Brain Injury, January 2013; 27(1): 41–47

Effect of binasal occlusion (BNO) on the visual-evoked potential(VEP) in mild traumatic brain injury (mTBI)

KENNETH J. CIUFFREDA, NAVEEN K. YADAV, & DIANA P. LUDLAM

Department of Biological and Vision Sciences, SUNY State College of Optometry, New York City, NY, USA

(Received 2 February 2012; revised 6 April 2012; accepted 30 May 2012)

AbstractPrimary objective: The purpose of the experiment was to assess the effect of binasal occlusion (BNO) on the visually-evokedpotential (VEP) in visually-normal (VN) individuals and in those with mild traumatic brain injury (mTBI) for whom BNOfrequently reduces their primary symptoms related to abnormally-increased visual motion sensitivity (VMS).Design and methods: Subjects were comprised of asymptomatic VN adults (n¼ 10) and individuals with mTBI (n¼ 10)having the symptom of VMS. Conventional full-field VEP testing was employed under two conditions: without BNO andwith opaque BNO which blocked regions on either side of the VEP test stimulus. Subjective impressions were also assessed.Results: In VN, the mean VEP amplitude decreased significantly with BNO in all subjects. In contrast, in mTBI, the meanVEP amplitude increased significantly with BNO in all subjects. Latency was normal and unaffected in all cases. RepeatVEP testing in three subjects from each group revealed similar test–re-test findings. Visuomotor activities improved, withreduced symptoms, with BNO in the mTBI group.Conclusions: It is speculated that individuals with mTBI habitually attempt to suppress visual information in the near retinalperiphery to reduce their abnormal VMS, with addition of the BNO negating the suppressive influence and thus producinga widespread disinhibition effect and resultant increase in VEP amplitude.

Keywords: Mild traumatic brain injury (mTBI), binasal occlusion, visual-evoked potential amplitude, visual-evoked potentiallatency, visual motion sensitivity, disinhibition

Introduction

Traumatic brain injury (TBI) is a major medicaland public health problem in the US [1]. It hasbecome heightened and more visible in recent yearsdue to the Iraq/Afghanistan conflicts [2]. This mayalso be attributed to the increased publicity relatedto sports-based concussions [3] and potentiallyrelated neurodegenerative disorders (e.g.Alzheimer’s, Parkinson’s) [4].

TBI occurs as a result of insult to the head andcontiguous regions, with the resultant forces trans-ferred to the underlying brain structures. It produceswidespread brain damage due to the initial and

immediate biomechanical effects (e.g. coup–countrecoup, shearing, diffuse axonal injury, etc.)and later the slower-acting biomolecular/cellularmechanisms, with the latter correlated to recovery[5]. Due to its global and pervasive nature, TBIwill result in a constellation of adverse effects ofa sensory, motor, perceptual, cognitive, linguistic,attentional and/or behavioural nature [6].

Since seven of the 12 cranial nerves are involvedin vision, as well as at least 30 distinct cortical areasof the brain [7], it is not surprising that adversevisual consequences frequently occur following aTBI (e.g. photosensitivity, oculomotor problems,

Correspondence: SUNY State College of Optometry, Department of Biological and Vision Sciences, 33 West 42nd Street, New York City, NY 10036, USA.Tel: 212-938-5765. Fax: 212-938-5760. E-mail: kciuffreda@sunyopt.edu

ISSN 0269–9052 print/ISSN 1362–301X online � 2013 Informa UK Ltd.DOI: 10.3109/02699052.2012.700088

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etc.) [7–9]. One of the most common and debilitat-ing, yet poorly understood, visual sequelae of TBIis ‘increased visual motion sensitivity’ (VMS) [10].That is, the presence of naturally-occurring visualmotion in the visual-field will have adverse physio-logical and perceptual effects in some individualswith TBI. They may report nausea, vertigo, unstead-iness, balance difficulties, disorientation and a senseof visual confusion/chaos [11]. These specific symp-toms have been referred to as the visual-vertigosyndrome [12], as well as the ‘supermarket syn-drome’, because such busy and globally encompass-ing visual environments readily provoke the abovesymptoms.

Three primary techniques have been used toreduce the intensity of the symptomatic increasedvisual motion sensitivity in TBI [11]. The first hasbeen the use of spectacle lens tints to reduce theluminous intensity of the disturbing visual object(s)or areas of the visual-field, thus reducing its visibility,and hence its effectiveness as a provocative stimulus.The second has been desensitization maneouvres,in which visual motion is purposely introduced intothe near and far peripheral visual field, for examplewith the therapist’s hand or a slowly-rotating opto-kinetic drum, with the goal of producing gradualhabituation and reduced perceived intensity to theiatrogenically-induced symptomatic visual motion.The third and last is binasal occlusion (BNO).Here either translucent or preferably opaque nasally-placed and superior temporally-angled partial occlu-ders are adhered to each spectacle lens. BNOprovides immediate and frequently full relief fromthe disturbing visual motion in the visual fieldin a sub-set of individuals with mTBI [13–15].The occluders block a region of visual space in thenear retinal periphery contralateral to the occludereye placement. The mechanism has been unclear,although some have speculated on general suppres-sive and/or central/peripheral visual-field interac-tions [13–15].

There has only been one formal research investi-gation specifically dealing with the effect of BNOin TBI on the VEP. Padula et al. [15] used theobjectively-based, visual-evoked potential (VEP) toassess immediate changes in cortical occipital brainresponsivity to binasal occluders in adult patientswith TBI (n¼10), as well as in adult visually-normalcontrol subjects (n¼10). In the former, with theaddition of the BNO, the VEP amplitude increasedin eight of the individuals with TBI, on averagechanging from 6.35 to 7.99 mV, which represented astatistically significant change. There was a concur-rent reduction of symptoms (e.g. visual instability) insome of these subjects. In the non-TBI, visually-normal controls, the VEP amplitude decreased in sixon average by 0.97mV, increased in two on average

by 0.88 mV and remained exactly the same in two,thus suggesting a small random statistical ‘noisephenomenon’. No subjective assessment was per-formed in the normals. Lastly, latency was notassessed in their study. However, the Padula et al.[15] experiment did not differentiate the base-inprism vs BNO effects on the VEP. Padula et al. [15]suggested that a future experiment should be con-ducted to disambiguate the findings; that is, testingshould be conducted with BNO only in place in bothpopulations.

The hypothesis of the present study is that therewill be an increase in the VEP amplitude, with littleif any change in latency, with BNO in the mTBIpopulation due to presumed reduction in attemptedchronic visual inhibition/suppression effects in thenear retinal periphery.

Thus, the purpose of the present experiment wasto assess objectively the effect of binasal occludersalone on the VEP amplitude and latency in individ-uals having mTBI and the symptom of increasedVMS, with comparison to asymptomatic, visually-normal, non-mTBI control subjects.

Methods

Subjects

Ten individuals with mTBI and 10 visually-normalasymptomatic adult subjects participated in thisstudy. The individuals with mTBI either incurreda motor vehicle accident (MVA) or a sports injury1–10 years earlier. The following criteria were usedfor the diagnosis of mTBI [16]: (1) loss of con-sciousness for less than 30 minutes or an alteredstate of consciousness, (2) 13 or greater score on theGlasgow coma scale (GCS) and (3) post-traumaticamnesia (PTA) lasting less than 24 hours. ThemTBI group had a mean age of 28.9 years(SEM� 1.0). The visually-normal group had amean age of 26.7 years (SEM� 4.4). Both groupshad best corrected visual acuity of 20/20 or better ineach eye at both distance and near. Exclusion criteriafor both groups included a history of seizures,constant strabismus and amblyopia, as well as anytype of ocular, systemic or degenerative neurologicaldisease. Those with mTBI were required to havethe symptom of ‘increased VMS’. They wererecruited either from the Raymond J. GreenwaldRehabilitation Center at the State University ofNew York (SUNY), State College of Optometry,or from its student body. The visually-normalsubjects were recruited from its student body andfaculty at the college. The study was approved bythe Institutional Review Board (IRB) at the SUNY,State College of Optometry. Written informed con-sent was obtained from all subjects.

42 K. J. Ciuffreda et al.

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Apparatus

The Diopsys NOVA-TR� visually-evoked potential(VEP) system (Diopsys, Inc., Pine Brook, NJ) wasused to generate the test stimulus and analyse theresponses with respect to amplitude and latency.This system had an artifact detector to eliminatenoise from the EEG signals produced by excessiveblinking and/or eye movements. An amplificationfactor of 10 K and a bandpass filter (0.5–100 Hz)were used.

The binasal occluders were constructed fromcircular (38 mm) transparent lucite disks that fitinto a conventional clinical trial frame (Figure 1).Opaque black tape was applied to the front surfaceof each lucite disk at an angle of 15� temporal andsuperior with respect to the objective vertical merid-ian. The BNO was purposely applied at this angleto reflect what is done by many clinicians to allowunobstructed convergence at near. The BNOs werethen adjusted to be approximately tangent to thenasal-superior pupillary-limbal margin of each eye.

Stimulus

A standard full-field (17 H� 15 V degrees), black-and-white, 64� 64 (20.6 minutes arc check size at1 metre) checkerboard stimulus pattern was used(Figure 2). It had a luminance of 64 cdm�2 and aMichelson contrast of 85%. The stimulus wasmodulated at a temporal frequency of 2 Hz(four reversals per second). Test trial duration was20 seconds. To control fixation and maintain visualattention, a small (0.25� radius) red, rotating,annular fixation target was presented in the centreof the test stimulus.

The VEP amplitude and latency were assessedwith binocular viewing and with refractive correction

in place under the following two experimentalconditions in both the mTBI and visually-normalsubjects:

. Condition 1: Full-field stimulus without binasalocclusion (BNO).

. Condition 2: Full-field stimulus with binasalocclusion (BNO).

Procedures

Electrode placement was slightly modified from theInternational 10/20 system as per the manufacturer’sinstructions. Three Grass (Grass Technologies,Astro-Med, Inc., West Warnick, RI) gold cupelectrodes were placed on the following head posi-tions: the active electrode was placed at the Ozposition which was 2.5 cm above the inion, thereference electrode was placed at the Fz position andthe ground electrode was placed at the Fp2 position.

Recordings

The impedance of each electrode was maintained at�5 K ohms, per the standards of the InternationalSociety for Clinical Electrophysiology of Vision(ISCEV) [17] and recommendation of the manu-facturer. Testing was performed with the subject’srefractive correction in the trial frame in a darkenedroom (38 lux). Subjects placed their chin on the chinrest, which was used to minimize head movementsand maintain a constant fixation distance throughoutthe experiment.

In the first experimental condition, subjects wereasked to fixate binocularly on the central red fixationtarget without the BNO while sitting at a distance of1 metre. This VEP response was used as the baselinefor the second experimental condition.

In the second experimental condition, subjectswore a trial frame with the binasal occluders in place.The binasal occluders were adjusted so that subjectssaw the entire checkerboard stimulus with each eyeand binocularly. A 5.7� H� 15� V region of space

Figure 1. Schematic representation of binasal occluders on asubject.

Figure 2. Standard full-field VEP checkerboard stimulus.Not drawn to scale.

Effect of binasal occlusion on the VEP in mTBI 43

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5.5� lateral to the edge of the test stimulus on eitherside was blocked by the binasal occluders. A sche-matic representation of the binocular visual-fieldwith the BNO is presented in Figure 3. The VEPresponse was then assessed with the BNO andcompared with the non-BNO condition.

Three trials per test condition were conducted.The first was a practice trial. The averages of thesecond and third trials were used in the data analysis.The group mean VEP amplitude and latency (P100ms) for each experimental condition were usedfor the analysis. GraphPad Prism 5 software wasused for the graphs and statistical analysis. All valuesin the text are presented as the mean� 1 SEM.

In addition, each subject was queried regardingtheir visual and visuomotor impressions with addi-tion of the BNO as compared with the non-BNOcondition. This included their sense of the VEPstimulus quality, ambulation down a long hallwayand grasping for nearby objects.

Results

Mean VEP amplitude with and without the BNO

(normals and mTBI)

The mean VEP amplitude in the visually-normal(n¼ 10) and in the mTBI (n¼ 10) groups withand without BNO is presented in Figure 4. In thevisually-normal group, the amplitude withoutBNO was 21.60� 3.72 mV, with a range from9.14–45.43mV. With BNO, the amplitude decreasedto 17.37� 3.03 mV, with a range from 7.37–35.91mV. This decrease with BNO was found in

all 10 subjects. This difference in amplitude betweenthe two conditions was significant [t(9)¼ 4.851,p¼ 0.0009]. In the mTBI group, the amplitudewithout BNO was 19.15� 2.40 mV, with a rangefrom 12.16–35.45mV. With BNO, the amplitudewas increased to 21.32� 2.42 mV, with a rangefrom 13.58–36.90 mV. This increase with BNOwas found in all 10 subjects. This difference inamplitude between the two conditions was signifi-cant [t(9)¼ 4.856, p¼ 0.0009].

Mean VEP latency (P100 ms) with and without

BNO (normals and mTBI)

The mean VEP latency (P100 ms) in the visually-normal and in the mTBI group was also assessedwith and without BNO. The difference in latencybetween the two conditions was not significantin either the visually-normal [t(9)¼1.97, p¼0.07]or in the mTBI [t(9)¼ 1.57, p¼ 0.15] group.Latency was normal and unaffected under all con-ditions (mean range¼ 104–106 ms).

Difference in mean VEP amplitude (percentage)

(normals and mTBI)

The mean amplitude difference in percentage (withBNO – without BNO/without BNO� 100) for theindividual subjects in each group is presented inFigure 5. In the visually-normal group, the differ-ence in mean amplitude decreased with the BNOin all 10 subjects. The amplitude difference rangedfrom �9.52 mV (20.94%) to �2.37 mV (25.92%).This represented a significant directional effect (signtest, p<0.05). In contrast, in the mTBI group, thedifference in mean amplitude increased with BNOin all 10 subjects. The amplitude difference ranged

Figure 3. Representation of binocular visual-field with binasaloccluders. Not drawn to scale. f¼ fovea.

Figure 4. Group mean amplitude for the full field without andwith binasal occluders in normals and in mTBI. Plotted is themeanþ 1 SEM (n¼ 10). * significant difference.

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from þ0.82 mV (5.28%) to þ5.08mV (31.61%).This too represented a significant directional effect(sign test, p< 0.05).

Repeatability

Repeatability was assessed in three subjects fromeach group in a second test session 2–7 days later.In the visually-normal sub-group, all three subjectsdemonstrated a decrease in mean VEP amplitudewith BNO in each session (session 1: 20.57 to18.10mV; session 2: 22.27 to 18.66mV). In themTBI sub-group, all three subjects demonstratedan increase in the mean VEP amplitude with BNO ineach session (session 1: 13.59 to 15.20 mV; session 2:15.28 to 17.86 mV). This is similar to what wasfound in the respective group data.

Control experiment

A control experiment was performed in two of thesubjects with mTBI and VMS. The purpose was todetermine if presence of the trial frame alone withoutBNO was a contributory factor to the VEP ampli-tude changes found with inclusion of BNO. This wasperformed in each case with refractive correctionin place. In subject 1, the mean VEP amplitude was14.36� 2.8, 11.91� 0.99 and 19.12� 1.67 mV withthe full field only, full field with the trial frame onlyand full field with trial frame and BNO, respectively.In subject 2, the mean VEP amplitude was13.96� 2.79, 12.35� 1.01 and 15.73� 0.09 mV forthe same three conditions, respectively.

Subjective impressions with and without the BNO

(normals and mTBI)

Lastly, each of the subjects with mTBI was queriedregarding their subjective visual and visuomotorimpressions with and without the BNO during theactual VEP testing, as well as during a simpleambulation task in the clinic corridor. All of thevisually-normal subjects disliked the BNO. It par-tially blocked their visual field, which they foundannoying and created a sense of visual discomfort.In contrast, eight out of the 10 individuals withmTBI reacted favourbly to the BNO; visuomotoractivities improved, with reduced symptoms (e.g.reduced nausea and decreased disorientation), withBNO. Furthermore, they indicated that the VEP teststimulus appeared brighter, clearer and seemedto flicker less. They also indicated that they couldfixate, walk and grasp objects more accurately andcomfortably with the BNO. In the two individualswith mTBI who disliked the BNO, they too felt itblocked the visual field, as did those that were VN.

Discussion

The current findings confirm, clarify and extend theearlier results of Padula et al. [15]. They found that80% of their hospital-based patients with TBIexhibited consistent increases in the VEP amplitudewith BNO as compared to the non-BNO condition.The present results were even stronger, namely100%. Furthermore, the results of the present studywith BNO alone produced similar findings to thatof Padula et al. [15], who used BNO plus base-in(BI) prism.

There was one critical difference between thetwo studies as implied above. In the present study,only the BNO was employed, whereas, in the Padulaet al. [15] investigation, BNO was always used inconjunction with BI prism. This combination usedin the latter study makes the findings difficult tointerpret as to the resultant component contributionto the overall VEP amplitude changes found. Futureresearch should be performed to differentiatebetween the BNO and base-in prism effects on theVEP in mTBI.

There are two possible mechanisms that mayexplain the present findings. First, it is speculatedthat a common element involves the ‘spread ofsuppression’, a neurophysiologically-based conceptderived from the strabismus literature [18], as wellas the field of visual psychology [19]. That is,the cortically-based suppressive effect directedover a specific region of visual space encompassingretinal/cortical regions ‘spreads’ and thus extends tocontiguous areas by up to a few degrees or more.With this in mind, it is speculated that the individual

Figure 5. Diagnostic group mean amplitude difference for indi-vidual subjects (%). Positive and negative percentage valuesrepresent an increase or decrease in mean amplitude differencevalues, respectively.

Effect of binasal occlusion on the VEP in mTBI 45

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with both mTBI and VMS habitually attempts tosuppress/inhibit visual motion in the peripheralvisual field to reduce the incoming troublesomevisual motion stimuli from this region. However,as the VMS still persists, this suppression appearsnot to be totally effective and therefore suggests‘partial suppression’. Without the BNO, this sup-pression occurring near the lateral edges of the VEPtest stimulus array spreads and extends 5� or more.This suppressive/inhibitory effect interacts with theexcitatory activity derived directly from the morecentral VEP stimulus itself neurophysiologically,thus acting to reduce the overall level of corticalexcitation and in effect reducing the VEP amplitude.However, with addition of the BNO, portions of thissame habitually-suppressed visual field are occluded,thus reducing the effective amount of suppressionover that region. Thus, there is now a reduction inthe intensity of the suppressive effect, which in turnresults in a relative increase in the VEP amplitude, asfound in the present experiment, as well as in that ofPadula et al. [15]. In contrast, using this same logic,normals habitually have more relative excitatoryactivity in these regions of the visual field; thereis no active and habitual suppression attemptedpresent as speculated here to be the case in mTBI.Hence, with addition of BNO in visually-normal,this normal excitatory activation is effectivelyreduced. Thus, there now is a relative reduction inthe magnitude of the suppressive spread. This wouldresult in a relative decrease in the VEP amplitude,as found in the present experiment, as well as in thatof Padula et al. [15] in many of their normalsubjects. This is believed to be the most plausibleexplanation. The speculation regarding attemptedvisual motion suppression in mTBI with VMSshould be tested in the future. Secondly, it isspeculated that there might be a ‘faulty’ filteringmechanism with respect to visual informationprocessing [20]. That is, normals can disregardirrelevant visual motion in the periphery, whereasmany of those with mTBI cannot. That is, the lattermay manifest an inability to inhibit fully this infor-mation from entering their visual processing stream(i.e. magnocellular pathway). Thus, with additionof the BNO, this inhibition would not be necessary,hence resulting in a relative increase in VEP ampli-tude. This speculation should also be tested inthe mTBI population with VMS in the future.Furthermore, it is possible that both processesmay be involved, namely incomplete suppressiveand filtering processes.

There are three important clinical implicationsof the present VEP findings. First, an objectivecorrelate to the decreased symptoms was found; thatis, changes in early cortical brain activity reflectedsubjective changes as reported by the individual with

respect to visual perceptual changes. Secondly, andrelated to the above, an objective correlate to theimproved sensorimotor and visuomotor performancewas found; that is, changes in the early cortical brainactivity reflected subjective changes as reported bythe individual with respect to gross and moderately-fine motor abilities. Thirdly, and perhaps mostdirectly clinically relevant, in these mTBI patientswith the symptom of VMS, if one does not obtaina consistent increase in VEP amplitude with BNO,the clinician should proceed with caution; BNO mayin fact be contraindicated and this notion warrantsfurther investigation. All subjects in the presentstudy and nearly all in the Padula et al. [15] studyexhibited a consistent increase in VEP amplitudewith BNO. Thus, for all of the above reasons, theVEP technique becomes another valuable tool in theclinician’s therapeutic armamentarium in individualswith mTBI having the symptom of VMS.

There are three primary areas for future research.First, a rating-scale questionnaire should be devel-oped to assess symptoms and quality-of-life (QoL),with and without BNO, in individuals with mTBIand VMS. This would allow one to quantify andstatistically analyse/compare the impact of BNO onthe patient’s everyday lifestyle and overall QoL.Secondly, and related to the above, changes in motorperformance should be quantified using subjectiveand/or objective approaches. For example, the clini-cian could videotape the performance of an individ-ual with mTBI and VMS, with and without BNO,while completing a dynamic ‘walk and search’ taskwithin a large objected-filled room. Accuracy andtime to find a select group of objects could bedetermined. Thirdly, there is a need to quantify theminimum ‘level’ of opaqueness for maximum reduc-tion of symptoms and optimal motor performance,perhaps by using neutral density (ND) filters ofvarying gradations, as patient satisfaction and long-term use are intimately related to cosmesis.

Acknowledgements

We thank Dr Jose-Manuel Alonso for his helpfuldiscussion and DIOPSYS Inc., Pine Brook,New Jersey, USA. We thank the anonymous reviewerfor his/her helpful comments and suggestions.

Declaration of Interest: The authors report noconflicts of interest. The authors alone are respon-sible for the content and writing of the paper.

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Effect of binasal occlusion on the VEP in mTBI 47

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