The Eyes and dys­functional, the central nervous system does Proprioception not recognize the correct status of tonicity of the muscles at rest or in movement, does not 1 Orlando Alves da Silva, MD integrate correctly the information that comes Teresa Alves da Silva, MD2 from sensory receptors, and has difficulty in modulating multisensorial integration, with 1Posturmed, Lisbon, Portugal consequences in motor behavior and cognitive 2 Hospital de Cascais, Dept. of functions. Orthopedics, Cascais, Portugal This results in a wide range of proprioceptive Editor’s Note: This article, principally abnormalities which are clinically related, are authored by O. Alves Da Silva, MD, treated together, and are termed as Postural is an invited paper. When I first Deficiency Syndrome (PDS) or more recently

ARTICLE became aware of Dr. Da Silva’s work Proprioceptive Dysfunction Syndrome. with prisms and proprioception, I encouraged him to share his experiences The author has personally observed more than as a pioneering ophthal­mologist in Lisbon, 40,000 patients suffering from this condition Portugal. Many of our readers will be aware of during the last 40 years and devised an active pioneering optometric involvement in this field. prism therapeutic protocol that is based on It was not Dr. Da Silva’s charge to review this, as the knowledge that small modifications of the has been amply done elsewhere (see here for muscular tonus of the oculomotor muscles can example: http://bit.ly/2Z6bYv0). For additional change the tonus of the axial paravertebral background, see the editorial in this issue. muscles.

This paper describes PDS diagnosis and pro­ ABSTRACT vides explanation of the updated active prism The proprioceptive system has an extensive protocol aimed toward vision professionals. influence on the maintenance of human health. When the proprioceptive system is Introduction This paper will introduce you to a relatively Correspondence regarding this article should be emailed to Orlando Alves da Silva, MD, at o.alvesdasilva@ unknown clinical entity that affects millions of gmail.com. All statements­ are the authors’ personal people and may have an ophthalmologic basis opinions and may not reflect the opinions of the for its treatment. This condition is historically College of Optometrists in Vision Development, Vision Development & Rehabilitation or any institution­ or called Postural Deficiency Syndrome (PDS) organization to which the authors may be affiliated. or in a more recent nomenclature Proprio­ Permission to use reprints of this article must be obtained from the editor. Copyright 2019 College of Optometrists ception Dysfunction Syndrome (PDS). The in Vision Development. VDR is indexed in the Directory understanding of its pathophysiology and of Open Access Journals. Online access is available at rationale for treatment entails a broad covd.org. https://doi.org/10.31707/VDR2019.5.2.p130 knowledge of neuroscience­ and neuro- Alves da Silva O. The eyes and proprioception. Vision ophthalmology. It also requires reconsideration Dev & Rehab 2019;5(2):130-47. of how oculomotor muscles can interfere with body postural tonus and cognitive brain Keywords: active prisms, functions. Our emphasis is on newer concepts Postural Deficiency Syndrome (PDS), about visual function and motor actions, Proprioception Dysfunction Syndrome, and how they can affect multi-sensory brain Proprioceptive System integration. We share how the evolution in

130 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 our thinking and approach has lead toward a axon terminations and mechanoreceptors paradigm shift in the application of prism and present in muscles, joint and organ capsules, complementary interventions for PDS. ligaments and enthesis (the connective tissue between tendon or ligament and bone). The What is proprioception? proprioceptive information can be transmitted Proprioception is the sense of self, the to the central nervous system by conscious and body’s conscious awareness of movement subconscious pathways. and position. It’s the sense necessary for brain The sensory information that becomes integration of the corporal limits, and necessary conscious is transmitted by the ascending for conscious and subconscious knowledge sensory tracts of Goll and Burdach. These of the relation between each segment of the pathways convey fibers for position sense and body, and between the body and environmental fine cutaneous sensation (touch, vibration, fine space around it. pressure and two point discrimination). They The idea that humans are limited to five are crossed pathways that travel from their senses comes from the Greek philosopher receptors through the spinal cord dorsal root, Aristotle. This is a 2500 year-old concept that medulla nuclei, midbrain and thalamus until is scientifically outdated. Proprioception has they reach the primary somatosensory area of been revealed as the sixth sense for more than cerebral cortex. 100 years. The subconscious sensory information is Taking this a step further, the French scien­ conveyed by ascending tracts, crossed and tist J.P. Roll refers to proprioception as our uncrossed, that go through the dorsal spinal first sense, “the sense that makes sense of our cord and medulla oblongata, terminating at senses”, signaling its importance.29,31,30 It is the cerebellum. The most well known of these believed to be present in all animal species and ascending tracts are the anterior and posterior is necessary to keep them alive. Even during spinocerebellar tracts and the cuneocerebellar the earliest stages of human evolution, normal tract that convey information from the lower proprioception was an essential sense.16 Faulty and upper body. proprioception can lead to a loss of precision in But we must not forget the other two movement or misperception of environmental important subconscious tracts most relevant dangers, with severe consequences for survival for our purposes, the spinotectal tract and mechanisms. While accurate proprioception is the spinoreticular tract. The spinotectal tract not a condition of survival in modern times in provides information for spinovisual reflexes most regions of the world, its deficits contribute and brings about movements of the eyes and to a range of motor and cognitive dysfunctions head toward the source of stimulation. The in our society that have serious consequences in spinoreticular tract provides cutaneous and quality of life, as will be illustrated in this paper. muscular afferent information for the reticular formation. What is the Proprioceptive System? The reticular formation in the brainstem As with our other sensory modalities, pro­ is a heterogeneous structure with no clear prio­ception should be conceived as a system boundaries between its nuclei, but is highly rather than as an isolated sense. The origin organized. It is home to numerous nuclei of this concept can be traced to Sherrington, and ascending and descending tracts, with who described it extensively in his treatise on projections between them that are involved physiology in 1906.34 in modulating sensory and motor functions. The proprioceptive system has its neurologic The reticular formation is also home to groups afferents in the muscle spindles, extrafusal of cells that produce neurotransmitters that

131 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 are sent to different areas throughout the and subconscious activities, and is responsible central nervous system to modulate sensory for modulating activity of pre-motor networks perception, motor activity and behavioral and ensure coordinated motor output. responses. Reticular formation neurons also Proprioception therefore extends far beyond establish circuits within the motor nuclei of the muscular tonus, equilibrium, joint movement cranial nerves, modulating the motor activity and postural control, as is usually presented in of the gastrointestinal system, respiratory health sciences education. We can summarize system and cardiovascular system. The same by stating that the Proprioceptive system has neuronal population also contributes to three overlapping major functions: orofacial motor responses by coordinating the 1) Regulation of muscular tonus. Posture activity of the trigeminal, facial and hypoglossal and body movement is mediated by nuclei. Also found in the reticular formation pro­prioception through the afferent are the descending pathways that help to information it receives from all sensory maintain posture and muscle tone through the receptors, and by the efferent information descending reticulospinal tract. it sends to the extrapyramidal motor This highly complex neuronal organization tracts. is evidence that all senses are related to each 2) Egocentric spatial localization. By inte­ other in the central nervous system, not only by grating and modulating the information simple reflex arcs but in a much more elaborate that comes from sensory receptors, the way that interfaces with cerebellar and cortical proprioceptive system informs the brain pathways. This is the basis of the neurologic about the relative position of the sensory concept of multisensorial integration, a CNS organs, the relation between each body process by which information from different segment, and the relative position of the sensory systems is combined to influence body in the surrounding environment. perception, decisions, motor actions and 3) Modulation of multisensory information. behavior. It is known that spatiotemporal Proprioceptive information known to be concordant cross-modal stimuli, for example transmitted in the multisensorial deep sounds and images, evoke enhanced layers of the superior colliculus in the responses. On the other hand, spatially dispar­ midbrain is believed to have a role in ate stimuli can suppress some responses. modulating multisensory integration. This Multisensory integration has been shown to modulation has consequences in motor enhance and speed the detection, localization, behavior and higher cognitive functions. and reaction to biologically significant events. Neuropsychological studies also demonstrate What is Postural Deficiency Syndrome? its importance in signal disambiguation in Postural Deficiency Syndrome (PDS) was hearing, speech and cognitive functions such described by the physiatrist H. Martins da as learning.35,17 Cunha, M.D. in 1979 as a clinical entity encom­ The proprioceptive system, from its passing multiple symptoms and signs related peripheral sensory components to the central to proprioceptive dysfunction.18 The Postural nervous system pathways, appears to be Deficiency Syndrome (PDS) was originally an important modulator of sensorimotor described as “a clinical entity of functional activity. This concept provides a new basis nature due essentially to an alteration of the for understanding how sensory information ideal biomechanics and to a deficiency of the from peripheral and spinal inputs can be proprioceptive and visual information”.20,22 integrated with information from the brain and Martins da Cunha stated that the patients cerebellum, both higher cognitive functions affected by this condition had in common a

132 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 stereotyped body posture with an asymmetrical its publication, when Martins da Cunha asked paravertebral and thoracic hypertonia associ­ him to study the ophthalmological aspects of ated with an asymmetrical lower limb position his PDS patients who did not seem to fit the and a permanent gaze deviation. pattern of what was expected to be found.19 Over the last 40 years the understanding Martins da Cunha was seeking the answer for of this condition, of its clinical manifestations, three ophthalmological questions: and its underlying neurological pathways has • The first question to be answered was why evolved. This condition is presently understood these patients had difficulty in correctly as a proprioceptive dysfunction with three main localizing the arrow related to the figures characteristics: in the Maddox Wing Test. 1. An impairment of the ocular, stoma­tog­ • The second question was why postural nathic and postural tonic equilibrium. reprogramming exercises normalized this 2. An impairment of egocentric spatial visual test. localization. • The third question was why PDS patients 3. A perceptual impairment disturbing the presented with their primary position of multisensorial brain integration.26,27 gaze altered. This alteration consisted of the following: healthy people, when fixating Therefore, a more comprehensive under­ at distance, present both eye axes parallel, standing of this clinical condition leads to and these are parallel to the sagittal plane. the current nomenclature, designating this In PDS patients both eye axes are still condition as Proprioception Dysfunction syn­ parallel, but are no longer parallel to the drome (PDS), maintaining its acronym. sagittal plane of the body, because of a Since the proprioceptive system is trans­ persistent head and trunk rotation. verse to all of the other body systems, the clinical manifestations of its disturbance cannot The regular devices and methods used in be localized to just one area of the body. ophthalmology at the time were unsatisfactory In addition, patients do not typically present in answering these three questions. The first with all of the possible symptoms. For example, author therefore devised a new method that patient A may present with upper body muscular he called directional scotometry to search pain as the predominant symptom. Patient B for a scientific answer.3 A Clement Clark may present with the predominant symptom synoptophore was equipped with a pair of as lack of balance, and patient C may present simultaneous perception slides (G3 and G4). cognitive impairment as the predominant The slides were shown to the patient in primary symptom. However, patients A, B and C are position, in levoversion and in dextroversion to diagnosed using the same proprioception compare their projection. (Figure 1) dysfunction diagnostic protocol and they Our study showed that in people having respond to the same proprioception dysfunction asymmetrical body posture favoring left treatment protocol. Before discussing the most limb support, a pseudoscotoma occurred common signs and symptoms of PDS as related in which part of the image was missing, only to each of the three main PDS characteristics, when making a version movement toward the some background is in order. opposite side on dextroversion. In contrast, those with postural asymmetry favoring right How Ophthalmologic Disturbances were limb support exhibited a pseudoscotoma only Crucial to the Understanding of PDS on levoversion.21-24 The first author’s (OAS) involvement with Further, we verified that there was a this medical condition began two years prior to consistent relationship between the results of

133 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 A B C D

Figure 1: A. Simultaneous perception Clement Clark slides G3 and G4. B. Synoptophore in primary position. C. Synoptophore arms in dextroversion. D. Synoptophore arms in levoversion directional scotometry and the limb support the side of preferential stance may shift from one the patient presented. For example, when moment to the other. On the “mixed” type you we verified a pseudoscotoma at 20° degrees will have pseudoscotomas in both levoversion in levoversion but no pseudoscotoma in and dextroversion. “Pure” PDS occurs when dextroversion at 20° and 30° degrees, this there is a clear lateral preference in plantar was always related to a strong right lower stance and you can identify the predominant limb support.23 Conversely, when there was a support. In pure cases, the pseudoscotomas pseudoscotoma at 20° degrees in dextroversion occur on only one side of version, on either and no pseudoscotoma in 20° or 30° degrees of levoversion or dextroversion. levoversion, the patient was always supported Within the “mixed” PDS type you can identify on his left lower limb. two different patterns. The “mixed pure” will Therefore, we concluded that in studying present with what we call a concordant postural the patient’s oculomotricity by this method head change, limitation of rotation and head it was possible to identify a pattern of dis- tilt to the same side. The “mixed pure” PDS ease in PDS patients, and establish a clinical patients have pseudoscotomas for symmetrical classification system with diagnostic and angles of version. therapeutic value. The classification system In the “mixed predominant” PDS type, the developed includes six different types of PDS head postural changes are non-concordant based on predominant limb support, postural and the pseudoscotomas are also bilateral, but changes in head extension and rotation, and occur for asymmetrical angles of version. synoptophore results.27,21 For each type, the terms “right” or “left” are This represented major progress because added as subtypes according to the laterality until then, just two types (right and left type) of the findings. could be identified by Martins da Cunha, Historically this was how the classification based only on clinical postural observation. was built, from postural observation to Ultimately this finding would pave the way oculomotor findings, but presently we know for developing our ophthalmologic treatment that the synoptophore analysis is the most protocol. (Table 1) accurate way to identify each type of PDS and prescribe the appropriate treatment.24 Diagnosis and Classification of PDS Nevertheless, clinical examination is abso­ Analyzing the classification system (Table lutely necessary, and one must master the 1) we must consider the strong influence of following clinical tests in order to establish clinical observation on how the diagnostic the diagnosis, and to document the postural classifications evolved. We call PDS “mixed” changes and spatial localization disorders when the patient stands with divergent feet, and characteristic of this syndrome.

134 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 Table 1. Diagnostic classification of PDS and treatment protocol with active prisms. Head Plantar stance Head extension Synoptophore Prismatic lenses Rotation Mixed Pure Divergent feet, side of Head exam is concordant: Pseudoscotomas for 2 Prisms of asymmetrical power preferential stance may Limitation of rotation and head symmetrical angles of version RE 125° LE 55° shift tilt in extension on the same Higher powered prism on the side side of head limitation “farther and shorter” to the same side

Mixed Pure right Divergent feet, plantar Limitation of rotation and head 20°/20° or 30°/30° RE- 3Δ 125° LE- 2Δ 55° stance may shift but with tilt in extension to the right preference for right side

Mixed Pure left Divergent feet, plantar Limitation of rotation and head 20°/20° or 30°/30° RE- 2Δ 125° LE- 3Δ 55° stance may shift but with tilt in extension to the left preference for left side

Mixed Predominant Divergent feet, side of Head exam is not concordant: Pseudoscotomas are 1 Prism preferential stance more Limitation of rotation for one asymmetrical RE 125° or LE 55° clearly defined side and head tilt in extension occur in higher angle of version Prism on the side of higher to the other side to the side of preferential angle of version and plantar stance preferential plantar stance

Mixed Predominant right Divergent feet, plantar Head exam is not concordant 30 ° dextroversion RE 125º stance with preference 20 ° levoversion 2Δ or 3Δ for right side

Mixed Predominant left Divergent feet, plantar Head exam is not concordant: 20 ° dextroversion LE 55º stance with preference Limitation of rotation for one 30 ° levoversion 2Δ or 3Δ for left side side and head tilt in extension to the other side

Pure Clear lateral preference Head exam is not concordant: Pseudoscotoma 1 horizontal prism in plantar stance, stance Limitation of rotation for one only to one side of version RE 180° LE 0° foot in sagittal position side and head tilt in extension the opposite side of plantar Prism on the side of plantar to the other side stance stance, On the opposite side of pseudoscotoma

Pure Right Right plantar stance Head exam is not concordant 20 ° levoversion RE 180° Right foot is sagittal 2Δ or 3Δ

Pure Left Left plantar stance Head exam is not concordant 20 ° dextroversion LE 0° Left foot is sagittal 2Δ or 3Δ

135 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 A. Clinical Tests Necessary for Classification The Mouth Opening Test The Head Extension Test The patient is asked to open the mouth as The patient is asked to extend the head much as he can and this opening is measured. backwards, and the distance from shoulder to In the case of proprioceptive dysfunction there ear on both sides are measured. In the presence can be limitation in mouth opening, and in some of proprioceptive dysfunction, both distances cases very severe. The proprioceptive response are asymmetrical, in spite of the patient having to prism can be dramatic in improving this.4 the sensation that they are symmetrical. The Tonic Convergence Test The Head Rotation Test The examiner moves the tip of a ballpoint The patient is asked to rotate the head to the pen or small size object on the midline toward right side and to the left side as far as he can. In the eyes. The distance at which asthenopia is the presence of proprioceptive dysfunction the experienced, and the distance at which fusion rotation is asymmetrical and limited. is disrupted are measured. In the case of proprioceptive dysfunction B. Clinical Tests Elucidating Altered both distances are remote, with asthenopia Muscular Tonus occurring before 6 inches and loss of converg­ H. Martins da Cunha originally proposed the ence occurring before 4 inches.10,28,2 use of trigger points, which are highly painful under finger pressure. When the patient wears C. Clinical tests elucidating dysperception active prisms to correct postural asymmetry, of spatial localization the pain is eliminated. That was, however, a The Eye-Hand Localization Test (Figure 2) more aggressive test that the first author was The eye-hand test, developed in our clinical not comfortable using. He therefore proposed practice, is described as follows: a pen mark the following standard tests: is drawn on the cutaneous ridge of the first

Figure 2: Example of eye-hand test, illustrating error and accuracy.

136 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 Table 2. The most prevalent symptoms of PDS, categorized by the main characteristic of the condition that they reveal. This is not an exhaustive list and other signs or symptom may be present in this clinical condition. impairment of ocular, stomatognatic and postural tonic impairment of impairment of multisensorial equilibrium impairment of egocentric spatial localization egocentric spatial brain integration impairment of multisensorial brain integration localization Musculoskeletal Ocular signs/ Stomatognatic Sensorial Cognitive signs/ and vasomotor symtoms signs /symptoms impairment symtoms signs/ symptoms

• Convergence • Limitation of • Asymmetrical • Clumsiness • Perceptive • Attention deficit insufficiency mouth opening body posture deafness • Memory • Non patterned • TMJ pain or • Painful muscular • Dyspraxia • Tinnitus impairment visual scotomas clicking contractures • Hyperacusia • Dyslexia • Pseudoscotomas • Malocclusion • Myalgia • Vertigo • Dysgraphia • Monocular • Deglutition • Pyriformis • Dysortographia Diplopia disorders syndrome • Dizziness • Binocular • Cheek our • Backpain • Agoraphobia Diplopia tongue bitting • Chronic fatigue • Poliopia • Breathing • Dysphagia • Claustrophobia disorders • Near exotropia • Headache • Frequent falls • Oculomotor • Migraine discoordination • Skin pallor • Image distortion • Paresthesias interdigital space of the dorsal aspect of the accuracy consistently improved in all cases after hand. An object, the pen, is presented to the treatment with active prisms and there was an patient by the observer within a comfortable established relation between the improvement grasping distance, on the contralateral side of of eye-hand accuracy and the normalization of the hand to be tested. The patient is asked head tilt as well as the gain in head rotation. to hit the pen with the hand mark while The eye-hand test can therefore be used as a regarding it, as quickly and as accurately as valuable diagnostic tool as well as a treatment possible, and to avoid final correction of the assessment instrument. trajectories. The observer then verifies if the Other spatial localization tests can be used patient hit the target correctly or if the target to show the patient and his family that there is was hit by any other finger region distant from something wrong concerning his proprioception. the drawn mark. The following are some examples: This test is believed to evaluate sensorimotor transformation involving eye, head, hand, and Mirror test: H. Martins da Cunha used to postural systems. It is a functional test that ask the patients to place themselves in a probably evaluates the well described function straight standing position in front of a mirror of the superior colliculus in reaching movements with their eyes closed. He then asked them and its role in orienting gaze and arms toward to open their eyes and see the difference a target. It differs from other common pointing between their body perception and reality. tests that evaluate cerebellar function, visual acuity or fine hand motricity related to another Feet position test: The patient is asked to neurologic pathways. close his eyes and copy the position of his The test has been validated using kinematic feet with his hands. When opening his eyes analysis of movement.11 It was confirmed to he will usually see that his hands are pointing be altered in every type of PDS. The hand in different directions that his feet are.

137 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 Tactile test: The clinician touches a point dysgraphia and dysorthographia also present over the patient’s thorax and asks him to as symptoms with great impact in PDS patients immediately touch himself at the same skin that can be improved through the treatment point. This is done quickly, pinpointing a protocol.36,33,27,15,8,7,14 random sequence of different skin points. We focus next on the signs of ophthal­ Family members can observe the error in mological disturbances found in PDS patients. the patient’s match, sometimes as large as several centimeters of discrepancy compared Signs of Ophthalmic Disturbances in PDS to where the clinician has touched. The ophthalmic signs of PDS are diverse and complex, as are the neuronal pathways they Symptoms of Ophthalmic Disturbances rely on. The following is a survey of ophthalmic in PDS signs and symptoms associated with PDS. As previously stated, the proprioceptive Visual scotomas are evidenced through system is transversal to all sensorimotor computerized campimetry (Visual Field Test), functions of the organism and in that way an with areas of relative and absolute scotomas impairment in proprioception can translate located para-centrally and in the periphery. The to several different symptoms. For better distribution or pattern of these scotomas does comprehension we can organize the symptoms not correspond to any specific neurological according to each main PDS characteristic condition and is sometimes incorrectly they reveal, as shown in Table 2. interpreted as normal tension glaucoma. The We particularly call attention to the symp­ scotomas represent a deficit in visual perception toms related to pain that are frequently consistent with processing delays that occur in musculoskeletal but can also be neuropathic the auditory system of patients with PDS. (for example sciatica or migraine) or organ Monocular diplopia can occur when one related (for example epigastralgia), as pain image of the target is linked to the fovea, in its many presentations is one of the most but another view is linked to an anomalous or prevalent complaints of PDS patients. eccentric fixation point.9 Interestingly, the pathophysiology under­ Pseudoscotomas appear when an error lying some symptoms of proprioceptive dys­ of proprioceptive information related to function resulting in numbness and paresthesias the position of the ocular globe leads to a is believed to stem from disturbances in discrepancy between objective and subjective vasomotricity and asymmetrical blood flow gaze relative to the target location.21 supply. H. Martins da Cunha was a pioneer in Binocular Diplopia is typically due to showing that asymmetrical arterial blood flow reduced capacity of sensory fusion, and often supply to the facial region could be normalized represents a central fusion disruption as can with proprioceptive treatment as documented occur in acquired brain injury. through infrared thermography of the face.25 Convergence insufficiency is the inability Other significative symptoms are those to sustain fusion at near. This is not an eye related to cognitive dysfunction that can muscle problem in PDS patients, as both eyes impair the learning process, irrespective of have normal adduction ability of the medial intelligence levels and good visual acuity. recti. When we test each eye in isolation, These symptoms are best explained by the asking the patient to close one eye and follow disturbance of multisensorial brain integration an approaching point with the other eye, that occurs as result of a faulty proprioception. there is total adduction with the near point of These symptoms include attention deficit, fixation to the nose. However, when the same hyperactivity and poor concentration. Dyslexia, PDS patient is asked to follow an approaching

138 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 point with both eyes open, the break point and between the body space and environment occurs well beyond the normal near point of space around it. This can be exhibited in convergence. This indicates a disturbance in difficulties with left and right orientation. It can binocular perception rather than weakness of be manifest in frequent falls or ankle sprains the medial recti. Disruption in fusion occurs due to difficulties in locating one’s body in because of the mismatch between image relation to the ground. It can be exhibited with localization of each eye, related to a faulty difficulty in motor planning and execution, such perception of the muscular tonus of one eye as precisely and automatically estimating the relative to the other eye. reaching distance to grab an object This can Near exotropia with exodeviation and lead to clumsiness, bumping into the furniture, associated diplopia at near, but with no poor sports performance, accidents while deviation and with single vision at distance. handling instruments, or while driving. Oculomotor dyscoordination with the These errors vary with the direction of patient presenting inability to coordinate the gaze and include the inaccurate perception eyes in most gaze positions. Symptoms of of the distance between one’s own body and diplopia and incomitant ocular deviation often surrounding objects, which appears to be less occur. This may be associated with nystagmoid than what it really is. movements that, although rare, have been The neuro-ophthalmologic explanation for recorded on video. perceptual impairment due to proprioceptive Ophthalmic migraine during which dysfunction is as follows. How does the micropsia or a relative scotoma can occur as brain know where surrounding objects are in with an aura. These altered visual perceptions relation to the observer, and where the eyes are frequently followed by headache. are in relation to the rest of the body? It is Sensation of ocular globe retraction, not the retina that informs the brain about the during which there is a sensation of feeling that exact location of the objects that surround the eyes are being pulled backward on inward. the observer, in relation to the observer. Error of spatial localization of objects, The retina is a receptive field that provides with figures and visual points of reference information for topographic organization of resulting in straight lines being perceived as the visual fields in the visual cortex. Each point curved. Examples are a picture hanging straight of the image seen activates the same point that is perceived as crooked; a vertical wall within the cortical visual map irrespective of being perceived as leaning; and while reading, eye, head or trunk position. The retina has lines in a text perceived as jumping. The Rey allocentric localization ability but does not complex figure test shows that in some PDS provide egocentric localization information. patients faulty visual perception also occurs The exact location of an object in relation to in two dimensional transformations involving an observer is given by the perception of the copying and memory reproduction.7,33 position of the eyes in relation to the rest of Errors of egocentric localization. We call the observer’s body, and by the perception egocentric localization the ability in locating of the position of the eyes in relation to the one’s body in space. In essence, errors of spatial object. and egocentric localization in PDS patients The brain knows where the eyes are are evidence of a mismatch between what because of the perception of the difference the subject feels as his body spatial position in tonus between the oculomotor muscles. and the real localization of his body in space. When looking straight ahead, there is tonic There is perceptual impairment of the real equivalence between the lateral and medial relation between each segment of the body, recti in each eye. When looking laterally, one of

139 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 (a) (b) Figure 3: Brain mapping of Postural Deficiency Syndrome/ Proprio­ception Dysfunction Syndrome patient. (a) without active prisms; (b) wearing active prisms these muscles has higher tonus than the other, as one is contracted and the other is relaxed. It is the perception of higher or lower tonus Figure 4: Directional Coordimetry of a Postural Deficiency that indicates to the brain the location of the Syndrome/ Proprioception Dysfunction Syndrome patient target object. By changing the muscular tonus without Active Prisms and with Active Prisms from left to of extraocular muscles, egocentric spatial right and from right to left. localization can be changed. Furthermore, changing the perception of tonus of distant frequency waves. When wearing the active structures as the neck muscles or the Achilles prisms, the values of absolute power obtained tendon, can result in an illusory movement of for the Delta frequency become similar to the visual target, the direction of which depends those encountered in the other frequencies on the muscles stimulated.32 Therefore, the measured (Figure 3b).7,33 correct perception of the relative tonicity of The normal waking EEG in adults does not the oculomotor muscles is crucial. If there is a usually record expressive Delta waves. They dysfunction of proprioception, as in PDS, this should be present only during sleep, as Delta perception is altered. activity is inhibited by the ascending cholinergic neurons from the reticular activating system. If Complementary Tests Delta waves appear as prominent in the waking Besides clinical examination and direc­tion­ record they usually suggest head trauma, al scotometry there are comple­ ­mentary tests intoxication, or demential cognitive impairment. that can further illustrate the neurological The brain maps obtained in PDS patients, with effects of PDS. These tests are not routinely none of the aforementioned conditions, suggest used in the clinic but have been very useful for that there is a reversible dysfunction most likely understanding the syndrome as a perceptual involving the reticular formation. The same brain impairment disturbing multisensorial brain maps also indicate that the effect of active prisms integration. is not restricted to a specific area or areas of the brain, but that the effect is associated with a Brain Mapping diffuse change in specific low frequency waves, Brain mapping by computerized electro­ in particular the Delta waves. en­cephalography indicates that patients with Postural Deficiency Syndrome (PDS) present Directional Coordimetry with higher values of absolute power (μv2) Classic Coordimetry is the conventional test than the values of absolute power found used to study ocular motor palsy with the Hess- in higher brain wave frequencies measured Lancaster Screen. Classic Coordimetry is carried (Delta, Theta, Alpha, Beta1 and Beta 2) (Figure out in spirals, where mislocalization due to ocular 3a). Particularly high values are found for Delta motor palsy results in a skewed box diagram.

140 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 Figure 5: Computerized campimetry in PDS patients. A and B – Computerized campimetry of left and right eye in a PDS patient prior to treatment. C and D – other example of PDS patient prior to treatment. Both patients show relative and absolute scotomas but there is not a neurologic specific pattern in any case.

Directional Coordimetry is a modified pro­ Note the following: to­­col of Classic Coordimetry used to study the • Without active prisms there are points Postural Deficiency Syndrome (PDS). Directional incorrectly localized, but the mis-locali­ Coordimetry is carried out line by line, right to left zation does not correspond to Hering’s and left to right; and up–down and down–up. In law for the pattern of displace­ment of PDS, shifts of localization that are not coherent the meridional points. relative to one another can be observed using • The same point is localized differently Directional Coordimetry (Figure 4).33,7 depending on whether gaze direction is The technique consists of showing the red moving from left to right or right to left. lights of the Hess-Lancaster screen not one • With active prisms all points are accurately by one in nine positions as done in the classic localized. spiral method, but line by line. It is done from • Looking at the results with active prisms, left to right, and repeated from right to the left. it is not possible to detect any evidence The first test simulates the eye movements of prismatic power. This means that while reading and the second test simulates the oculomotor system absorbed the eye movements while doing elementary mathe­ prismatic power. matics exercises. Other directions had been tested during our research in order to show To summarize, in contrast with the results that the localization of the same point is not normally obtained in Classic Coordimetry, constant, and depends on the direction in which using Directional Coordimetry one can observe gaze is moving. that active prisms correct inaccuracies in local­ ization, but the images are not shifted by the

141 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 prismatic power. This indicates that the potency would swim in aberrant elliptical patterns. This of the active prisms has been absorbed by the occurred even in the absence of vision, leading oculomotor system. him to conclude that there is a relationship between eye muscle tonus and paravertebral Computerized Visual Fields skeletal muscles based on proprioception. When the first author started researching J.B. Baron also showed in his practice that PDS at the University Hospital in Lisbon, most in some human patients having insufficiency of the patients reported that they could see of convergence, improvement was obtained clearer immediately after putting on trial lenses through the use of low powered base out with active prisms. This was not reflected in any prism. That was quite unexpected, because it change in visual acuity. However computerized was written in all textbooks of strabismus that campimetry (Figure 5) showed visual paracentral the direction of prism indicated to help under- absolute and relative scotomas. These convergence should be a base in rather than a scotomas were not indicative of any particular base out prism. pattern of field loss associated with neurovisual The fact that many patients responded or neurological insult or disease, and they positively to base out prism was the intriguing disappeared with proprioceptive treatment. fact that promoted the first author’s clinical Apparently patients were seeing more clearly investigation. Methodical patient evaluation because their visual field had become intact.1,5 brought the new knowledge that these cases were the ones we classified as left pure PDS Treatment of PDS type. Clinical investigation also concluded that Our treatment approach to PDS incorporates patients with convergence insufficiency not an active prism protocol reviewed in Tables 1 responding to base out prism belonged to other and 3. In addition to the prismatic lens protocol PDS types that responded positively to other we employ a Postural Reprogramming program kinds of prisms. We therefore theorized that according to the Martins da Cunha Technique. when prisms helped, we were eliminating the This is done in conjunction with proprioceptive underlying problem that resulted in the postural insoles, equipment to improve the ergonomics condition rather than masking a symptom. of a workstation as a reading ramp, and other This was the basis for the establishment of proprioceptive stimulations that are beyond the active prism treatment protocol that was the scope of this article. developed by the first author3 and validated in In cases of dyslexia and other learning dif­fi­ the following years.6 culties, treatment also includes exercises involv­ The protocol of active prism consists of ing cognitive training done by our psychologist, prescribing low powered prismatic lenses usually completed in six to ten sessions. from 1 to 4 diopters with base out or upper temporal base, applied to one or both eyes Active Prism Prescription Protocol simultaneously.24,13,6,3 In 1955 the French scientist, neurologist As it is known, humans do not possess purely and ophthalmologist J.B. Baron published a vertical eye muscles. The superior rectus muscle doctoral thesis12 in which he showed the effect is at a 23 degree oblique angle. This means that of surgical alteration of extraocular muscles to elevate the eye there must be a simultaneous on the proprioceptive system in fish. Inducing action of two muscles, the superior rectus and a deviation equal or lesser than four degrees the inferior oblique muscle. In introducing a in the horizontal muscles resulted in the fish vertical prism, we are stimulating intorsion and swimming in circles. When the same deviation extorsion simultaneously, and this may produce a was made in the oblique muscles the fish proprioceptive conflict between the two actions.

142 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 In accordance with the previously men­ needed power is 3 diopters if we select a tioned works of Baron, there is a direct base out prism, and 2 diopters if we select an connection between oculomolotor muscles upper temporal prism. This covers more than and the musculoskeletal system. Therefore, 90 percent of the cases. it is not surprising that by stimulating oculo­ In other cases we need to use lower or motor muscles we can observe changes in higher powers in the 1 to 4 diopter range. the perception of muscular tonus in different For instance, in cases of diplopia there is segments of the body. A vertical prism, by often indication to reduce the prism power. simultaneously stimulating two antagonist In cases where we do not attain correction of eye muscles, may produce a conflict between asymmetry in head rotation, there is often the antagonist muscles in other anatomic locations. need to increase the power of the prism. We This is in contrast to lateral prism or oblique increase or decrease prism in these cases in prism largely targeting one muscle. As an 0.5 diopter intervals. example, base out prism in front of the right As previously mentioned, PDS is classified eye produces a horizontal image displacement in 6 types according to the postural clinical to the left. In response, the eye tries to relocate exam (head rotation, head extension and lower the image to the right by relaxing the right limb position) and directional scotometry lateral rectus muscle. Base out prism in front of evaluated by the synoptophore. the left eye produces a horizontal to the right, with relocation of the image made possible Active Prism Prescription by Case Type through relaxation of the left lateral rectus. For each type of PDS there is a specific Prism can be also be introduced obliquely active prism prescription as indicated in Table to target the response of individual muscles. 1. When there are only psedocotomas for one Applying an upper temporal prism in front of side of version or pseudoscotomas that exist the right eye at 125 degrees, a relaxation effect in asymmetrical angles, the patient only needs is produced on the right inferior oblique muscle. one prism that is applied in front of the eye that Applying an upper temporal prism in front of the is on the side of preferential plantar stance. left eye at 55 degrees will relax the left inferior When there are pseudoscotomas for oblique. An important point to underline is that symmetrical angles of levoversion and dextro­ in using a base out or an upper temporal prism version, the patient needs two prisms of we are stimulating one oculomotor muscle at a asymmetrical power, as noted in Table 1 and time. Consequently, in targeting these muscles, summarized in Table 3. The higher powered we stimulate corresponding skeletal muscles prism will be applied on the side to which head that are proprioceptively related. extension is shorter. We must remember that the lateral rectus The final decision of what active prism to is an abductor muscle and that the inferior prescribe is based upon clinical observation of oblique has 3 different actions, external rotation the patient. All the semiologic tests described (excylcorotation), abduction and elevation. We above are performed before and after applying believe that in PDS patients the postural changes the active prisms, with only a few minutes of are due to a non-antagonized predominance of interval in between. If they are normalized the external rotators, abductors and extensors. with the same profile of prism, the prism Concerning the power of the prism, we may be prescribed with confidence. If not, all have verified that the most frequent power parameters must be reviewed. needed is 2 or 3 diopters when both eyes The correct active prism is the one that needed upper temporal prisms. When only simultaneously corrects all of the previous one eye needs a prism the most commonly clinical parameters. The only exception for this

143 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 Table 3 – Simplified active prisms prescription protocol. RE- right eye; LE- left eye; *In Mixed pure type, if Maddox test is normal the high powered prism of 3Δ will be replaced by 2.5Δ prism. More commonly PDS type Peripheral Pseudoscotomas prescribed active prisms

right Pseudoscotomas levoversion at 20° RE 180° 3Δ Pure only to one side of version left the opposite side of plantar stance dextroversion at 20° LE 0° 3Δ dextroversion at 30° right Pseudoscotomas are asymmetrical RE 125° 2Δ or 3Δ Mixed levoversion at 20° Predominant occur in higher angle of version to levoversion at 30° left LE 55º 2Δ or 3Δ the side of preferential plantar stance dextroversion at 20° RE 3Δ 125° * right levoversion at 20° Pseudoscotomas dextroversion at 20° LE 2Δ 55° Mixed Pure or RE 2Δ 125° left for symmetrical angles of version levoversion at 30° dextroversion at 30° LE 3Δ 55° * is the tonic eye convergence test, that does prescribing for cases of PDS mixed pure, but not correct immediately in every case. When not to diagnose anything. there is not a full correction of the clinical signs, In the conventional assessment of binocular the decision of what power of active prism to vision and strabismus, the Maddox test at prescribe may be further aided by performing distance is used to detect heterophorias. the Maddox test at distance. The same test is used in the assessment Beyond delineating our prism protocol, of proprioception, but with a different it is equally important to contrast it with purpose. PDS patients do not usually have conventional approaches to ocular or postural true heterophoria, but have a perception of disturbances or misalignment. Some authors the visual image as being displaced. We can use the Maddox test or other haploscopic confirm that this is not a true heterophoria tests in their protocol for prism prescription. because there is an absence of refixation Whenever the patient reports one image higher movement on the cover test. than the other, they interpret this as a vertical The same is true using the Maddox wing heterophoria. The phoria is then believed to be test. On this test the arrow is actually pointing the primary cause of the symptoms. The solution to zero, but the PDS patient sees it as if it was proposed by these authors is to compensate pointing to 14 or 16 at the scale. Once more the supposed phoria by prescribing a vertical this is not an indication of true heterophoria, prism. However, if we do a cover test on these as confirmed by the absence of refixation patients, we will verify that there is no objective movement on the near vision cover test. sign of refixation movement, nor a subjective To reiterate, the displacement of the visual sensation of image displacement. image without strabismus is called hetero­ In our opinion this is not a vertical hetero­ localization. We believe this occurs because of phoria, but a deficit in localization. We refer a misperception of the muscular tonus of the to this as heterolocalization. This is usually oculomotor muscles. As it is known, the brain evident in the horizontal plane on the near decodes the egocentric spatial localization of Maddox test, and in the vertical plane on an object seen based on the perception it has the distance Maddox test. This aberrant of eye muscle tonus. localization mimics a heterophoria, but in reality Conventionally, practitioners tend to split is a sign of proprioceptive disturbance. Some prism equally between the right and left eyes. ophthalmologic authorities even misinterpret For treatment purposes of PDS, when the this as a small compensated strabismus. The Maddox test is normal in patients of the mixed Maddox test is useful in our clinic as an aid in pure type, the power difference between right

144 Vision Development & Rehabilitation Volume 5, Issue 2 • June 2019 and left active prisms may be reduced. In the ments in horizontal gaze which we have termed other types of PDS, however, reducing the power directional scotometry; asymmetry in head difference measured or derived by observation tilts and rotations; and rotation in supporting may lead to a false prescription protocol. heel and foot support. Our treatment protocol then applies prisms asymetrically to each eye Summary and Conclusion to effectively produce changes in these visual, The proprioceptive system has an extensive head, and body asymmetries. influence on the maintenance of human Our diagnostic and treatment protocol health. When the proprioceptive system is is constantly being refined. To date we have dysfunctional, the central nervous system does seen success in the treatment of a variety of not recognize the correct status of tonicity of functional types of oculomotor dyscoordination the muscles at rest or in motion, does not ranging from binocular disturbances such integrate correctly the information that comes as convergence insufficiency, near exotropia and from sensory receptors, and has difficulty asthenopia, to unilateral visual disturbances such in modulating multi-sensory integration, as monocular diplopia, paracentral scotomas with consequences in motor behavior and of the visual field, and metamorphopsia. PDS cognitive function. This results in a wide range and its treatment can extend to certain types of proprioceptive abnormalities which are of cognitive dysfunction, functional ataxia, clinically related and are treated together, dyspraxia, dyslexia, postural imbalances, and termed as Postural Deficiency Syndrome (PDS). pain. Low powered active prisms, up to four It is possible to influence body proprio­ diopters, can influence blood circulation as ception by stimulating not only direct mechano­ shown by arterial Doppler ultrasound. receptors like neuromuscular spindles, or joint An understanding of the significance of the or tendon neurologic terminations, but also by visual system in PDS provides an important modulating the information from other sensory role for the vision professional in managing input as well. These range from visual receptors proprioceptive dysfunctions. Relatively inex­ connected to the retinocolicular pathway in pensive, non-invasive, and accurate diagnosis the uppermost region of the body to the sole is possible leading to more effective treatment plantar receivers underfoot. of PDS patients with significant impact on their The first author’s contribution to this quality of health and life. field extends the work of Martins da Cunha by using an active prism protocol to treat REFERENCES postural asymmetries that produces a change 1. Almeida L, Pereira R, Leite H, Martins da Cunha H, Alves in oculomotor system and modifies the da Silva O, Ribeiro da Silva J (1993) Perimetria estática computorizada e SDP [Static computorized campimetry visual information input. This therapeutic and PDS]. Arq Port Oftalmol II:31–34. effect is based on the knowledge that small 2. Alves da Silva O, Mendes A, Pinhal F M da CH (1988) modifications of the muscular tonus of the Fusion – Visual information and proprioceptivity. Proc XVII oculomotor muscles can change the tonus of Meet Eur Strabol Assoc Murube del Castillo Ed 89–93. 3. Alves da Silva O (1987) Scotometrie directionelle et the axial paravertebral muscles. corrections prismatiques dans le syndrome de deficience Prisms have been conventionally prescribed posturale. Agressologie, 28(9):945-6. Agressologie 28(9): by arbitrarily splitting the power between the 945–6. two eyes, or by taking into account asymmetries 4. Alves da Silva O (1988) A importância das alterações oftalmológicas no sindome disfuncional da ATM exhibited in sensory projection of binocular [importance of ophtalmological disturbances in TMJ targets. The diagnostic protocol the first author syndrome]. Rev Port Estomatol e Cir Maxilofac 28:35–40. has devised goes beyond this to encompass 5. 5. Alves da Silva O (1988) [New interdisciplinary approaches in ophthalmology]. Agressologie 29:681–682. pseudoscotomas observed on versional move­

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BIOGRAPHY: org/10.1146/annurev-neuro-061010-113728 Orlando Alves da Silva, MD 18. Martins da Cunha H (1979) Syndrome de déficience Consultant Ophthalmologist; Professor posturale. Actual en réeducation Fonct rèadaptation” 4e of Ocular Motricity and Proprioception serie:27–31. Postumed, Lisbon, Portugal 19. Martins da Cunha H (1983) Informação Proprioceptiva e AUTHOR: Teresa Alves da Silva, MD Visual no Sindrome de Deficiência Postural [Proprioceptive Hospital de Cascais, Department of and visual Information in PDS]. Acta Reum. Port. VIII: Orthopedics, Cascais, Portugal 20. Martins da Cunha H (1987) [Postural deficiency syndrome]. Postumed, Lisbon, Portugal Agressologie 28:941–943. 21. Martins da Cunha H, Alves da Silva O (1983) Semiologia Dr. Orlando Alves da Silva is based in Lisbon, Oftalmologica no Sindrome de Deficiencia Postural where he directs a busy multi­disciplinary [ophtal­mological semiology in PDS]. Arq. Port. Oftalmol. clinic and provides specialist training to medical professionals from all over the Vol especi: world. After graduating in Medicine from 22. Martins da Cunha H, Alves da Silva O (1986) Syndrome de the University of Coimbra, Portugal in 1971, Défcience posturale. Un Nouveau et Grand Chapitre de he specialized in Ophthalmology at the L’Olphtalmologie, J Fr Ophtalmol (Paris), 9:747-755. J Fr University Hospital St Maria, Lisbon. From Ophtalmol 747–755. 1977-2005 he was Director of Strabismus at the University Hospital St. Maria. There he collaborated with Dr. Martins da 23. Martins da Cunha H, Alves da Silva O (1986) Disturbances Cunha, Director of Rehabilitation Medicine on Active Prisms of binocular function in the postural deficiency syndrome. for the management of Proprioception Dysfunction Syndrome/ Agressologie 27:63–67. Postural Deficiency Syndrome. 24. Martins Da Cunha H, Alves Da Silva O (1986) [Postural Dr. da Silva was the Portuguese lead for the European project deficiency syndrome. Its importance in ophthalmology]. J on infant videorefractive screening programs, coordinated by Fr Ophtalmol 9:747–755. professor Janette Atkinson, and a founding member and first 25. Martins da Cunha H, Passos Angelo E (1979) Changes in president of the Portuguese Group of Pediatric Ophthalmology thermographic patterns of the face induced by postural and Strabismus. He was a member of ESA, and has presented correction. Agressologie 20B:169– 170. his group’s research at numerous international conferences as keynote speaker. 26. Quercia P, Marino A (2017) Oeil et Bouche. Beaune, France He is a Visiting Professor in several postgraduate courses encom­ 27. Quercia P, Robichon F, Alves da Silva O (2004) Dyslexie de passing Italy, France, Spain and Portugal, and has published six Developpement et Proprioception. Association Graine books on the treatment of Proprioception Dysfunction Syndrome. Lecteur, Beaune

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