Sensory gating impairment in development of post-concussive symptoms in mild head injury

Article (PDF Available)inPsychiatry and Clinical Neurosciences 59(4):466-72 · September 2005with 124 Reads 
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DOI: 10.1111/j.1440-1819.2005.01400.x · Source: PubMed
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Abstract
Post-concussive symptoms reported by mild head injury (MHI) patients have been inadequately understood. Post-concussive symptoms reported by patients with MHI have so far been explained in terms of impairment in neurocognitive functions or deficits in modulation of flow of information. There are no studies that have looked into sensory gating impairment in MHI and its relation to post-concussive symptoms. The purpose of the present paper was to investigate the role of sensory gating impairment in post-concussive symptoms in mild head injury patients. Thirty MHI patients were evaluated for their neuropsychological functions, sensory gating deficits, and post-concussive symptoms. Neuropsychological functions were in the domain of attention, executive functions, and learning and memory. Sensory gating was assessed by Structured Interview for Assessing Perceptual Anomalies and post-concussive symptoms were assessed using the Neurobehavioral Rating Scale. Multiple regression method was used to identify predictors for post-concussive symptoms. Post-concussive symptoms were predicted by sensory gating deficits when sensory gating deficit was one of the predictors along with neuropsychological functions. Post-concussive symptoms were predicted by scores of Digit Vigilance and Digit Symbol Substitution Test, when predictors were restricted to neuropsychological functions. Sensory gating deficits were correlated with performance on Digit Symbol Substitution test. Post-concussive symptoms reported by MHI patients are the result of poor modulation of incoming sensory information.
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  • ... In contrast, when task demands deem one of two or more simultaneously presented stimuli to be task-irrelevant, the irrelevant stimulus is often suppressed or filtered out of the processing stream. This is known as sensory gating, a term which refers to the inhibition of sensory information as it travels from the periphery to the cortex [10][11][12]. Gating is thought to protect higher cortical centres from being overcome with irrelevant incoming information [12], and can occur via multiple mechanisms. For example, bottom-up gating can occur during active or passive movement [13][14][15][16][17][18]. ...
    ... This is known as sensory gating, a term which refers to the inhibition of sensory information as it travels from the periphery to the cortex [10][11][12]. Gating is thought to protect higher cortical centres from being overcome with irrelevant incoming information [12], and can occur via multiple mechanisms. For example, bottom-up gating can occur during active or passive movement [13][14][15][16][17][18]. ...
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    While there is evidence to show early enhancement of modality-specific somatosensory cortical event-related potentials (ERP) when two stimuli are task-relevant, less is understood about the cortical and behavioural correlates of early modality-specific sensory gating. This study sought to understand how attentional gating affects cortical processing of visual and tactile stimuli at early stages of modality-specific representation. Specifically, alterations in early somatosensory and visual processing based on attentional relevance were examined, along with the effect of an unattended sensory stimulus on cortical processing and behavioural performance. Electroencephalography (EEG) was collected from healthy participants as they performed a sensory selection task. This task required participants to make a scaled motor response to the amplitudes of visual and tactile stimuli presented individually or concurrently. Results showed that the somatosensory N70 ERP was significantly attenuated when tactile stimuli were unattended. When visual stimuli were unattended, modulation of visual potentials occurred later, at the visual P2 potential. Since unattended tactile stimuli were gated at early cortical processing stages, when they were used as distractors, no changes in cortical responses to target stimuli were observed. Additionally, there was no decrease in task accuracy when grading attended stimuli in the presence of a tactile distractor. However, since early gating was not observed in the visual modality, a visual stimulus used as an unattended distractor resulted in smaller-amplitude cortical responses to attended tactile stimuli and less accurate task performance when grading attended stimuli. In conclusion, this study suggests that early gating of unattended stimuli supports modality-specific cortical processing of target stimuli and maintains behavioural task performance.
  • ... Modulating cortical excitability based on a stimulus' relevance to the task at hand is a component of sensory gating, and serves to protect higher cortical centers from being overwhelmed with irrelevant information (McIlroy et al., 2003;Kumar et al., 2005;Wasaka et al., 2005). This study examined relevancy-based modulation of cortical excitability, and corresponding behavioral responses, in the face of distracting stimuli in participants with and without a history of concussion (mean age 22 ± 3 SD years; most recent concussion 39.1 ± 30 SD months). ...
    ... We are surrounded by multiple competing stimuli at all times during daily life, but not all stimuli need to elicit equivalent cortical responses. Sensory gating is the process by which the transmission of sensory information from the periphery to the cortex can be modulated to prevent overwhelming higher cortical centers with irrelevant information (McIlroy et al., 2003;Kumar et al., 2005;Wasaka et al., 2005). The relevance of a stimulus to the task at hand is a contributor to how the stimulus is processed, with more relevant stimuli eliciting more robust cortical responses. ...
    Article
    Full-text available
    Modulating cortical excitability based on a stimulus’ relevance to the task at hand is a component of sensory gating, and serves to protect higher cortical centers from being overwhelmed with irrelevant information (McIlroy et al., 2003; Kumar et al., 2005; Wasaka et al., 2005). This study examined relevancy-based modulation of cortical excitability, and corresponding behavioral responses, in the face of distracting stimuli in participants with and without a history of concussion (mean age 22 ± 3 SD years; most recent concussion 39.1 ± 30 SD months). Participants were required to make a scaled motor response to the amplitudes of visual and tactile stimuli presented individually or concurrently. Task relevance was manipulated, and stimuli were occasionally presented with irrelevant distractors. Electroencephalography (EEG) and task accuracy data were collected from participants with and without a history of concussion. The somatosensory-evoked N70 event-related potential (ERP) was significantly modulated by task relevance in the control group but not in those with a history of concussion, and there was a significantly greater cost to task accuracy in the concussion history group when relevant stimuli were presented with an irrelevant distractor. This study demonstrated that relevancy-based modulation of electrophysiological responses and behavioral correlates of sensory gating differ in people with and without a history of concussion, even after patients were symptom-free and considered recovered from their injuries.
  • ... Similarly, an NPC may reduce an individual's ability to respond to undifferentiated stimuli, such as those experienced during casual leisure occupations (Arciniegas et al., 1999). This undifferentiated stimulation influences cognition, attention, memory, sensory motor functioning, and processing capacity (Kumar et al., 2005). Howell (1999) suggested that a combination of the environment and a health condition could overload or deprive an individual of sensory stimulation. ...
    ... Other research conducted into the effects of sensory gating deficits has included many NPCs, such as Huntington's disease (Uc, Skinner, Rodnitzky, & Garcia-Rill, 2003), multiple sclerosis, Parkinson's disease (McCarley et al., 1997), and head injury (Kumar et al., 2005). ...
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    Background: This article explores whether engagement with listening occupations varies depending on the occupational role or the level of sensory stimulation presented to participants with neuropalliative conditions. Method: The study used a multiple case quasi-experimental study involving marginal-participant time-sampled observations of engagement of individuals with neuropalliative conditions, with casual leisure occupations using the Individual Child Engagement Record. Data was collected using the Individual Child Engagement Record with 14 participants (who had Barthel scores averaging 7/100). The participants represented a particular sub-group of individuals with profound levels of neurological disability. Results: The time-sampled observations of engagement showed a significant difference between the scores for the control condition, engagement in a potentially active role at a music-making group, and engagement in a passive audience role when listening to an audio recording. Therefore, passively listening to an audio recording appears to be less engaging than the potentially active role offered by the music-making group for participants with neuropalliative conditions. Conclusion: The small sample size and the use of a single observer without video recording backup compromised the reliability of the data while complying with the facility’s POVA policy. Switching on an auditory recording or broadcast, while easy to arrange, may not be sufficiently engaging to prevent boredom and occupational deprivation. Consideration of an individual’s sensory, support, and role preference should be undertaken when designing leisure occupations for individuals with neuropalliative conditions rather than simply switching on an audio recording or broadcast.
  • ... 9 Postconcussive symptoms usually resolve over a period of several days 10 ; however, a subgroup of patients experience continuous postconcussive difficulties and neuropsychological deficits that can persist for months or even years. [11][12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28] The diagnosis of mTBI is typically based on subjective clinical measures (i.e., symptom checklists). 29 However, these measures lack objectivity, and decisions based upon them are questionable. ...
    ... This channel showed significant differences between groups, in particular between concussed groups with PCS and with minor symptoms. A significant negative correlation was found for the symptom severity score and brain oxygenation during the visual memory task (r (25) = 20.443, p,0.05; Figure 6). ...
    Article
    Full-text available
    Diagnostic methods are considered a major concern in the determination of mild traumatic brain injury. The authors examined brain oxygenation patterns in subjects with severe and minor persistent postconcussive difficulties and a healthy control group during working memory tasks in prefrontal brain regions using functional near-infrared spectroscopy. The results demonstrated decreased working memory performances among concussed subjects with severe postconcussive symptoms that were accompanied by decreased brain oxygenation patterns. An association appears to exist between decreased brain oxygenation, poor performance of working memory tasks, and increased symptom severity scores in subjects suffering from persistent postconcussive symptoms.
  • ... It would be a challenge to go about your daily life and accomplish even the most mundane tasks. We avoid this overload situation by means of sensory gating, the inhibition of incoming sensory information traveling from the periphery to the cortex, thought to protect higher cortical centers from being overwhelmed with irrelevant information (Kumar et al. 2005;McIlroy et al. 2003;Wasaka et al. 2005). ...
    Article
    Full-text available
    Patients with lesions of the prefrontal cortex (PFC) show increased distractibility and impairments in inhibiting cortical responses to irrelevant stimuli. This study was designed to test the role of the PFC in the early modality-specific modulation of event-related potentials (ERPs) generated during a sensory selection task. The task required participants to make a scaled motor response to the amplitudes of visual and tactile stimuli presented individually or concurrently. Task relevance was manipulated and continuous theta burst stimulation (cTBS) was used to transiently inhibit PFC activity to test the contribution of the PFC to modulation of sensory gating. Electroencephalography (EEG) was collected from participants both before and after cTBS was applied. The somatosensory-evoked N70 ERP was shown to be modulated by task relevance before but not after cTBS was applied to the PFC, and downregulating PFC activity through the use of cTBS abolished any relevancy differences in N70 amplitude. In conclusion, this study demonstrated that early modality-specific changes in cortical somatosensory processing are modulated by attention, and that this effect is subserved by prefrontal cortical activity.
  • ... The mild traumatic brain injury group may potentially need special therapeutic adjustments to maximize visual rehabilitation. For example, patients with a history of mild traumatic brain injury often exhibit sensory-gating deficits, 12 increased visual sensitivity to motion, photosensitivity, and photophobia. 13,14 Vision therapy with such patients may include additional use of fusional prism spectacles (for diplopia), tinted spectacles (for photosensitivity), and yoked prism spectacles (for visual-spatial hemispheric inattention with or without a manifest visual field defect). ...
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    Purpose We investigated whether differences in the pattern visual evoked potentials exist between patients with convergence insufficiency and those with convergence insufficiency and a history of concussion using stimuli designed to differentiate between magnocellular (transient) and parvocellular (sustained) neural pathways. Methods Sustained stimuli included 2-rev/s, 85% contrast checkerboard patterns of 1- and 2-degree check sizes, whereas transient stimuli comprised 4-rev/s, 10% contrast vertical sinusoidal gratings with column width of 0.25 and 0.50 cycles/degree. We tested two models: an a priori clinical model based on an assumption of at least a minimal (beyond instrumentation’s margin of error) 2-millisecond lag of transient response latencies behind sustained response latencies in concussed patients and a statistical model derived from the sample data. Results Both models discriminated between concussed and nonconcussed groups significantly above chance (with 76% and 86% accuracy, respectively). In the statistical model, patients with mean vertical sinusoidal grating response latencies greater than 119 milliseconds to 0.25-cycle/degree stimuli (or mean vertical sinusoidal latencies >113 milliseconds to 0.50-cycle/degree stimuli) and mean vertical sinusoidal grating amplitudes of less than 14.75 mV to 0.50-cycle/degree stimuli were classified as having had a history of concussion. The resultant receiver operating characteristic curve for this model had excellent discrimination between the concussed and nonconcussed (area under the curve = 0.857; P < .01) groups with sensitivity of 0.92 and specificity of 0.80. Conclusions The results suggest a promising electrophysiological approach to identifying individuals with convergence insufficiency and a history of concussion.
  • ... To date no studies have examined the neural basis (i.e., structural or functional) of neurosensory deficits (e.g., visual, auditory or vestibular symptoms) during the acute to semi-acute phase of mTBI despite suggestions that these deficits represent a major contributing factor for chronic post-concussive symptoms (Hoffer, 2015;Pogoda et al., 2012). Early non-invasive imaging work examining unisensory cortical functioning suggests gating deficits across the TBI spectrum (Arciniegas et al., 2000;Arciniegas and Topkoff, 2004), and that post-concussive symptoms result in part from sensory gating abnormalities (Kumar et al., 2005). SPECT (Stamatakis et al., 2002), PET (Kato et al., 2007;Nakashima et al., 2007) and fMRI (Kim et al., 2012) studies also indicate hypometabolism or hypoperfusion in unisensory cortex in severe TBI patients, providing additional evidence that cortical dysfunction may contribute to selfreported neurosensory symptoms. ...
    Article
    Mild traumatic brain injury patients (mTBI) frequently report symptoms of increased distractability and sensory disturbances during mutisensory stimulation. These common post-concussive symptoms could putatively result from dysfunction within the cognitive control network (CCN; top-down) or from unisensory cortex (bottom-up) itself. Functional magnetic resonance imaging (fMRI) and high-resolution structural data were therefore prospectively collected during a multisensory (audio-visual) cognitive control task from 46 mTBI patients within 3 weeks of injury and 46 matched healthy controls (HC), with a subset of participants returning at 4 months. Multisensory stimuli were presented at two frequencies to manipulate cognitive and perceptual load. Patients self-reported more cognitive, emotional, somatic, vestibular and visual symptoms relative to HC, which improved, but did not entirely resolve, over the 4 month follow-up period. There were no group differences in behavior or functional activation during cognitive control (incongruent – congruent trials). In contrast, patients exhibited abnormal activation within different regions of visual cortex that depended on whether attention was focused on auditory or visual information streams. Patients also exhibited increased activation within bilateral inferior parietal lobules during higher cognitive/perceptual loads, suggesting a compensatory mechanism to achieve similar levels of behavioral performance. Functional abnormalities within the visual cortex and inferior parietal lobules were only partially resolved at 4 months post-injury, suggesting that neural abnormalities may take longer to resolve than behavioral measures used in most clinical settings. In summary, current results indicate that abnormalities within unisensory cortex (particularly visual areas) following mTBI, which likely contribute to deficits commonly reported during multisensory stimulation. Hum Brain Mapp, 2015. © 2015 Wiley Periodicals, Inc.
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    Objective: Jockeys have high rates of concussion, with 5% of jockeys receiving at least one concussion annually. The impact of acute concussion upon cognition is well understood, but less is known about the long-term effects of concussion upon cognition. Our aim was to assess the impact of concussion upon jockeys who had provided pre-concussion assessments of cognition using a prospective design. Method: In this study, over a 5-year period, we assessed the cognitive performance of jockeys with ≥1 medically diagnosed concussion (MDC; n = 17, months since concussion, M = 29.18), against those who had not been concussed (NC; n = 41). Jockeys who had not been concussed in the preceding 6 months completed four computer-based cognitive assessments from the CogSport battery. Results: Unlike the majority of the small existing literature, there was no difference (p ≥ .05) between the MDC and NC groups after controlling for age and baseline performance. Additionally, we used a measure of reliable change to assess for clinically meaningful decrements from baseline in each test and composite score 5 years later. None of the jockeys in the MDC group recorded significant decrements on any CogSport measure from baseline (z > -1.65). Conclusions: The findings suggest that the presence of concussion does not result in persistent decrements in cognitive performance and that when findings are considered collectively, assessing factors beyond medically diagnosed concussion (e.g., chronic stress, undiagnosed concussion) may improve the interpretation of our current findings.
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