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Eye Movements MHD – Neuroscience Module January 28, 2016 Gregory Gruener, MD, MBA Vice Dean for Education, SSOM Professor & Associate Chair, Department of Neurology LUHS/Trinity Health and Catholic Health East

Objectives Describe the actions of the extraocular muscles Outline conjugate eye movements, pathways and components Slow/pursuit eye movements (PPRF, MLF, vestibuloocular reflex) Fast/ballistic/saccadic eye movements (frontal eye fields) Describe components/pathway for vergence eye movements Define/describe internuclear ophthalmoplegia

Ocular Motility Motility is controlled by six extraocular muscles Four rectus muscles (superior, inferior, lateral, medial) originate from a common tendinous ring (annulus of Zinn) Insert anteriorly in the sclera Two oblique muscles (superior and inferior) Originate from the sphenoid bone (back of the orbit, SO) or the front medial floor of the orbit (IO) Insert posteriorly in the sclera Fast and precisely controlled, motor units are unusually small, composed of fatigue-resistant type 2A fibers Binocular vision necessitates precise alignment of both eyes Coordinated changes involve activity of all six extraocular muscles Each muscle has a primary and secondary actionswhen starting from a primary position Action is determined by direction and position of tendon insertion Vertical recti & oblique muscles have functions that vary according to eye position

“Cardinal” positions of gaze – a theoretical concept http://www.instantanatomy.net Modified from Schuenke M, Schulte E, Schumacher U. Thieme Head and Neuroanatomy, 2007

Eye structures passing through the orbital fissures (not this detail on the exam) sciencephoto.com frontal zygomatic maxillary http://www.instantanatomy.net

Cavernous sinus (not this detail on the exam) http://www.instantanatomy.net

Centers for Conjugate Gaze Brainstem Rostral interstitial nucleus (vertical gaze center) PPRF (horizontal gaze center) Cortical “Frontal eye field” (Brings an object onto the fovea) Initiates saccadic eye movt.’s “Occipital eye field” (Keeps an object on the fovea) Necessary for smooth pursuit Schuenke M, Schulte E, Schumacher U. Thieme Head and Neuroanatomy, 2007

Conjugate eye movements – slow/pursuit Slow eye movements that keep images on the fovea (~100 degrees/s); allows continuous feedback from vestibular and visual systems to regulate speed/duration Smooth pursuit movements Visual feedback keeps images of moving targets on the fovea Volitional, originates in the extrastriate cortex & uniquely requires cerebellum (flocculus) for its generation Vestibuloocular reflex (clinically tested as part of the Doll’s eyes maneuver) Generates compensatory eye movements in opposite direction from head movements, relies on vestibular input Can be suppressed to allow head and eye movements to shift gaze Vergence movements Accommodation signals are used to guide vergence eye movements (CN III, MR) Cerebellum involved but not essential for movements Optokinetic movements Compensates for head movement, but relies on visual cues to the entire retina

Pursuit eye movement recording This is a volitional eye movement that is attempting to “guess” where the target is going and to move the fovea onto it as quickly as possible. During a saccadic eye movement, vision is blurred. Once the target is reached, smooth pursuit takes over and as long as the target is moving slowly, can keep the fovea on it and allows a sharp image; smooth pursuit is a reflex and “automatic” In this recording the eyes don’t have a target so, smooth pursuit can’t occur and all you see are fast saccadic eye movements as the brain tries to follow a virtual target smoothly, but can’t. In this recording the eyes have a “target “so, smooth pursuit can occur. Tracking a light in a dark room Imagine a light was moving in a dark room “Following “ their finger moving in a dark room These are all recordings of eye movements and in this case we are seeing smooth pursuit of the eyes, but it requires that the eyes have a target and that the target is moving slowly. Nolte. The human brain. Mosby, 2010 Nolte. Essentials of he human brain. Mosby, 2009

Vestibuloocular reflex (VOR) Stabilizes the image on the retina during a rotation of the head and faster than visual tracking As the head rotates the VOR rotates the eyes with the same speed, but in the opposite direction Without this reflex, the image would appear “smeared” upon the retina Once the head stops moving the eyes remain in that same direction of gaze “Stabilization” occurs through the nucleus prepositus hypoglossi Tonic activation maintains the activation/activity of the involved cranial nerve nuclei (the 3rd and 6th)

Eye movement integration with vestibular system Trends in Neurosci 2012;35:185-196

Vestibular pathways involved with eye movements

Vestibuloocular reflex Head is rotating to the right The right horizontal canal is activated Right vestibular nucleus is “activated’ The left 6th nucleus (via PPRF) is activated and the left lateral rectus muscle contracts The left PPRF “activates neurons in the right 3rd nucleus and the right medial rectus contracts … both eyes begin to move to the left The object of interest “stays” on the fovea Nolte. The human brain. Mosby, 2009

Conjugate eye movements - saccadic Fast eye movements that move an image onto the fovea (~700 degrees/s); brainstem motor programs that are triggered by cerebral or cerebellar center. Ballistic eye movements place an image onto the fovea, same as fast phase of nystagmus Initiated from the contralateral frontal eye fields (middle frontal gyrus) Used in reading, scanning scenes & pictures, etc. Modulated by output from basal ganglia, inhibits frontal & supplementary eye fields, sc Modulated by the cerebellum (vermis), regulates timing of muscle contractions (dysmetric saccades) Rapid horizontal eye movements - generated from the paramedian pontine reticular formation (PPRF) Rapid vertical eye movements - generated from the reticular formation dorsomedial to the red nucleus (riMLF)

Conjugate eye movements – saccadic (volitional looking to the left) http://www.neuroanatomy.wisc.edu/Bs97/TEXT/er/er.htm

Pathway for the near reflex http://www.instantanatomy.net

Ophthalmoplegia MLF lesion – internuclear ophthalmoplegia The direction of the blue arrow is the direction the person is asked to look The side of the PPRF lesion corresponds to the side of failure of lateral gaze The MLF lesion is on the side of the eye that can’t adduct on lateral gaze On testing convergence, both eyes can move in (adduct) and you confirm that the medial rectus of the eye that doesn’t adduct on lateral gaze is functional! Convergence involves the anterior portion of the MLF so. it “bypasses” the lesion in the inferior portion of the MLF where it is disrupted. Here is the lesion MLF lesion – internuclear ophthalmoplegia PPRF lesion – gaze palsy Sakai K, Yokota H, Akazawa K, Yamada K Brainstem White Matter Tracts and the Control of Eye Movements. Semin Ultrasound CT MRI 2014;35:517-526