Accepted Manuscript Somatosensory evoked potentials show plastic changes following a novel motor training task with the thumb D. Andrew, H. Haavik, E. Dancey, P. Yielder, B. Murphy PII: DOI: Reference:
S1388-2457(14)00295-8 http://dx.doi.org/10.1016/j.clinph.2014.05.020 CLINPH 2007117
To appear in:
Clinical Neurophysiology
Accepted Date:
21 May 2014
Please cite this article as: Andrew, D., Haavik, H., Dancey, E., Yielder, P., Murphy, B., Somatosensory evoked potentials show plastic changes following a novel motor training task with the thumb, Clinical Neurophysiology (2014), doi: http://dx.doi.org/10.1016/j.clinph.2014.05.020
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Somatosensory evoked potentials show plastic changes following a novel motor training task with the thumb Andrew, D.1, Haavik, H.2, Dancey, E., Yielder, P.1, Murphy, B.1 1
University of Ontario Institute of Technology Faculty of Health Sciences 2000 Simcoe Street North Oshawa, Ont. L1H 7K4 Canada 2
New Zealand College of Chiropractic Centre for Chiropractic Research 6 Harrison Road Mt Wellington P.O. Box 112-044 Newmarket Auckland 1149 New Zealand
Corresponding author: Bernadette Murphy Faculty of Health Sciences University of Ontario Institute of Technology 2000 Simcoe Street North Oshawa, Ont. L1H 7K4 Canada Tel: +1-905-721-8668 ext 2778 Fax: +1-905-721-3179 E-mail: [email protected]
1
HIGHLIGHTS • Performance of novel motor tasks induces immediate changes in sensorimotor regions including cerebellar projections. • Early somatosensory evoked potentials demonstrate immediate changes following novel motor tasks, demonstrating their potential as neural markers of plasticity. • Understanding neural changes in a healthy population is critical to enhance our understanding of adaptive versus maladaptive plasticity responses in clinical populations.
ABSTRACT Objective: Accumulating evidence indicates that plastic changes can be maladaptive in nature, resulting in movement and neurological disorders. The aim of this study was to further the understanding of these neurophysiological changes in sensorimotor integration (SMI) using somatosensory evoked potentials (SEPs) and concurrent performance changes following a repetitive typing task. Methods: SEPs were recorded following median nerve stimulation at the wrist and performed pre and post intervention. 24 participants were randomly assigned to either an intervention group which performed a 20 minute repetitive typing task or a control group which participated in a 20 minute period of mental recitation. Results: The P22-N24 amplitude increased by 59.6%, compared to only 0.96% increase following the control. The P22-N30 SEP peak amplitude increased on average 13.4% following the motor training, compared to only 0.92% following the control. Significant improvement in reaction time when comparing performance of the motor task for the intervention group was observed.
2
Conclusions: The N24 increase supports the involvement of cerebellar connections and the N30 increase provides further support for changes in SMI following motor learning. Significance: Combining motor training tasks with electrophysiological techniques gives insight into the mechanisms of disordered SMI and whether the changes are adaptive or maladaptive.
KEYWORDS: Somatosensory evoked potentials (SEP); motor learning; sensorimotor integration (SMI); repetitive movement; cerebellum.
3
INTRODUCTION It is now well established that altered afferent input to the central nervous system (CNS) leads to plastic changes in the way that the CNS processes information (Pascual-Leone et al., 2005). These CNS alterations have been shown to persist following the period of altered input which induces organizational changes in both the primate and human cortex (Byl et al., 1997; Classen et al., 1998; Haavik Taylor and Murphy, 2007a, 2007b; Murphy et al., 2003). Only a few studies have used somatosensory evoked potentials (SEPs) to investigate the implications of repetitive muscular activity in humans (Haavik Taylor and Murphy, 2007a, 2007b; Classen et al., 1998). One of these studies has demonstrated changes in cortical somatosensory evoked potentials following the cessation of a repetitive typing task (Murphy et al., 2003). A primate study by Byl et al. (1997) determined that highly repetitive motor movements were associated with changes in the somatosensory cortex over a period of several weeks. These use dependent cortical changes have given rise to the concept that the homuncular maps of the body in the sensorimotor areas of the brain are quite flexible (Sanes and Donoghue, 2000). It is the continuous response to peripheral input that prompts these alterations in connectivity and strengths in synaptic connections. These alterations may trigger neurological and upper extremity disorders such as focal hand dystonia (Byl et al., 1997; Elbert et al., 1998) and carpal tunnel syndrome (Tinazzi et al., 1998). Input in the form of behavioural training has been shown to induce these organizational changes and the retention of such alterations reflects the reinforcement of sensorimotor skill acquisition or motor skill learning (Nelson et al., 2009). One way to evaluate these plastic changes which occur in the CNS is through the use of SEPs. SEPs are electrical field potentials generated by different neuronal substrates within the peripheral and central nervous systems induced by 4
physiological or electrical stimulation of somatosensory receptors and their axons (Angel et al., 1984; Mauguiere et al., 1999). The measurement of SEPs under various test conditions provides a refined technique for studying the relationships between electrical events and sensory processes (Angel et al., 1984). In this case specifically, by combining SEP protocols with motor learning paradigms, changes in neural processing resulting from motor learning can be investigated. Previous work has investigated the effects of a repetitive typing task on somatosensory afferent information utilized sequences which were relatively simple in nature. One such task involved the repetitive typing of the sequence of numbers “7, 8, 9” in ascending order (Haavik-Taylor and Murphy, 2007; Murphy et al., 2003). This work found that there were cortical changes observed following the learning task, however, subcortical changes were not seen (Haavik Taylor and Murphy, 2007). These authors found a reduction in intrinsic inhibition processing at the cortical level following the repetitive movement task. This may reflect a normal part of motor learning, however, in some susceptible individuals the persistence of the release of inhibition appears to lead to maladaptive plasticity (Haavik Taylor and Murphy, 2007). There is a growing interest in investigating the involvement of the cerebellum in motor learning (Desmond and Fiez, 1998), and it has recently been shown that early primary cortex processing, including cerebellar involvement, can be studied using SEPs (Haavik and Murphy, 2013). Through the utilization of dipole source analysis, the N24 SEP peak originates within the primary somatosensory cortex (S1) (Restuccia et al., 2001). It was also shown that in individuals with unilateral cerebellar lesions that there are significant decreases in amplitudes of only the N24 peak (Restuccia et al., 2001). This indicates that the cerebellum influences the early phases of somatosensory processing, thus making the N24 a potentially important component in investigating cerebellar influences on sensorimotor integration (Restuccia et al., 2001; Haavik 5
and Murphy, 2013). Several authors have demonstrated that when a faster stimulation rate is utilized, the N24 peak can be better differentiated from the N30 (Garcia Larrea et al., 1992; Haavik and Murphy, 2013). Additionally, Haavik and Murphy (2013) demonstrated increases in the N24 peak following repetitive motor training for a period of 20 minutes. Functional imaging studies have determined that there are differences in brain activity associated with areas of executive function in motor execution of simple, sequential movements and longer, more complex sequential tasks (Catalan et al., 1998; Sadato et al., 1996). After long periods of practice, almost any skill can be executed quickly, accurately and with little or no conscious deliberation. It is at this point that the behaviour is now referred to as automatic (Ashby and Crossley, 2012). The use of a simple task, such as the repetitive finger movements or simple sequences of pressing set keys, would allow the participants to develop a standardized pattern as the sequence that never changes. Furthermore, the involved numbers may be situated beside each other on the keyboard allowing for additional ease of performing the simple ordered sequence. Studies have shown that repetition of motor behaviour leads to a decrease in functional activation across all motor areas (Dassonville et al., 1998). The use of a more complex task in randomly generated sequences would provide a task which cannot be predicted. The current study utilizes such a task. Motor skill learning refers to the process by which movements are executed more accurately with practice (Dayan and Cohen, 2011). If we are inducing these cortical changes through means of behavioural input, an emphasis on behavioural aspects such as accuracy and reaction time is fundamental. Motor learning tasks results in changes in median nerve SEP peaks as has been demonstrated with the use of a three digit repetitive typing task (Murphy et al., 2003). This study involved typing with the 2nd-4th digits and stimulation of the median nerve at the wrist which conveys
6
afferent input primarily from the thumb, or the first digit. It therefore explores processing of information from afferents that predominantly were not involved in the task. This study sought to investigate somatosensory processing changes following a repetitive typing task using a thumb muscle, the abductor pollicis brevis (APB) by measuring changes in SEP peak amplitudes from stimulation of afferents originating in the muscle involved with the motor training task. Pre and post measures of motor performance were also included to determine if SEP changes were concomitant with improvements in performance. The prevalence of repetitive strain injuries (RSI) and occupational overuse injuries (OOI) have had a marked over the past few decades. According to the Canadian Community Health Survey, one out of every 10 Canadian adults suffers from an RSI or OOI serious enough to limit their normal daily activities (Statistics Canada, 2000). Internationally, reported upper-extremity disorder rates in the United States tripled between 1986 and 1993 while large increases in these disorders have also been documented within the UK, Australia, Norway, Sweden and Japan (Yassi, 1997). Impaired SMI may help in explaining the occurrence of workplace injuries following high levels of repetitive activity. Investigation of the complex circuitry that is involved in SMI with a focus on not only cortical but subcortical and cerebellar projections will give a better understanding of the mechanisms underlying adaptive and maladaptive plasticity subsequent to repetitive motor activity. This may ultimately enable better prevention and management of factors that lead to overuse injuries in workers.
METHODS
7
Subjects 24 participants with no known neurological conditions, comprised of 8 males and 16 females (mean age 23.2; range 18-34) participated in this study were randomly assigned either a motor task training session or a control session. Informed consent was obtained and the study was approved by the ethics committee at the University of Ontario Institute of Technology. This study was a pseudo-randomized experimental design. Stimulation Parameters The stimuli consisted of electrical pulses which were 1 ms in duration and delivered at rates of both 2.47Hz and 4.98 Hz through Ag/AgCl ECG conductive adhesive skin electrodes (MEDITRACE™ 130, Ludlow Technical Products Canada Ltd., Mansfield, MA) (impedance
S1388-2457(14)00295-8 http://dx.doi.org/10.1016/j.clinph.2014.05.020 CLINPH 2007117
To appear in:
Clinical Neurophysiology
Accepted Date:
21 May 2014
Please cite this article as: Andrew, D., Haavik, H., Dancey, E., Yielder, P., Murphy, B., Somatosensory evoked potentials show plastic changes following a novel motor training task with the thumb, Clinical Neurophysiology (2014), doi: http://dx.doi.org/10.1016/j.clinph.2014.05.020
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Somatosensory evoked potentials show plastic changes following a novel motor training task with the thumb Andrew, D.1, Haavik, H.2, Dancey, E., Yielder, P.1, Murphy, B.1 1
University of Ontario Institute of Technology Faculty of Health Sciences 2000 Simcoe Street North Oshawa, Ont. L1H 7K4 Canada 2
New Zealand College of Chiropractic Centre for Chiropractic Research 6 Harrison Road Mt Wellington P.O. Box 112-044 Newmarket Auckland 1149 New Zealand
Corresponding author: Bernadette Murphy Faculty of Health Sciences University of Ontario Institute of Technology 2000 Simcoe Street North Oshawa, Ont. L1H 7K4 Canada Tel: +1-905-721-8668 ext 2778 Fax: +1-905-721-3179 E-mail: [email protected]
1
HIGHLIGHTS • Performance of novel motor tasks induces immediate changes in sensorimotor regions including cerebellar projections. • Early somatosensory evoked potentials demonstrate immediate changes following novel motor tasks, demonstrating their potential as neural markers of plasticity. • Understanding neural changes in a healthy population is critical to enhance our understanding of adaptive versus maladaptive plasticity responses in clinical populations.
ABSTRACT Objective: Accumulating evidence indicates that plastic changes can be maladaptive in nature, resulting in movement and neurological disorders. The aim of this study was to further the understanding of these neurophysiological changes in sensorimotor integration (SMI) using somatosensory evoked potentials (SEPs) and concurrent performance changes following a repetitive typing task. Methods: SEPs were recorded following median nerve stimulation at the wrist and performed pre and post intervention. 24 participants were randomly assigned to either an intervention group which performed a 20 minute repetitive typing task or a control group which participated in a 20 minute period of mental recitation. Results: The P22-N24 amplitude increased by 59.6%, compared to only 0.96% increase following the control. The P22-N30 SEP peak amplitude increased on average 13.4% following the motor training, compared to only 0.92% following the control. Significant improvement in reaction time when comparing performance of the motor task for the intervention group was observed.
2
Conclusions: The N24 increase supports the involvement of cerebellar connections and the N30 increase provides further support for changes in SMI following motor learning. Significance: Combining motor training tasks with electrophysiological techniques gives insight into the mechanisms of disordered SMI and whether the changes are adaptive or maladaptive.
KEYWORDS: Somatosensory evoked potentials (SEP); motor learning; sensorimotor integration (SMI); repetitive movement; cerebellum.
3
INTRODUCTION It is now well established that altered afferent input to the central nervous system (CNS) leads to plastic changes in the way that the CNS processes information (Pascual-Leone et al., 2005). These CNS alterations have been shown to persist following the period of altered input which induces organizational changes in both the primate and human cortex (Byl et al., 1997; Classen et al., 1998; Haavik Taylor and Murphy, 2007a, 2007b; Murphy et al., 2003). Only a few studies have used somatosensory evoked potentials (SEPs) to investigate the implications of repetitive muscular activity in humans (Haavik Taylor and Murphy, 2007a, 2007b; Classen et al., 1998). One of these studies has demonstrated changes in cortical somatosensory evoked potentials following the cessation of a repetitive typing task (Murphy et al., 2003). A primate study by Byl et al. (1997) determined that highly repetitive motor movements were associated with changes in the somatosensory cortex over a period of several weeks. These use dependent cortical changes have given rise to the concept that the homuncular maps of the body in the sensorimotor areas of the brain are quite flexible (Sanes and Donoghue, 2000). It is the continuous response to peripheral input that prompts these alterations in connectivity and strengths in synaptic connections. These alterations may trigger neurological and upper extremity disorders such as focal hand dystonia (Byl et al., 1997; Elbert et al., 1998) and carpal tunnel syndrome (Tinazzi et al., 1998). Input in the form of behavioural training has been shown to induce these organizational changes and the retention of such alterations reflects the reinforcement of sensorimotor skill acquisition or motor skill learning (Nelson et al., 2009). One way to evaluate these plastic changes which occur in the CNS is through the use of SEPs. SEPs are electrical field potentials generated by different neuronal substrates within the peripheral and central nervous systems induced by 4
physiological or electrical stimulation of somatosensory receptors and their axons (Angel et al., 1984; Mauguiere et al., 1999). The measurement of SEPs under various test conditions provides a refined technique for studying the relationships between electrical events and sensory processes (Angel et al., 1984). In this case specifically, by combining SEP protocols with motor learning paradigms, changes in neural processing resulting from motor learning can be investigated. Previous work has investigated the effects of a repetitive typing task on somatosensory afferent information utilized sequences which were relatively simple in nature. One such task involved the repetitive typing of the sequence of numbers “7, 8, 9” in ascending order (Haavik-Taylor and Murphy, 2007; Murphy et al., 2003). This work found that there were cortical changes observed following the learning task, however, subcortical changes were not seen (Haavik Taylor and Murphy, 2007). These authors found a reduction in intrinsic inhibition processing at the cortical level following the repetitive movement task. This may reflect a normal part of motor learning, however, in some susceptible individuals the persistence of the release of inhibition appears to lead to maladaptive plasticity (Haavik Taylor and Murphy, 2007). There is a growing interest in investigating the involvement of the cerebellum in motor learning (Desmond and Fiez, 1998), and it has recently been shown that early primary cortex processing, including cerebellar involvement, can be studied using SEPs (Haavik and Murphy, 2013). Through the utilization of dipole source analysis, the N24 SEP peak originates within the primary somatosensory cortex (S1) (Restuccia et al., 2001). It was also shown that in individuals with unilateral cerebellar lesions that there are significant decreases in amplitudes of only the N24 peak (Restuccia et al., 2001). This indicates that the cerebellum influences the early phases of somatosensory processing, thus making the N24 a potentially important component in investigating cerebellar influences on sensorimotor integration (Restuccia et al., 2001; Haavik 5
and Murphy, 2013). Several authors have demonstrated that when a faster stimulation rate is utilized, the N24 peak can be better differentiated from the N30 (Garcia Larrea et al., 1992; Haavik and Murphy, 2013). Additionally, Haavik and Murphy (2013) demonstrated increases in the N24 peak following repetitive motor training for a period of 20 minutes. Functional imaging studies have determined that there are differences in brain activity associated with areas of executive function in motor execution of simple, sequential movements and longer, more complex sequential tasks (Catalan et al., 1998; Sadato et al., 1996). After long periods of practice, almost any skill can be executed quickly, accurately and with little or no conscious deliberation. It is at this point that the behaviour is now referred to as automatic (Ashby and Crossley, 2012). The use of a simple task, such as the repetitive finger movements or simple sequences of pressing set keys, would allow the participants to develop a standardized pattern as the sequence that never changes. Furthermore, the involved numbers may be situated beside each other on the keyboard allowing for additional ease of performing the simple ordered sequence. Studies have shown that repetition of motor behaviour leads to a decrease in functional activation across all motor areas (Dassonville et al., 1998). The use of a more complex task in randomly generated sequences would provide a task which cannot be predicted. The current study utilizes such a task. Motor skill learning refers to the process by which movements are executed more accurately with practice (Dayan and Cohen, 2011). If we are inducing these cortical changes through means of behavioural input, an emphasis on behavioural aspects such as accuracy and reaction time is fundamental. Motor learning tasks results in changes in median nerve SEP peaks as has been demonstrated with the use of a three digit repetitive typing task (Murphy et al., 2003). This study involved typing with the 2nd-4th digits and stimulation of the median nerve at the wrist which conveys
6
afferent input primarily from the thumb, or the first digit. It therefore explores processing of information from afferents that predominantly were not involved in the task. This study sought to investigate somatosensory processing changes following a repetitive typing task using a thumb muscle, the abductor pollicis brevis (APB) by measuring changes in SEP peak amplitudes from stimulation of afferents originating in the muscle involved with the motor training task. Pre and post measures of motor performance were also included to determine if SEP changes were concomitant with improvements in performance. The prevalence of repetitive strain injuries (RSI) and occupational overuse injuries (OOI) have had a marked over the past few decades. According to the Canadian Community Health Survey, one out of every 10 Canadian adults suffers from an RSI or OOI serious enough to limit their normal daily activities (Statistics Canada, 2000). Internationally, reported upper-extremity disorder rates in the United States tripled between 1986 and 1993 while large increases in these disorders have also been documented within the UK, Australia, Norway, Sweden and Japan (Yassi, 1997). Impaired SMI may help in explaining the occurrence of workplace injuries following high levels of repetitive activity. Investigation of the complex circuitry that is involved in SMI with a focus on not only cortical but subcortical and cerebellar projections will give a better understanding of the mechanisms underlying adaptive and maladaptive plasticity subsequent to repetitive motor activity. This may ultimately enable better prevention and management of factors that lead to overuse injuries in workers.
METHODS
7
Subjects 24 participants with no known neurological conditions, comprised of 8 males and 16 females (mean age 23.2; range 18-34) participated in this study were randomly assigned either a motor task training session or a control session. Informed consent was obtained and the study was approved by the ethics committee at the University of Ontario Institute of Technology. This study was a pseudo-randomized experimental design. Stimulation Parameters The stimuli consisted of electrical pulses which were 1 ms in duration and delivered at rates of both 2.47Hz and 4.98 Hz through Ag/AgCl ECG conductive adhesive skin electrodes (MEDITRACE™ 130, Ludlow Technical Products Canada Ltd., Mansfield, MA) (impedance
