsychiatric disorders, e.g. schizophrenia. disorders, e.g. schizophrenia.

[Arnfred, 2005; Seiss et al., 2003][Arnfred, 2005; Seiss et al., 2003]

ReferencesReferences Arnfred, S., Chen, A. C., Eder, D., Glenthoj, B., Hemmingsen, R. Arnfred, S., Chen, A. C., Eder, D., Glenthoj, B., Hemmingsen, R.

(2000) Proprioceptive evoked potentials in man: cerebral (2000) Proprioceptive evoked potentials in man: cerebral responses to changing weight loads on the hand. responses to changing weight loads on the hand. Neurosci LettNeurosci Lett, , 288, 111-4.288, 111-4.

Arnfred, S. M. (2005). Proprioceptive event related potentials: Arnfred, S. M. (2005). Proprioceptive event related potentials: gating and task effects. gating and task effects. Clin NeurophysiolClin Neurophysiol, 116, 849-60., 116, 849-60.

Bear, M. F., Connors, B. W., Paradiso, M. A. (2001) Bear, M. F., Connors, B. W., Paradiso, M. A. (2001) Neuroscience: Neuroscience: Exploring theExploring the brain.brain. Lippincott, Williams, & Wilkins, Baltimore Lippincott, Williams, & Wilkins, Baltimore MD, Chapter 13. MD, Chapter 13.

Bötzel, K., Eceker, C., Schulze, S. (1997) Topography and dipole Bötzel, K., Eceker, C., Schulze, S. (1997) Topography and dipole analysis of reafferent electrical brain activity folllowing the analysis of reafferent electrical brain activity folllowing the Breitschaftsponttial. Breitschaftsponttial. Exp. Brain Res.,Exp. Brain Res., 114, 352-361. 114, 352-361.

Seiss, E., Hesse, C.W., Drane, S., Oostenveld, R., Wing, A.M., Seiss, E., Hesse, C.W., Drane, S., Oostenveld, R., Wing, A.M., Praamstra, P., (2002) Proprioception-related evoked potentials: Praamstra, P., (2002) Proprioception-related evoked potentials: origin and sensitivity to movement parameters. origin and sensitivity to movement parameters. NeuroimageNeuroimage, 17(1) , 17(1) 461-8. 461-8.

Seiss, E., Praamstra, P., Hesse, C.W., Rickards, H. (2003). Seiss, E., Praamstra, P., Hesse, C.W., Rickards, H. (2003). Proprioceptive sensory function in Parkinson’s disease and Proprioceptive sensory function in Parkinson’s disease and Huntington’s disease: evidence from proprio-ception-related EEG Huntington’s disease: evidence from proprio-ception-related EEG potentials. potentials. Exp. Brain Res.Exp. Brain Res., 148, 308-319., 148, 308-319.

proprioception-related evoked potentials presented by efrat barak

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