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Changes in the P300 Component of the Tactile Event-Related Potential Following Spinal Cord Injury

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Changes in the P300 Component of the Tactile Event-Related Potential Following Spinal Cord Injury Paraplegia (1996) 34,107-112 © 19961nternalional Medical Society of Paraplegia All rights reserved 0031-1758/96 $12.00 Changes in the P300 component of the tactile event-related potential following spinal cord injury l 3 l l l MJ Cohen ,2, , PA Ament , SL Schandler ,4 and M Vulpe ,2 I 2 Department of Veterans Affairs Medical Center, Long Beach; Department of Neurology, University of California, Irvine; 3 Department of Psychiatry and Human Behavior, University of California, Irvine; and 4 Division of Psychology, Chapman University, Orange, California, U.S,A, Previous studies have demonstrated that significant changes in action or behaviour (function) and morphology occur in the deafferentated and the adjacent somatosensory cortex after amputation or experimental spinal cord injury, These studies have shown changes in somatotopic mappings and somatosensory perception as well as altered evoked responses, The purpose of the present study was to examine the potential effect of these changes on cognitive processes using the tactile P300 event-related potential (ERP) in a spinal cord injured (SCI) population. The P300 ERP has been associated with more complex cognitive functioning such as selective attention, memory, and stimulus evaluation rather than earlier sensory processing of stimuli. Three groups consisting of healthy control, paraplegic, and tetraplegic subjects participated in a transcutaneous electrical stimulation 'oddball' task. Results indicate that all groups were successful in maintaining target counts and produced significantly larger P300 amplitudes with longer latencies to target trials compared to non-target trials. The SCI groups, however, produced P300 ERPs for both targets and non-targets that were significantly reduced in amplitude compared to the control group. In the case of the tetraplegia patients, the P300 was almost abolished. No differences in latency of the P300 was observed between any of the groups. Keywords: spinal cord lllJunes; P300; event related potentials; somatosensory; cognition; paraplegia Introduction The central nervous system demonstrates significant less sensitivity compared to control subjects, particu­ plasticity to a variety of situations. Experiments larly in spine and neck areas. I I One possible showing changes in the cerebral cortex followin� interpretation of these results is that the reorganiza­ I peripheral injury, ,2 sustained peripheral stimulation, tion found in brain mapping studies may have learning,4,5 experimental amputation,6,7 or experimen­ functional perceptual and cognitive consequences in 8 9 l tal spinal cord injury in cats, , and in macaques O are the spinal cord injured. Obviously, there are other of particular importance for understanding which interpretations including reorganization at the spinal changes may occur in various brain regions, particu­ cord level. larly the somatosensory cortex, in spinal cord injured Surprisingly little is known, however, regarding the (SCI) humans. impact on perception and cognition after central We have attempted to assess the possible functional deafferentation in the SCI population. To measure components of the cortical changes following the loss attention-arousal mechanisms in paraplegic and of ascending sensory pathways from supraspinal tetraplegic humans, we manipulated intensity of centers (central deafferentation) due to spinal cord auditory and visual stimuli and measured the effect injury in humans. We have previously used standard on the event-related potential (ERP) measured at C3 1 psychophysical techniques to determine if paraplegic and C4. 2 Overall, the SCI groups had attenuated patients with and without chronic dysesthetic pain cortical responding compared to a control group. syndrome (DPS) would show perceptual changes to Though the paraplegic and tetraplegia groups did not tactile stimulation in intact somatic areas. The SCI significantly differ from each other, the tetraplegic pain patients exhibited more sensitivity to two-point group had a flatter ERP. The difference among groups discrimination tests (smaller distance between stimula­ was most evident in the NlOO-P200 component which tion points) while the SCI no-pain patients exhibited is hypothesized to reflect processing of the physical properties of the stimulus as well as selective attention 13 Correspondence: MJ Cohen processes. Changes in tactile P300 ERP after spinal cord injury MJ Cohen et al 108 The current study was designed to further examine inpatient and outpatient units in the spinal cord injury the extent of attenuated cortical ERP responding in wards and clinics of a major medical centre with a SCI humans and to assess the potential effects of ERP large spinal cord injury inpatient and outpatient attenuation on cognition, particularly selective atten­ population. Controls were recruited from staff and tion processes as related to processing somatosensory volunteers of the medical centre and the student stimuli. To achieve this, we used a tactile oddball populations of two nearby university campuses. paradigm to examine the later P300 component of the event-related potential in tetraplegic, paraplegic and Apparatus and recordings control groups while ERP measures were made at Fz, The EEG was recorded from Fz, Cz, and pz ' Cz and pz cortical locations. The P300 ERP is a (International 10-20 system 5) scalp sites from silver particularly robust endogenous element associated cup 10 mm electrodes and referenced to linked-earlobe with higher order cognitive processing, particularly AI-A2 sites using 7.5 mm Ag/AgCI electrodes. selective attention, resource allocation and processing Electrode impedances were maintained below 10 k speed.14 The oddball paradigm, during which the ohms. The electro-oculogram (EOG) was also re­ subject attends to a relatively infrequent target corded to identify eye movement artifact by position­ stimulus while ignoring a more frequently occurring ing 3 mm Ag/AgCI electrodes in an oblique non-target stimulus, is especially valuable for deter­ configuration with one electrode slightly inferior to mining functional (action or behaviour) cognitive the outer canthus and the other electrode positioned changes. To a large extent this paradigm examines supraorbitally, superior to the inner canthus of the cognitive stimulus evaluation processes that are non-dominant eye. Pairs of 7 mm Ag/AgCI electrodes separate and distinct from the normal perceptual were also attached to central forehead and ventral foot processing of the physical characteristics of the sites in order to record electrodermal (skin conduc­ stimulus. In healthy control populations, the P300 tance) responses although this data will not be reported ERP is of higher amplitude and longer latency in here. One of the skin conductance electrodes served as response to the target stimuli compared to the non­ subject ground. The EEG bandpass was set at 0.15-75 targets. However, the effects of altered somatosensory Hz and the EOG bandpass was set at 0.1-35 Hz perceptual processing due to SCI on the cognitive Transcutaneous tactile stimulation, just above evaluation of those stimuli are unknown. Since the threshold level, was delivered through two pairs of P300 reflects factors associated with cognitive evalua­ 32 mm diameter disk electrodes applied with adhesive tion rather than perceptual processing, it might be collars having 10 mm diameter skin contact areas expected that the spinal cord injured groups will using Soltm electrode cream. Pairs of electrodes were respond in a similar fashion to the control group. positioned approximately 3 cm to the left and right respectively of the midline of the dorsal neck area midway between the inion and the seventh cervical Methods process. In all cases the electrodes were positioned above the level of the sentient part of the lllJury. Subjects Stimulation was provided by a Grasstm model A total of 45 paid volunteers, four females and 41 SlODSCMA Constant Voltage Stimulator set to males, participated in this study and consisted of 15 deliver a 0.2 ms width square-wave pulse through the healthy controls, 15 with paraplegia, and 15 with SI lead. Pulses were directed through a Grasstm model tetraplegia. The paraplegic group consisted of eight SIU8 Stimulus Isolation Unit. The output of the individuals with complete spinal cord injuries (SCI). isolation unit was connected to computer controlled The level of injury for the paraplegic group ranged relays which then delivered the stimulus pulse to either from T-6 to L-4, and for the tetraplegic subjects ranged the right or left electrode pair positioned on the dorsal from C-2 to C-7 and nine had incomplete injuries while neck. The use of the dorsal neck stimulation site was six had complete injuries. Due to the nature of the necessary due to the fact that this site is the lowest tactile discrimination task, we did not select any somatic region with intact sensory function for the complete tetraplegic subject with an injury level above complete tetraplegia subjects selected for this study. C-4. Subjects ranged in age from 19 to 66 years, Very low-level transcutaneous stimulation (range 0.1 (M = 41.2, SD = 13.2). to 0.3 milliamperes) at this site was used to reduce the Subjects in all groups were matched for age and possibility of artifact contamination of the EEG, were screened for the absence of any history of loss of particularly at the pz site. There were no differences consciousness, head injury, seizures, mental illness, or in stimulus intensities among the groups. substance
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