Post-traumatic headaches and vision: A review

Abstract

BACKGROUND:

Post-traumatic headache is the most common sequela of brain injury and can last months or years after the damaging event. Many headache types are associated with visual concerns also known to stem from concussion.

OBJECTIVES:

To describe the various headache types seen after head injury and demonstrate how they impact or are impacted by the visual system.

METHODS:

We will mirror the International Classification of Headache Disorders (ICHD) format to demonstrate the variety of headaches following brain injury and relate correlates to the visual pathways. The PubMed database was searched using terms such as headache, head pain, vision, concussion, traumatic brain injury, glare, visuomotor pathways.

RESULTS:

Every type of headache described in the International Classification of Headache Disorders Edition III can be initiated or worsened after head trauma. Furthermore, there is very often a direct or indirect impact upon the visual system for each of these headaches.

CONCLUSION:

Headaches of every described type in the ICHD can be caused by brain injury and all are related in some way to the afferent, efferent or association areas of the visual system.

Keywords

Post-concussion syndrome concussion traumatic brain injury headache vision oculomotor dysfunction visuomotor rehabilitation

1 Introduction

The United States Center for Disease Control (CDC) reports that traumatic brain injury (TBI) in the USA amounts to 2.5 million emergency room visits, admissions to hospital and deaths annually (Prevention, 2015). Of these patients, over 75% have normal conventional imaging (i.e., CT or MRI) and are subsequently labeled as “mild traumatic brain injury” (mTBI). Furthermore, CDC also reports that more than 90% of these mTBI patients suffered “blunt trauma” sustained during motor vehicle accidents (MVA), falls, assaults and sport-related activities. The most common symptomatic sequela of mTBI is headache, estimated to have an incidence as high as 90% (AFHSC, 2013). It is important to note that not only is the definition of “mild” TBI not universally accepted, but also that the “mild” aspect mainly speaks to the absence of findings on conventional imaging (GL, 2006; Williams, 1990), and not that the injury itself is mild. Mild TBI events can certainly cause long lasting, pervasive, and disabling health problems. Indeed, the lack of structural deficits on conventional imaging does not rule out functional deficits demonstrable on physical examination as per the current NIH definition (GL, 2006), e.g., oculomotor dysfunction (OMD) or indirect traumatic optic neuropathy (ITON). The current NIH definition states: “A person with a mild TBI may remain conscious or may experience a loss of consciousness for a few seconds or minutes. Other symptoms of mTBI include headache, confusion, light-headedness, dizziness, blurred vision or tired eyes, ringing in the ears, bad taste in the mouth, fatigue or lethargy, a change in sleep patterns, behavioral or mood changes, and trouble with memory, concentration, attention, or thinking”. It is noteworthy that the section on vision is quite vague (i.e., “tired eyes”). In fact, studies on mTBI have shown an incidence of OMD as high as 69% for having at least one deficiency of saccades, accommodation, convergence deficits and smooth pursuits (Master, 2016).

The development or worsening of headaches after a head injury is even more pronounced in certain populations such as active military service members. Over 98% of Operation Enduring Freedom / Operation Iraqi Freedom (OEF/OIF) veterans with TBI reported headaches; 37% reported headaches lasting longer than 3 months (Theeler, 2010). Twenty seven percent of soldiers in this same study reported headaches on an on-going chronic basis. However, only approximately half of these headaches meet the diagnostic criteria for post-traumatic migraine headaches (PTMH), leaving questions about the nature of the remaining headache types. These more chronic symptom trajectories must not be dismissed as they may contribute to the 3x-higher rate of suicide in mTBI patients compared to the general population (Fralick, 2016). One of the most tragic statistics in this research, which examined suicide rates in the post-concussion population using a large sample size (more than 235,000), was that over 50% of those who committed suicide had a documented visit with a physician within the last week of life. In fact, over time it was reported also that these suicide rates exceeded the rates of suicide in the general (non-mTBI and mTBI) armed forces. This finding should be a call to healthcare professionals to listen carefully to the symptoms of mTBI patients with caution to avoid dismissing any as “frivolous” or “idiopathic”. Sadly, patients often do not have the vocabulary to express many of their symptoms, hence the rather nebulous term “tired eyes” in the NIH description cited previously. While it is known that visual symptoms present frequently after mTBI and patients are often found to demonstrate disorders listed above, patients might only describe vague complaints such as difficulty reading, or eyes not working together or simply “discomfort around the eyes” (Kontos et al., 2020; Lovell, 2004). The peri-ocular and ocular headache that might be described as a “pressure feeling around the eyes” was seen with more than a 10-fold rate in concussed athletes compared to controls (Poltavski, 2014).

Functional visual difficulties can often be improved with appropriate visual rehabilitative interventions (Ciuffreda, 2016; Gallaway, 2017; Thiagarajan, 2–14, 2014; Thiagarajan, J.E.; Ludlam, Kapoor, 2014; Widmer, 2018), thus heightened awareness by both physicians, optometrists, physical therapists and other allied healthcare professionals is necessary. In our experience, appropriately qualified optometrists and ophthalmologists are often those providers more likely to identify OMD in concussion and recommend rehabilitation directed at this concern, something undertaken for the most part by optometrists with advanced training in the area. The need to direct patients to these providers has also been expressed by other professions who treat concussed patients such as otolaryngologists, psychiatrists, and sports medicine providers (Marshall, 2015; Matuszak, 2016; Park, 2019).

Recent research on inter-disciplinary care of mTBI (Kontos et al., 2020) has shown that of the six global vectors of symptomatology (i.e., migraine, ocular, vestibular, cervical, sleep and cognitive/psychological), migraine was most common followed by ocular symptoms. Furthermore, the highest correlations between symptom areas were found between ocular-migraine followed by ocular-cognitive. Finally, the two highest areas in terms of ability to differentiate controls from mTBI (using Receiving Operator Characteristic / ROC) analysis were migraine and ocular, respectively. This supports the notion that consideration of visual symptomatology is vital when treating mTBI patients with on-going symptomatology in general, and for those with visual symptoms, in particular when headaches are also reported.

Recognizing that at least 40% of the primate brain subserves vision (Felleman, 1991) and that both cortical and sub-cortical areas of the brain are heavily involved in processing visual information, it seems most reasonable to engage in a robust discussion of the confluence of headache, mTBI and vision. Given the pervasiveness of both photophobia and peripheral visual motion hypersensitivity symptoms (often described by our patients as “visual overwhelming”) in mTBI cases (Singman E.L.; Quaid, 2019), it appears logical to discuss global visual motion processing mechanisms both from direct magnocellular pathways and indirect superior colliculus / pulvinar pathways, converging to regions such as the middle temporal Area (MT/V5) (Born, 2005). Area MT/V5 is believed to be part of the dorsal stream of visual processing, sometimes referred to as the “where pathway”, i.e., that pathway associated with motion and location, as opposed to the ventral stream, referred to as the “what pathway”, i.e., that pathway associated with form recognition. It seems reasonable to suggest that photophobia might involve pathways similar to peripheral visual motion because M-cells, i.e., retinal ganglion cells that project to the magnocellular layers of the primate lateral geniculate nucleus are much more sensitive to luminance contrast than P-cells which project to the parvocellular layers and also that M-cells mediate the dorsal stream, whereas P-cells mediate the ventral stream (Digre & Brennan, 2012; Purpura, Kaplan, & Shapley, 1988).

2 Headache after head trauma through the lens of vision

We will discuss specific vision issues and their connections to headaches following the classification system of the International Headache Society (IHS), known as ICHD-III (International Classification of Headache Disorders, 3^rd Edition). It is vital to note that the terms primary and secondary headache should be understood in the context of the ICDH-III. If a patient develops a new headache, which occurred for the first time, and this situation has a close temporal relation to another disorder known to cause headache, the new headache is coded as a secondary headache attributed to the causative disorder. This remains true even when the headache has the characteristics of a primary type headache (i.e. migraine, tension-type or cluster headache). This is important to keep in mind in the context of mTBI, as many patients have no history of headaches prior to the reported mTBI event.

Note that the layout of this review will purposefully mirror the order of the classification of the ICHD-III to ensure consistency with the International Headache Society ordering and facilitate cross-referencing.

3 Part I: Primary headaches

3.1 Migraine headaches

Post traumatic headache (PTHA) is a well-recognized and common phenomenon (Argyriou et al., 2021; Ashina, Iljazi, Amin, et al., 2020). Both its incidence and duration has been reported to be greater after mild TBI than severe TBI (Sirko, Mizyakina, & Chekha, 2021). Furthermore, a large study of concussion in youth reported that 46.5% of concussed patients suffered post traumatic headache of the migraine phenotype and that these patients require significantly longer time to recover (on average, 3 months) than patients with non-migrainous headaches (Kamins et al., 2021). Vision is affected by migraine; migraineurs have demonstrated prolonged post-ictal reduced visual field sensitivity (McKendrick & Badcock, 2004), visual snow (Schankin et al., 2014; Viana, Puledda, & Goadsby, 2020), glare sensitivity and photophobia (Diel et al., 2021; Wilkins, Haigh, Mahroo, & Plant, 2021), dry eye (Diel et al., 2021), convergence insufficiency (Singman, Matta, & Silbert, 2014) and increased saccadic latency (Filippopulos et al., 2021). Notably, all of these visual defects have also been reported in patients with TBI (Alvarez et al., 2021; Burstein, Noseda, & Fulton, 2019; Ciuffreda, Han, Tannen, & Rutner, 2021; Diel et al., 2021; Dise-Lewis et al., 2019; Mehta, Garza, & Robertson, 2021; Patel & LaBella, 2021; Shepherd et al., 2020; Walsh et al., 2015; Whitney & Sparto, 2019). Therefore, it is difficult to know whether the TBI and/or the migraine initiated the visual phenomena. It is also important to note that visual stimulation seems capable of triggering migraine, particularly stimulation from glare (Hayne & Martin, 2019) and flickering patterns (Shepherd & Joly-Mascheroni, 2017). In addition, it has been reported that migraineurs are less tolerant (i.e., find greater discomfort) to low and high wavelengths of light during the interictal period (Main, 2000). These data lead us to believe that it would be reasonable to explore whether migraine perpetuates concussion symptoms via a vicious circle (Benemei et al., 2020).

3.2 Tension-type headaches

Tension type headache is common after concussion, although perhaps not as common as migraine (Ashina, Iljazi, Al-Khazali, et al., 2020; Ashina, Iljazi, Amin, et al., 2020). Tension headache is also known as muscle contraction or stress headache and often is felt on the forehead with a band-like quality (Shah & Hameed, 2021). While there seem to be no visual symptoms caused by tension type headache (other than periocular discomfort), tension type headache can be brought on by ptosis (Bahceci Simsek, 2017), deficiency of accommodation (Jaschinski, Konig, Mekontso, Ohlendorf, & Welscher, 2015) and visuomotor deficits such as convergence insufficiency (Garcia-Munoz, Carbonell-Bonete, & Cacho-Martinez, 2014). Since concussion is known to lead to glare sensitivity and concomitant squinting (Hayne & Martin, 2019) as well as accommodative paresis (Alvarez et al., 2021) and convergence insufficiency (Alvarez et al., 2021; Whitney & Sparto, 2019), one must wonder about the extent to which post-concussion visual symptoms contribute to the post-concussion tension type headache.

3.3 Cluster headaches and other trigeminal autonomic cephalalgias

Cluster headaches can be precipitated or worsened after TBI (Barloese et al., 2020). Notably, one risk factor for cluster headache is a deficiency in serum testosterone (Delaruelle et al., 2018; Stillman, 2006) and hypogonadism is known to follow TBI (Ashley, 2020; Isaacs & Geracioti, 2015). The possible connection between cluster headache, serum testosterone level and TBI has not been reported but it seems to be a reasonable area for careful exploration. Even less information has been published on any correlation between TBI and trigeminal neuralgia (TN). A single case report describes the onset of TN after TBI (Gkekas, Primikiris, & Georgakoulias, 2014). Notably, animal models of repetitive concussion suggest that closed head injury causes both cephalic and extracephalic tactile pain hypersensitivity (Bree, Stratton, & Levy, 2020). Furthermore, there appears to be a selective trigeminal hyper-nociception as well after even mild closed head injury (Benromano et al., 2015). Taken together, these results suggest a need to explore more carefully for the presence of TN in TBI patients.

3.4 Other primary headaches

Post traumatic is a secondary headache. However, post traumatic headaches have been shown to encompass symptoms that might be considered primary headache save for the history of TBI. A recent large study of American service personnel indicated that post traumatic headaches differ from non-concussive headaches by severity more than type (Scher et al., 2021).

4 Part II: Secondary headaches

4.1 Headaches attributed to neck and/or neck trauma

Head trauma is intimately associated with neck injury with considerable overlap of whiplash and concussion symptoms (Cheever, McDevitt, Phillips, & Kawata, 2021; Gil & Decq, 2021; Kuperman et al., 2021; Mathew & Cooper, 2021). It is known that patients with concussion have significantly higher odds of sustaining a comorbid neck injury (Sutton et al., 2019). Furthermore, neck injuries mimic post-concussion headache (with occipital neuralgia being the archetype for this (Laguerre, McGargill, & Herman, 2020)) and contribute to post-concussion symptoms (Kennedy, Quinn, Chapple, & Tumilty, 2019). In addition, cervicogenic rehabilitation is a valuable adjunct not only to neck trauma but also to the entire spectrum of post-concussion care (Brown & Camarinos, 2019). This supports the concept that the post-traumatic derangement of interactions between the kinesthetic (via the neck), vestibular and visual systems require targeted and coordinated rehabilitation efforts to optimize recovery from TBI (Kontos et al., 2018).

4.2 Headaches attributed to cranial or cervical vascular disorder

Post-traumatic headaches secondary to vascular disorders can include life-threatening emergencies such as arterial dissections, aneurysms, cavernous-carotid fistulas and intracranial hemorrhages, all of which can affect vision (Ibanez, Navallas, de Caceres, Martinez-Chamorro, & Borruel, 2021). The manifestations of these conditions on the visual system may include proptosis, heterotropias, nystagmus, accommodative paresis, ptosis, lagophthalmos, blepharospasm, mydriasis, miosis and papilledema (Spiegel & Moss, 2021). In some patients, the visual findings may even precede the headache, making it imperative that eye care providers are familiar with this subject and understand when and how to refer. In addition, chronic subdural hematoma may develop even when imaging in the acute period shows no hemorrhage (Edlmann, Whitfield, Kolias, & Hutchinson, 2021); therefore lingering visual system complaints with unresolving or worsening headache may be an indication to re-image the patient’s head and/or neck.

4.3 Headache attributable to non-vascular intracranial disorder

Post-traumatic headache in this category, particularly ones associated with visual findings, would most likely stem from cerebrospinal fluid (CSF) hypo- and hypertension, Chiari malformation, seizure (post-ictal headache), and possibly pituitary hypofunction. CSF hypotension can be associated with third and sixth cranial nerve palsies and visual field defects (Pilo-de-la-Fuente, Gonzalez Martin-Moro, Navacerrada, Plaza-Nieto, & Jimenez-Jimenez, 2013). CSF hypertension is also associated with diplopia and visual field, visual acuity, and color vision defects, particularly from papilledema (Ambika, Arjundas, Noronha, & Anshuman, 2010). The most common visual manifestation of Chiari malformation is nystagmus (Giammattei, Messerer, Daniel, Aghakhani, & Parker, 2020). Notably, Chiari malformation may be subclinical until a head injury (Woodward & Adler, 2018), and its presence increases the risk of post-concussion syndrome (Spencer & Leach, 2017). Mild TBI such as concussion does not appear to be a risk factor for post-traumatic epilepsy (Wennberg, Hiploylee, Tai, & Tator, 2018), although severe trauma certainly is (Khalili, Kashkooli, Niakan, & Asadi-Pooya, 2021; Rumalla et al., 2018). Because post-ictal headaches frequently meet criteria for migraine (Caprara et al., 2020), visual sequelae therein can be expected (vide supra), particularly glare sensitivity. Finally, it should be mentioned that post-traumatic endocrinologic changes could occur including hypotestosteronism (Ciarlone et al., 2020; Isaacs & Geracioti, 2015). This may elevate the risk of cluster headache (Barloese et al., 2020; Stillman, 2006), which can be associated with conjunctival injection, lacrimation, miosis/ptosis (i.e., sympathetic defect) and eyelid edema (parasympathetic defect) (Gouveia, Parreira, & Pavao Martins, 2005).

4.4 Headaches attributed to substance use or withdrawal

There is a bidirectional relationship between TBI and substance abuse, i.e., patients with substance abuse disorders have an elevated risk of TBI and patients with TBI have an elevated risk of developing substance abuse disorders (Jacotte-Simancas, Fucich, Stielper, & Molina, 2021). From a visual perspective, there is a rare phenomenon of acute onset esotropia caused by abrupt withdrawal of opiates which resolves when opiates are re-instituted (Firth, 2005). In addition, a significant number of medications used for posttraumatic headache have anticholinergic side effects, which can cause mydriasis and accommodative paresis, leading to symptoms of blurred or fluctuating vision for the patient.

4.5 Headache attributed to infection

Head trauma can be associated with orbital fractures. Although antibiotic prophylaxis has been shown to be unnecessary in patients without open wounds (Esce, Chavarri, Joshi, & Meiklejohn, 2021), heightened awareness on the part of the provider and patient is necessary so that orbital infection is recognized should it occur. On the other hand, infection is among the most common complication following non-missile penetrating head injuries (Harrington, Gretschel, Lombard, Lonser, & Vlok, 2020), and visual system dysfunction can result depending upon the proximity of the infection nidus to the orbit or visual pathways.

4.6 Headache attributed to disorder of homeostasis

Patients with head injury may require air-evacuation. Low barometric pressure puts the head injury patient at risk for complications such as increased intracranial pressure, tension pneumocephalus, orbital emphysema and brain herniation (Helling & McKinlay, 2005; Ismailov & Lytle, 2016). These conditions can be fulminant and fatal; mydriasis, loss of normal ocular motility and orbital swelling are visual system signs of concern (Tadevosyan & Kornbluth, 2021).

4.7 Headache attributable to disorder of cranium, neck, eyes, ear, nose, sinuses, teeth, mouth, or facial / cranial structures

It behooves the provider to consider intermittent angle closure when evaluating headaches with visual sequelae (redness, pain, tearing, halos around objects). These symptoms are consistent with angle closure glaucoma. Intermittent angle closure can mimic migraine with aura (Stan, Stan, & Rednik, 2020) (as might be seen after TBI) and chronic angle closure has been reported after head and orbit trauma (E. Singman, 2020; Tse, Titchener, Sarkies, & Robinson, 2009). Furthermore, patients with Post-traumatic migraine have been successfully treated with amitriptyline and topiramate prophylaxis (Silberstein, 2015; Xu, 2017). However, it is important to note that amitriptyline has anticholinergic side effects, which can trigger angle closure via pupillary block; in addition Topiramate, can trigger acute angle closure via swelling of the ciliary body (Lachkar, 2007; Yang, 2019).

4.8 Headaches attributable to psychiatric disorder

Depression and other aspects of post-traumatic stress disorder (PTSD) are common psychiatric comorbidities of mild TBI and contribute to the reported quality, duration, and intensity of headache (Ashina et al., 2021; Bomyea et al., 2016; Kulas & Rosenheck, 2018). Depression has a strong positive association with dry eye (Weatherby, Raman, & Agius, 2019) and PTSD is associated with impaired visuo-motor integration in TBI patients (Walker et al., 2018).

5 Part III: Neuropathies & facial pains and other headaches

5.1 Painful lesions of the cranial nerves and other facial pain

Orbital and periorbital pain is common after head trauma. Hyperesthesia from entrapment of the infraorbital nerve (Beigi et al., 2017), supraorbital nerve (Stewart, Boyce, & McGlone, 2012) and supratrochlear nerve (Filipovic et al., 2017; Mathew & Cooper, 2021) can cause orbit pain. In addition, pain can be referred to the orbit from the maxilla associated with facial trauma (Petersen, Ipsen, Felding, von Buchwald, & Steinmetz, 2021)), the temporomandibular joint (associated with post-concussion bruxism(Herrero Babiloni et al., 2020)) and the neck (e.g., greater occipital neuralgia (Mathew & Cooper, 2021)), for example. It should be mentioned that post-traumatic cranial neuropathies can also be associated with hypo-esthesia.

5.2 Other headaches

This section can be used for headaches pertaining to oculomotor disorders connected to vergence and accommodative disorders. These headaches stem from a reduced ability to control the vergence, pursuit, accommodative and saccadic systems properly; as such, they do not really fit into the previous categories. In the author’s experience, vergence and accommodative disorders are often reported as being accompanied by a “dull ache” and “tired feeling behind the eyes”. The headaches are associated with an increasing severity with at-near visual tasks such as reading or scrolling on a computer screen. This is logical, as at-near visual tasks required greater endurance for convergence and accommodation.

6 Discussion

Given that vergence, accommodation, pursuit and saccadic-eye movement deficits are (i) common in mTBI and (ii) are not related to eye pathology per se, we would posit that the term “ ocular ”, mentioned above in reference to screening tools employed to inform a multidisciplinary approach (Kontos et al., 2020) might more appropriately be replaced with the term “ vision ”; terminology matters greatly. We think of the term “eyesight” as pertaining to visual acuity, visual field, color vision, etc. Furthermore, the term “ocular” refers to the globe itself and, while certainly appropriate for ocular disease related issues, is not actually an adequate descriptor for the innervational (as opposed to mechanical) oculomotor deficits listed above. On the other hand, we think of the term “vision” as referring to an entire visual process including the neural processing of afferent and efferent visual information, visual memory, etc., a far more complex activity.

Our semantic approach is similar to the rationale for the nomenclature used in the vestibular aspect of TBI (i.e., central/brain-related deficit versus peripheral/end organ-related deficit). In mTBI, the “eyeball itself” is often healthy with some exceptions (e.g., ITON (Singman; Daphalapurkar, 2016)), but there are very frequently oculomotor problems. The archetypal deficit might be convergence insufficiency (CI), which is estimated to be demonstrated in as many as 49% of TBI patients (Barnett, 2015; Vernau, 2015). In CI, the patient has full adduction towards the nose monocularly, yet cannot converge when both eyes are engaged, thereby ruling out a myogenic defect. Notably, evidence suggests that convergence is not innate, but rather only starts to develop at 4 months post-birth with full peak normal vergence occurring by 5–6 years of age (Weinacht, 1999). Fusional mechanisms that support convergence certainly require intact ocular and orbital tissues but also need the development of more complex central structures. There are many serial systems involved vergences; the midbrain appears to be a key relay station of the subservient pathways via networks to the cerebellum and pons (Gamlin, 2002), area V1 (Trotter, 1996), MST (Middle Superior Temporal) cortex (Takemura, 2001) and Frontal Eye Fields (FEF) (Gamlin, 2002). It is probable that diffuse axonal injury (DAI) resulting from TBI might affect multiple locations along this complex network (Thiagarajan, D.P., 2011). Although this makes determining the exact location of injury difficult in terms of a diagnosis of deficient vergences, it does support the idea that vergence deficiency is a sensitive clinical indicator of concussion.

The vestibular-ocular reflex (VOR) can also become deranged after TBI despite the absence of evident damage to the eye or inner ear, i.e., the ocular and vestibular end organs, respectively. Indeed, the central processes supporting the VOR appear to be quite susceptible to damage after TBI, manifesting as dizziness with head and/or eye movements in many patients (Herdman, 2014).

A key central processor for visual motion detection and responsiveness is Area MT/V5, one of the very few visual areas almost fully myelinated at birth (Gilaie-Dotan, 2016). Area MT receives a substantial thalamic magnocellular input, which in turn receives major input from peripheral retina, i.e., that portion of the retina enabling motion processing, flicker perception and contrast gain (Born, 2005; Derrington, 1984). This pathway permits area MT to function as a significant contributor to visual motion processing. Indeed, Area MT is so critical to gross motor development in infants that global motion perception can be used to aid in the evaluation of dorsal visual stream function in early childhood (Thompson, 2017). Notably, symptoms of fluorescent lighting- and peripheral motion-intolerance as well as photophobia are frequent patient complaints after mTBI, supporting the idea that Area MT (or, at least, dorsal visual stream function) is particularly susceptible to damage after head trauma.

It should be mentioned that the vestibular system is also fully formed at birth (D.J., 2012). The contemporaneous and early development of a mature Area MT and a mature vestibular system at birth permits the VOR to support an infant’s ability to “orientate in space”. Specifically, the robust VOR represents the confluence of the infant brain’s efforts to employ two significant sensory systems in an integrated manner. This integration determines the infant’s sense of “where” (i.e., where am I and where is everything around me) weeks or even months before the fully matured sense of “what” (i.e., what are those images and colors mean). Furthermore, the substantial motion-dominated magnocellular input to Area MT (Bourne, 2006; Gilaie-Dotan, 2016) lays the foundation for a stable platform upon which the development of fine central vision depends.

In the context of headaches after mTBI, it is known that patients commonly report headache when trying to sustain stable gaze or perform saccades, functions subserved by Area MT. They also report painful intolerance to perceiving motion stimuli or performing rapid head turns, functions subserved by VOR integration. These frequent symptoms become a challenge for the clinician because the vestibular system often must be assessed indirectly via the visual system, i.e., through the examination of eye movements. Therefore, headaches secondary to oculomotor dysfunction can result in ambiguity during VOR assessment if not properly identified prior to vestibular testing (Mantokoudis, 2016; Singman; Quaid, 2019). As mentioned previously, these ocular (we prefer “ vision ”) post-TBI headaches (i.e., “tired eyes”) are not readily captured in current headache classifications. Therefore, we suggest that headaches related to oculomotor dysfunction after TBI be included in above-mentioned IHC-3 Part III(14) section, i.e., headache from somewhere else in the brain, until such time as the location of damage and origin of headache is clarified.

Another subject begging clarification concerns the effect of light on patients with TBI. Main & Dowson (2000) reported that short and long wavelengths lowered the discomfort thresholds in migraineurs during the interictal period. Blue light may cause damage to the cornea lens and retina and yet may be critical for refractive development and regulating circadian rhythm (Zhao, 2018). A recent randomized controlled trial demonstrated that patients with mTBI enjoyed significantly better sleep patterns after blue light exposure (469nm) compared to placebo (Killgore, 2020). While this paper did not look at photophobia specifically in migraine, the authors have noted anecdotally in their clinics, that blue tints in post concussion syndrome patients appear to reduce photophobia and hypersensitivity to high contrast motion in peripheral gaze (i.e., OKN drum). It is difficult to reconcile the conflicting data and there are likely a number of confounding variables such as the contribution of dry eye to photophobia and migraine (Diel, Kardon, Buse, Moulton, & Galor, 2021), as well as the degree to which intensity rather than wavelength plays a role (Zivcevska, 2020). The distribution and density of photoreceptors in the human retina is highly variable (Curcio, 1990; Roorda, 1999). Short wavelength cones (peak absorbance 420nm) are relatively absent in the foveola suggesting they stimulate processes associated with peripheral vision. Furthermore, area MT neurons, while receiving input from all 3 cone types, respond in a directionally selective manner to S cones (Seidemann, 1999), consistent with the idea that S cones are involved in motion detection, i.e., peripheral rather than central visual processing, or the “where” rather than the “what”. Presuming the visual pathways of the MT area are damaged after concussion and that this damage underlies the photophobia and peripheral motion intolerance experiences by concussed patients, then one could hypothesize that stronger or more enriched S-cone stimulation might recruit greater activity in an MT pathway made somehow deficient by TBI and offer some symptomatic relief.

7 Conclusions

Every type of headache can be initiated or worsened after head injury. Furthermore, the visual system is very likely to be affected directly along with the headache, or by the headache, or may even be part of the triggering mechanisms for the headache. The visual system is complex in nature. Given the obvious pervasiveness of visual symptomatology post-mTBI, which includes visually-triggered headaches, it is reasonable to conclude that there are many common pathways shared by the dynamic responsibilities of the visual system such as vergences, accommodation, fixation disparity, saccades and pursuits and those pathways involved in headache. Further research is needed to not only identify those shared pathways but to determine whether their interactions after TBI stem from the maladaptive activation of existing neural substrates or the development of new neural connections during the recovery period. The elucidation of these interactions could lead to new methods for prevention, mitigation, treatment, and rehabilitation of vision-related-headache after TBI.

Conflict of interest

The authors declare that they have no conflict of interest.

References

(AFHSC)., A. F. H. S. C. (2013). Incident diagnosis of common symptoms (“sequelae”) following traumatic brain injury, active component, U.S. Armed Forces. MSMR, 20(6), 9–13.

Alvarez,

T. L.

, Yaramothu,

, Scheiman,

, Goodman,

, Cotter,

S. A.

, Huang,

,... Master,

C. L.

(2021). Disparity vergence differences between typically occurring and concussion-related convergence insufficiency pediatric patients. Vision Res, 185, 58–67. doi: 10.1016/j.visres.2021.03.014

Ambika,

, Arjundas,

, Noronha,

, & Anshuman. (2010). Clinical profile, evaluation, management and visual outcome of idiopathic intracranial hypertension in a neuro-ophthalmology clinic of a tertiary referral ophthalmic center in India. Ann Indian Acad Neurol, 13(1), 37–41. doi: 10.4103/0972-2327.61275

Argyriou,

A. A.

, Mitsikostas,

D. D.

, Mantovani,

, Litsardopoulos,

, Panagiotopoulos,

, & Tamburin,

(2021). An updated brief overview on post-traumatic headache and a systematic review of the non-pharmacological interventions for its management. Expert Rev Neurother, 21(4), 475–490. doi: 10.1080/14737175.2021.1900734

Ashina,

, Al-Khazali,

H. M.

, Iljazi,

, Ashina,

, Amin,

F. M.

, Lipton,

R. B.

, & Schytz,

H. W.

(2021). Psychiatric and cognitive comorbidities of persistent post-traumatic headache attributed to mild traumatic brain injury. J Headache Pain, 22(1), 83. doi: 10.1186/s10194-021-01287-7

Ashina,

, Iljazi,

, Al-Khazali,

H. M.

, Ashina,

, Jensen,

R. H.

, Amin,

F. M.

,... Schytz,

H. W.

(2020). Persistent post-traumatic headache attributed to mild traumatic brain injury: Deep phenotyping and treatment patterns. Cephalalgia, 40(6), 554–564. doi: 10.1177/0333102420909865

Ashina,

, Iljazi,

, Amin,

F. M.

, Ashina,

, Lipton,

R. B.

, & Schytz,

H. W.

(2020). Interrelations between migraine-like headache and persistent post-traumatic headache attributed to mild traumatic brain injury: a prospective diary study. J Headache Pain, 21(1), 134. doi: 10.1186/s10194-020-01202-6

Ashley,

M. J.

(2020). Testosterone, sex steroids, and aging in neurodegenerative disease after acquired brain injury: a commentary. Brain Inj, 34(7), 983–987. doi: 10.1080/02699052.2020.1763461

Bahceci Simsek,

(2017). Association of Upper Eyelid Ptosis Repair and Blepharoplasty With Headache-Related Quality of Life. JAMA Facial Plast Surg, 19(4), 293–297. doi: 10.1001/jamafacial.2016.2120

10.

Barloese,

M. C. J.

, Beske,

R. P.

, Petersen,

A. S.

, Haddock,

, Lund,

, & Jensen,

R. H.

(2020). Episodic and Chronic Cluster Headache: Differences in Family History, Traumatic Head Injury, and Chronorisk. Headache, 60(3), 515–525. doi: 10.1111/head.13730

11.

Barnett,

B. P. S E.L.

(2015). Vision concerns after mTBI. Curr Treat Options Neurol, 17(2), 329–335.

12.

Beigi,

, Beigi,

, Niyadurupola,

, Saldana,

, El-Hindy,

, & Gupta,

(2017). Infraorbital Nerve Decompression for Infraorbital Neuralgia/Causalgia following Blowout Orbital Fractures: A Case Series. Craniomaxillofac Trauma Reconstr, 10(1), 22–28. doi: 10.1055/s-0036-1592095

13.

Benemei,

, Labastida-Ramirez,

, Abramova,

, Brunelli,

, Caronna,

, Diana,

,... European Headache Federation School of Advanced, S. (2020). Persistent post-traumatic headache: a migrainous loop or not? The preclinical evidence. J Headache Pain, 21(1), 90. doi: 10.1186/s10194-020-01135-0

14.

Benromano,

, Defrin,

, Ahn,

A. H.

, Zhao,

, Pick,

C. G.

, & Levy,

(2015). Mild closed head injury promotes a selective trigeminal hypernociception: implications for the acute emergence of post-traumatic headache. Eur J Pain, 19(5), 621–628. doi: 10.1002/ejp.583

15.

Bomyea,

, Lang,

A. J.

, Delano-Wood,

, Jak,

, Hanson,

K. L.

, Sorg,

,... Schiehser,

D. M.

(2016). Neuropsychiatric Predictors of Post-Injury Headache After Mild-Moderate Traumatic Brain Injury in Veterans. Headache, 56(4), 699–710. doi: 10.1111/head.12799

16.

Born,

R. T. B D.C.

(2005). Structure and Function of Visual Area MT. Annu Rev Neurosci, 28, 157–189.

17.

Bourne,

J. A. R M.G.P.

(2006). Hierachical development of the primate visual cortex, as revealed by neurofilament immunoreactivity: early maturation of the middle temporal (MT) area. Cereb Cortex, 16, 405–414.

18.

Bree,

, Stratton,

, & Levy,

(2020). Increased severity of closed head injury or repetitive subconcussive head impacts enhances post-traumatic headache-like behaviors in a rat model. Cephalalgia, 40(11), 1224–1239. doi: 10.1177/0333102420937664

19.

Brown,

, & Camarinos,

(2019). The Role of Physical Therapy in Concussion Rehabilitation. Semin Pediatr Neurol, 30, 68–78. doi: 10.1016/j.spen.2019.03.011

20.

Burstein,

, Noseda,

, & Fulton,

A. B.

(2019). Neurobiology of Photophobia. J Neuroophthalmol, 39(1), 94–102. doi: 10.1097/WNO.0000000000000766

21.

Caprara,

, Leticia,

, Rissardo,

J. P.

, Leite,

M. T. B.

, Silveira,

J. O. F.

, Jauris,

P. G. M.

,... Fighera,

M. R.

(2020). Characteristics of Post-Ictal Headaches in Patients with Epilepsy: a Longitudinal Study. Seizure, 81, 244–249. doi: 10.1016/j.seizure.2020.08.001

22.

Cheever,

, McDevitt,

, Phillips,

, & Kawata,

(2021). The Role of Cervical Symptoms in Post-concussion Management: A Systematic Review. Sports Med. doi:10.1007/s40279-021-01469-y

23.

Ciarlone,

S. L.

, Statz,

J. K.

, Goodrich,

J. A.

, Norris,

J. N.

, Goforth,

C. W.

, Ahlers,

S. T.

, & Tschiffely,

A. E.

(2020). Neuroendocrine function and associated mental health outcomes following mild traumatic brain injury in OEF-deployed service members. J Neurosci Res, 98(6), 1174–1187. doi: 10.1002/jnr.24604

24.

Ciuffreda,

K. J.

, Han,

M. E.

, Tannen,

, & Rutner,

(2021). Visual snow syndrome: evolving neuro-optometric considerations in concussion/mild traumatic brain injury. Concussion, 6(2), CNC89. doi: 10.2217/cnc-2021-0003

25.

Ciuffreda,

K. J. L. D.

, Yadav,

N. K

, & Thiagarajan

(2016). Traumatic Brain Injury: Visual consequences, diagnosis and treatment. Advances in Ophthalmology and Optometry, 1, 307–333.

26.

Curcio,

C. A. S., K.R.

, & Henrickson

R. E. ,A. E.

(1990). Human photoreceptor topography. J Comp Neurol, 292(4), 497–532.

27.

D.J., C. (2012). Chapter 10: Sensory System Changes Functional Movement Development Across Lifespan (3rd Edition): Elsevier.

28.

Delaruelle,

, Ivanova,

T. A.

, Khan,

, Negro,

, Ornello,

, Raffaelli,

,... European Headache Federation School of Advanced, S. (2018). Male and female sex hormones in primary headaches. J Headache Pain, 19(1), 117. doi: 10.1186/s10194-018-0922-7

29.

Derrington,

A. M. L P.

(1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. J Physiol, 357, 219–240.

30.

Diel,

R. J.

, Mehra,

, Kardon,

, Buse,

D. C.

, Moulton,

, & Galor,

(2021). Photophobia: shared pathophysiology underlying dry eye disease, migraine and traumatic brain injury leading to central neuroplasticity of the trigeminothalamic pathway. Br J Ophthalmol, 105(6), 751–760. doi: 10.1136/bjophthalmol-2020-316417

31.

Diel,

R. J. M D.

; Kardon

, Buse,

D.C.

, Moulton,

, & Galor,

(2021). Photophobia: Shared pathophysiolgy underlying dry eye disease, migraine and traumatic brain injury leading to central neuroplasticity of the trigeminothalamic pathway. Br J Ophthalmol, 105(6), 751–760.

32.

Digre,

K. B.

, & Brennan,

K. C.

(2012). Shedding light on photophobia. J Neuroophthalmol, 32(1), 68–81. doi: 10.1097/WNO.0b013e3182474548

33.

Dise-Lewis,

J. E.

, Forster,

J. E.

, McAvoy,

, Stearns-Yoder,

K. A.

, Bahraini,

N. H.

, Laker,

S. R.

, & Brenner,

L. A.

(2019). The Natural History of Postconcussion Recovery Among High School Athletes. J Head Trauma Rehabil, 34(5), E36–E44. doi: 10.1097/HTR.0000000000000469

34.

Edlmann,

, Whitfield,

P. C.

, Kolias,

, & Hutchinson,

P. J.

(2021). Pathogenesis of Chronic Subdural Hematoma: A Cohort Evidencing De Novo and Transformational Origins. J Neurotrauma. doi:10.1089/neu.2020.7574

35.

Esce,

A. R.

, Chavarri,

V. M.

, Joshi,

A. B.

, & Meiklejohn,

D. A.

(2021). Evaluation of Antibiotic Prophylaxis for Acute Nonoperative Orbital Fractures. Ophthalmic Plast Reconstr Surg. doi:10.1097/IOP.0000000000001915

36.

Felleman

DJ, V. E. D.

(1991). Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex, 1(1), 1–47.

37.

Filipovic,

, de Ru,

J. A.

, van de Langenberg,

, Borggreven,

P. A.

, Lackovic,

, & Lohuis,

(2017). Decompression endoscopic surgery for frontal secondary headache attributed to supraorbital and supratrochlear nerve entrapment: a comprehensive review. Eur Arch Otorhinolaryngol, 274(5), 2093–2106. doi: 10.1007/s00405-017-4450-x

38.

Filippopulos,

F. M.

, Goeschy,

, Schoeberl,

, Eren,

O. E.

, Straube,

, & Eggert,

(2021). Reflexive and Intentional Saccadic Eye Movements in Migraineurs. Front Neurol, 12, 669922. doi: 10.3389/fneur.2021.669922

39.

Firth,

A. Y.

(2005). Heroin and diplopia. Addiction, 100(1), 46–50. doi: 10.1111/j.1360-0443.2005.00915.x

40.

Fralick,

M. T D.

Tien

H.C.;

, & Redelmeier,

D. A.

(2016). Risk of suicide after a concussion. Can Med Assoc J, 188(7), 497–504.

41.

Gallaway,

M. S M.

, & Lynn Mitchell,

(2017). Visoin Therapy ofr post Concussion Vision Disorders. Optom Vis Sci, 94(1), 68–73.

42.

Gamlin,

P. D.

(2002). Neural mechanisms for the control of vergence eye movements. Ann N Y Acad Sci, 956, 264–272.

43.

Garcia-Munoz,

, Carbonell-Bonete,

, & Cacho-Martinez,

(2014). Symptomatology associated with accommodative and binocular vision anomalies. J Optom, 7(4), 178–192. doi: 10.1016/j.optom.2014.06.005

44.

Giammattei,

, Messerer,

, Daniel,

R. T.

, Aghakhani,

, & Parker,

(2020). Long-term outcome of surgical treatment of Chiari malformation without syringomyelia. J Neurosurg Sci, 64(4), 364–368. doi: 10.23736/S0390-5616.17.04063-2

45.

Gil,

, & Decq,

(2021). How similar are whiplash and mild traumatic brain injury? A systematic review. Neurochirurgie, 67(3), 238–243. doi: 10.1016/j.neuchi.2021.01.016

46.

Gilaie-Dotan,

(2016). Visual motion serves but is not under the purview of the doral pathway. Neuropsychologia, 89, 378–392.

47.

Gkekas,

, Primikiris,

, & Georgakoulias,

(2014). Acute onset of trigeminal neuralgia, facial paresis and dysphagia after mild head injury. Br J Neurosurg, 28(1), 122–124. doi: 10.3109/02688697.2013.815327

48.

GL, I. (2006). Complicated vs uncomplicated mild traumatic brain injury: acute neuropsychological outcome. Brain Inj, 20(13), 1335–1344.

49.

Gouveia,

R. G.

, Parreira,

, & Pavao Martins,

(2005). Autonomic features in cluster headache. Exploratory factor analysis. J Headache Pain, 6(1), 20–23. doi: 10.1007/s10194-005-0146-5

50.

Harrington,

B. M.

, Gretschel,

, Lombard,

, Lonser,

R. R.

, & Vlok,

A. J.

(2020). Complications, outcomes, and management strategies of non-missile penetrating head injuries. J Neurosurg, 134(5), 1658–1666. doi: 10.3171/2020.4.JNS20122

51.

Hayne,

D. P.

, & Martin,

P. R.

(2019). Relating Photophobia, Visual Aura, and Visual Triggers of Headache and Migraine. Headache, 59(3), 430–442. doi: 10.1111/head.13486

52.

Helling,

, & McKinlay,

A. J.

(2005). Considerations for the head-injured air-evacuated patient: a case report of frontal sinus fracture and review of the literature. Mil Med, 170(7), 577–579. doi: 10.7205/milmed.170.7.577

53.

Herdman

SJ, C. R.

(2014). Anatomy and Physiology of the Normal Vestibular System Vestibular Rehabilitation, Contemporary Perspectives in Rehabilitation (CPR): Jaypee Brothers Medical Publications Ltd.

54.

Herrero Babiloni,

, Exposto,

F. G.

, Bouferguene,

, Costa,

, Lavigne,

G. J.

, & Arbour,

(2020). Temporomandibular Disorders in Traumatic Brain Injury Patients: A Chronic Pain Condition Requiring Further Attention. Pain Med, 21(12), 3260–3262. doi: 10.1093/pm/pnaa234

55.

Ibanez,

, Navallas,

, de Caceres,

I. A.

, Martinez-Chamorro,

, & Borruel,

(2021). CT Features of Posttraumatic Vision Loss. AJR Am J Roentgenol, 217(2), 469–479. doi: 10.2214/AJR.20.24164

56.

Isaacs,

K. H.

, & Geracioti,

T. D.

(2015). Post-TBI central hypogonadism and PTSD. Am J Psychiatry, 172(11), 1160. doi: 10.1176/appi.ajp.2015.15060750

57.

Ismailov,

R. M.

, & Lytle,

J. M.

(2016). Traumatic Brain Injury: Its Outcomes and High Altitude. J Spec Oper Med, 16(1), 67–69.

58.

Jacotte-Simancas,

, Fucich,

E. A.

, Stielper,

Z. F.

, & Molina,

P. E.

(2021). Traumatic brain injury and the misuse of alcohol, opioids, and cannabis. Int Rev Neurobiol, 157, 195–243. doi: 10.1016/bs.irn.2020.09.003

59.

Jaschinski,

, Konig,

, Mekontso,

T. M.

, Ohlendorf,

, & Welscher,

(2015). Computer vision syndrome in presbyopia and beginning presbyopia: effects of spectacle lens type. Clin Exp Optom, 98(3), 228–233. doi: 10.1111/cxo.12248

60.

Kamins,

, Richards,

, Barney,

B. J.

, Locandro,

, Pacchia,

C. F.

, Charles,

A. C.

,... Blume,

H. K.

(2021). Evaluation of Posttraumatic Headache Phenotype and Recovery Time After Youth Concussion. JAMA Netw Open, 4(3), e211312. doi: 10.1001/jamanetworkopen.2021.1312

61.

Kennedy,

, Quinn,

, Chapple,

, & Tumilty,

(2019). Can the Neck Contribute to Persistent Symptoms Post Concussion? A Prospective Descriptive Case Series. J Orthop Sports Phys Ther, 49(11), 845–854. doi: 10.2519/jospt.2019.8547

62.

Khalili,

, Kashkooli,

N. R.

, Niakan,

, & Asadi-Pooya,

A. A.

(2021). Risk factors for post-traumatic epilepsy. Seizure, 89, 81–84. doi: 10.1016/j.seizure.2021.05.004

63.

Killgore,

W. D. S. V J.R.

; Shane,

B.R.

, Weber,

, & Bajaj,

(2020). A randomized, double-blind, placebo-controlled trial of blue wavelength on light exposure on sleep and recovery of brain structure, function, and cognition following mild traumatic brain injury. Neurobiol Dis, 134, 1–16.

64.

Kontos,

A. P.

, Collins,

M. W.

, Holland,

C. L.

, Reeves,

V. L.

, Edelman,

, Benso,

,... Okonkwo,

(2018). Preliminary Evidence for Improvement in Symptoms, Cognitive, Vestibular, and Oculomotor Outcomes Following Targeted Intervention with Chronic mTBI Patients. Mil Med, 183(suppl_1), 333–338. doi: 10.1093/milmed/usx172

65.

Kontos,

A. P. E R.J

; Trbovich

, Womble,

; Said,

; Sumrok,

S V.F.

; French,

, Kegel,

; Puskar,

; Sherry,

; Holland,

, & Collins,

(2020). Concussion Clincial Profiles Screening (CP Screen) Tool: Preliminary Evicence to Inform a Multidisciplinary Approach. Neurosurgery, 87(2), 348–356.

66.

Kulas,

J. F.

, & Rosenheck,

R. A.

(2018). A Comparison of Veterans with Post-traumatic Stress Disorder, with Mild Traumatic Brain Injury and with Both Disorders: Understanding Multimorbidity. Mil Med, 183(3-4), e114–e122. doi: 10.1093/milmed/usx050

67.

Kuperman,

, Granovsky,

, Fadel,

, Bosak,

, Buxbaum,

, Hadad,

,... Granot,

(2021). Head- and neck-related symptoms post-motor vehicle collision (MVC): Separate entities or two-sides of the same coin?Injury, 52(5), 1227–1233. doi: 10.1016/j.injury.2021.03.003

68.

Lachkar,

Y. B. W.

(2007). Drug induced acute angle closure glaucoma. Curr Opin Ophthalmol, 18(2), 129–133.

69.

Laguerre,

, McGargill,

, & Herman,

D. C.

(2020). Occipital Neuralgia - A Masquerading Cause of Concussion Symptoms. Curr Sports Med Rep, 19(9), 344. doi: 10.1249/JSR.0000000000000745

70.

Lovell,

M. C. M. B J.

(2004). Return to play following sports related concussion. Clin Sports Med, 23(3), 421–441.

71.

Main,

A. V I.

, & Dowson,

(2000). The Wavelenth of Light causing Photophobia in Migraine and Tension-Type Headache between Attacks. Headache, 40(3), 194–199.

72.

Mantokoudis,

G. S. T., A.S.

; Wozniak

, Eidenberger,

; Kattah,

J.C.

; Guede,

C.I.

, Zee,

D.S.

, & Newman-Toker,

D.E.

(2016). 26. 4, 375-385.

73.

Marshall,

S. B., M.

; McCullagh

; Velikonja,

; Berrigan,

; Ouchterlony,

, & Weeger,

(2015). Updated clinical practice guidelines for concussion / mild traumatic brain injury and persistent symptoms. Brain Inj, 29(6), 688–700.

74.

Master,

C. L., S. M.

, Gallaway,

, Goodman,

, Robinson,

R. L.

, Master,

S. R.

, & Grady,

M. F.

(2016). Vision diagnoses are common after concussion in adolescents. Clin Pediatr (Phila), 55(3), 260–267.

75.

Mathew,

P. G.

, & Cooper,

(2021). The Diagnosis and Management of Posttraumatic Headache with Associated Painful Cranial Neuralgias: a Review and Case Series. Curr Pain Headache Rep, 25(8), 54. doi: 10.1007/s11916-021-00969-w

76.

Matuszak,

J. M. M., J.

; McPherson,

; Wiler,

, & Leddy,

(2016). A Practical Concussion Physical Examination Toolbox. Sports Health, 8(3), 260–269.

77.

McKendrick,

A. M.

, & Badcock,

D. R.

(2004). Decreased visual field sensitivity measured day, then week, after migraine. Invest Ophthalmol Vis Sci, 45(4), 1061–1070. doi: 10.1167/iovs.03-0936

78.

Mehta,

D. G.

, Garza,

, & Robertson,

C. E.

(2021). Two hundred and forty-eight cases of visual snow: A review of potential inciting events and contributing comorbidities. Cephalalgia, 333102421996355. doi:10.1177/0333102421996355

79.

Park,

J. H. K., J.W.

(2019). Chapter 17: Neurosensory diagnostic techniques for mild traumatic brain injury. In B. C. D. Hoffer M.E (Ed.), Neurosensory Disorders in Mild Traumatic Brain Injury (pp. 279–295): Academic Press (Elsevier).

80.

Patel,

R. D.

, & LaBella,

C. R.

(2021). Contributions of PCSS, CISS, and VOMS for Identifying Vestibular/Ocular Motor Deficits in Pediatric Concussions. Sports Health, 1941738121994116. doi:10.1177/1941738121994116

81.

Petersen,

L. O.

, Ipsen,

E. O.

, Felding,

U. A.

, von Buchwald,

, & Steinmetz,

(2021). Sequelae of Major Trauma Patients with Maxillofacial Fractures. Ann Otol Rhinol Laryngol, 130(5), 475–482. doi: 10.1177/0003489420958732

82.

Pilo-de-la-Fuente,

, Gonzalez Martin-Moro,

, Navacerrada,

, Plaza-Nieto,

F. J

, & Jimenez-Jimenez,

F. J.

(2013). Concentric visual field defect related to spontaneous intracranial hypotension. Int Ophthalmol, 33(5), 583–587. doi: 10.1007/s10792-012-9699-x

83.

Poltavski,

D. V. B. D.

(2014). Screening for lifetime concussion in atheletes: Importance of oculomotor measures. Brain Inj, 28(4), 475–485.

84.

Prevention, N. C. f. I. P. a. C. D. o. U. I. (2015). Report to Congress on Traumatic Brain Injury in the USA. Epidemiology and Rehabilitation. Retrieved from Report to Congress:.

85.

Purpura,

, Kaplan,

, & Shapley,

R. M.

(1988). Background light and the contrast gain of primate P and M retinal ganglion cells. Proc Natl Acad Sci U S A, 85(12), 4534–4537.

86.

Roorda,

A. W. D.R.

(1999). The arrangement of the three cone classes in the living human eye. Nature, 397(6719), S20–S22.

87.

Rumalla,

, Smith,

K. A.

, Letchuman,

, Gandham,

, Kombathula,

, & Arnold,

P. M.

(2018). Nationwide incidence and risk factors for posttraumatic seizures in children with traumatic brain injury. J Neurosurg Pediatr, 22(6), 684–693. doi: 10.3171/2018.6.PEDS1813

88.

Schankin,

C. J.

, Maniyar,

F. H.

, Sprenger,

, Chou,

D. E.

, Eller,

, & Goadsby,

P. J.

(2014). The relation between migraine, typical migraine aura and “visual snow”. Headache, 54(6), 957–966. doi: 10.1111/head.12378

89.

Scher,

A. I.

, McGinley,

J. S.

, Wirth,

R. J.

, Lipton,

R. B.

, Terrio,

, Brenner,

L. A

,... Schwab,

(2021). Headache complexity (number of symptom features) differentiates post-traumatic from non-traumatic headaches. Cephalalgia, 41(5), 582–592. doi: 10.1177/0333102420974352

90.

Seidemann,

E. P., A. B.

, Wandell

B. A.

, & Newsome

W. T.

(1999). Color Signals in Area MT of the Macaque Monkey. Neuron, 24, 911–917.

91.

Shah,

, & Hameed,

(2021). Muscle Contraction Tension Headache StatPearls. Treasure Island (FL).

92.

Shepherd,

A. J.

, & Joly-Mascheroni,

R. M.

(2017). Visual motion processing in migraine: Enhanced motion after-effects are related to display contrast, visual symptoms, visual triggers and attack frequency. Cephalalgia, 37(4), 315–326. doi: 10.1177/0333102416640519

93.

Shepherd,

, Landon,

, Kalloor,

, Barker-Collo,

, Starkey,

, Jones,

,... Group, B. R. (2020). The association between health-related quality of life and noise or light sensitivity in survivors of a mild traumatic brain injury. Qual Life Res, 29(3), 665–672. doi: 10.1007/s11136-019-02346-y

94.

Silberstein,

S. D.

(2015). Migraine Treatment: Continuum (Minneap.Minn. Headache, 21(4), 973–989.

95.

Singman,

(2020).

96.

Singman

E. L.

; Daphalapurkar

N. W H.

; Nguyen,

T. D.

; Panghat,

; Chang,

, & McCulley,

(2016). Indirect traumatic optic neuropathy. Mil Med Res, 3(2), 1–6.

97.

Singman,

E. L.

, & Quaid,

P. T.

(2019). Chapter 15: Vision Disorders in Mild Traumatic Brain Injury. In B. C. D. Hoffer M.E (Ed.), Neurosensory Disorders in Mild Traumatic Brain Injury: Academic Press (Elselvier).

98.

Singman,

E. L.

, Matta,

N. S.

, & Silbert,

D. I.

(2014). Convergence insufficiency associated with migraine: a case series. Am Orthopt J, 64, 112–116. doi: 10.3368/aoj.64.1.112

99.

Sirko,

, Mizyakina,

, & Chekha,

(2021). Post-Traumatic Headache. Current Views on Pathophysiological Mechanisms of Development and Clinical Specifics (Review). Georgian Med News (313), 60-65.

100.

Spencer,

, & Leach,

(2017). Asymptomatic Chiari Type I malformation: should patients be advised against participation in contact sports?Br J Neurosurg, 31(4), 415–421. doi: 10.1080/02688697.2017.1297767

101.

Spiegel,

S. J.

, & Moss,

H. E.

(2021). Neuro-Ophthalmic Emergencies. Neurol Clin, 39(2), 631–647. doi: 10.1016/j.ncl.2021.01.004

102.

Stan,

, Stan,

, & Rednik,

A. M.

(2020). Migraine or Acute Angle Closure?Rom J Ophthalmol, 64(3), 310–312.

103.

Stewart,

, Boyce,

, & McGlone,

(2012). Post-traumatic headache: don’t forget to test the supraorbital nerve! BMJ Case Rep, 2012. doi:10.1136/bcr-2012-006936

104.

Stillman,

M. J.

(2006). Testosterone replacement therapy for treatment refractory cluster headache. Headache, 46(6), 925–933. doi: 10.1111/j.1526-4610.2006.00436.x

105.

Sutton,

, Chan,

, Escobar,

, Mollayeva,

, Hu,

, & Colantonio,

(2019). Neck Injury Comorbidity in Concussion-Related Emergency Department Visits: A Population-Based Study of Sex Differences Across the Life Span. J Womens Health (Larchmt), 28(4), 473–482. doi: 10.1089/jwh.2018.7282

106.

Tadevosyan,

, & Kornbluth,

(2021). Brain Herniation and Intracranial Hypertension. Neurol Clin, 39(2), 293–318. doi: 10.1016/j.ncl.2021.02.005

107.

Takemura,

A. I. Y.

, Kawano

; Quaia

, & Miles

F. A.

(2001). Single unit activity in cortical area MST associated with disparity-vergence eye movements: evidence for population coding. J Neurophysiol, 85(5), 2246–2266.

108.

Theeler

BJ, F. F

, & Erickson,

J. C.

(2010). Headaches after concussion in US soldiers returning from Iraq or Afghanistan. Headache, 50(8), 1262–1272.

109.

Thiagarajan

P. C. K. J.

, Versional eye tracking in mild tramatic brain injury (mTBI): effects of oculomotor training (OMT. Brain Inj, 28(7), 930–943.

110.

Thiagarajan,

P. C. K. J.

(2014). Effect of oculomotor rehabilitation on accommodative responsivity in mild traumatic brain injury. J Rehabil Res Dev, 51(2), 175–191.

111.

Thiagarajan,

P. C. K. J. C.-A. J.E.

; Ludlam

D.P.

, & Kapoor

(2014). Oculomotor neurorehabilitation for reading in mild traumatic brain injury (mTBI): an integrative approach. NeuroRehabilitation, 34(1), 129–146.

112.

Thiagarajan,

P. C. K. J. L. D.P.

(2011). Vergence dysfunction in mild traumatic brain injury (mTBI): a review. Ophthalmic Physiol Opt, 31(5), 456–468.

113.

Thompson,

B. M., C.J.D.

; Chakraborty,

; Anstice,

N.S.

; Jacobs,

R.J.

; Paudel,

; Yu,

; Ansell,

J.M.

; Wouldes,

T.A.

, & Harding,

J.E.

, CHYLD Team. (2017). Global motion perception is associated with motor function in 2-year-old children. Neuroscience, 658(177-181), 177.

114.

Trotter,

Y. C. S.

, Stricanne;

; Thorpe,

, & Imbert,

(1996). Neural processing of stereopsis as a function of viewing distance in primate visual cortex area V. J Neurophysiol, 76(5), 2872–2885.

115.

Tse,

D. M.

, Titchener,

A. G

, Sarkies,

, & Robinson,

(2009). Acute angle closure glaucoma following head and orbital trauma. Emerg Med J, 26(12), 913. doi: 10.1136/emj.2008.071720

116.

Vernau,

B. T. G., M. F.

, Goodman,

; Wiebe,

D. J.

; Basta,

; Park,

; Arbogast,

K. B.

, & Master,

C. L.

(2015). Oculomotor and neurocognitive assessment of youth ice hockey players: baseline associations and observations after concussion. Dev Neuropsychol, 40(1), 7–11.

117.

Viana,

, Puledda,

, & Goadsby,

P. J.

(2020). Visual snow syndrome: a comparison between an Italian and British population. Eur J Neurol, 27(10), 2099–2101. doi: 10.1111/ene.14369.

118.

Walker,

W. C.

, Hirsch,

, Carne,

, Nolen,

, Cifu,

D. X.

, Wilde,

E. A.

,... Williams,

(2018). Chronic Effects of Neurotrauma Consortium (CENC) multicentre study interim analysis: Differences between participants with positive versus negative mild TBI histories. Brain Inj, 32(9), 1079–1089. doi: 10.1080/02699052.2018.1479041

119.

Walsh,

D. V.

, Capo-Aponte,

J. E.

, Jorgensen-Wagers,

, Temme,

L. A.

, Goodrich,

, Sosa,

, & Riggs,

D. W.

(2015). Visual field dysfunctions in warfighters during different stages following blast and nonblast mTBI. Mil Med, 180(2), 178–185. doi: 10.7205/MILMED-D-14-00230

120.

Weatherby,

T. J. M.

, Raman,

V. R. V.

, & Agius,

(2019). Depression and dry eye disease: a need for an interdisciplinary approach?Psychiatr Danub, 31(Suppl 3), 619–621.

121.

Weinacht,

S. K. C.

; Monting,

, J. S.;,

, & Gottlob,

(1999). Visual development in pre-term and full-term infacts: a prospective masked study. Invest Ophthalmol Vis Sci, 40(2), 346–353.

122.

Wennberg,

, Hiploylee,

, Tai,

, & Tator,

C. H.

(2018). Is Concussion a Risk Factor for Epilepsy?Can J Neurol Sci, 45(3), 275–282. doi: 10.1017/cjn.2017.300

123.

Whitney,

S. L.

, & Sparto,

P. J.

(2019). Eye Movements, Dizziness, and Mild Traumatic Brain Injury (mTBI): A Topical Review of Emerging Evidence and Screening Measures. S-S. J Neurol Phys Ther, 43(Suppl 2), 36. doi: 10.1097/NPT.0000000000000272

124.

Widmer,

D. E. O., T.S.

; Limbachia

; Kulp,

M.T.

; O’Toole,

A.J.

; Kashou,

N.H.

, & Fogt,

(2018). Post-therapy Functional Magnetic Resonance Imaging in Adults with Symptomatic Convergence Insufficiency. Optom Vis Sci, 95(6), 505–514.

125.

Wilkins,

A. J.

, Haigh,

S. M.

, Mahroo,

O. A.

, & Plant,

G. T.

(2021). Photophobia in migraine: A symptom cluster? Cephalalgia, 3331024211014633. doi:10.1177/03331024211014633

126.

Williams

DH, L. H

, & Eisenberg

HM.

(1990). Mild head injury classification. Neurosurgery, 27(3), 422–428.

127.

Woodward,

J. A

, & Adler,

D. E.

(2018). Chiari I malformation with acute neurological deficit after craniocervical trauma: Case report, imaging, and anatomic considerations. Surg Neurol Int, 9, 88. doi: 10.4103/sni.sni_304_16

128.

Xu,

X. M. L., Y.

; Dong

M. X.

; Zou,

D. Z.

, & Wei,

Y. D.

(2017). Tricyclic Anti-Depressants for preventing Migraine in Adults. Medicine (Baltimore), 96(22), e6989.

129.

Yang,

M. C. L. K.Y.

(2019). Drug induced Acute Angle Closure Glaucoma: A Review. J Curr Glaucoma Pract, 13(3), 104–109.

130.

Zhao,

Z. C. Z., Y.

; Tan

, & Li

(2018). Research progress about the effect and prevention of blue light on eyes. Int J Ophthalmol, 11(12), 1999–2003. doi: 10.18240.ijo.2018.12.20

131.

Zivcevska,

M. L., S.

; Blakeman,

, MacGregor,

, Goltz,

H. C.

, & Wong,

A. M.

(2020). Investigation of light-induced lacrimation and pupillary responses in episodic migraine. PLoS One, 15, e2411490. doi: 10.1371/journal.pone.0241490