Components of Eye Movement Systems 1 Superior Colliculus SC

The superior colliculus forms the anterior roof of the midbrain (Fig. 1B). Its rostral border is the pretectum, and its caudal border is adjacent to the inferior

INPUTS FROM:

Cerebral Cortex

Extrastriate visual cortex (occipital) Multimodal association cortex (parietal) Auditory association cortex (temporal) Somatosensory association cortex (postcentral) Premotor, motor, and oculomotor cortex (precentral) Prefrontal association cortex (frontal Diencephalon

Hypothalamus; Zona incerta; Fields of Forel Thalmic nuclei: reticular, ventral medial, ventral lateral, geniculate Mesencephalon

Nucleus of the posterior commissure Mesencephalic Reticular Formation (MRF) Cuneiform nucleus Periaqueductal grey Contralateral superior colliculus Superficial superior colliculus

Colliculus Anterior

Figure 3 Inputs and outputs of the intermediate and deep layers of the superior colliculus. Layers of gray matter and optic fibers are indicated (right). Afferent connections are shown on the left side and efferent projections on the right side. Ascending projections are above the section of the superior colliculus and descending connections are below the section. See Table I for abbreviations.

INPUTS FROM:

Mesencephalon

Substantia Nigra

Inferior colliculus & Brachium

Nuclei of the lateral lemniscus

Locus coeruleus

Dorsal raphe nucleus

Pons

Dorsomedial periolivary nucleus Nucleus of the trapezoid body Medulla

Vestibular complex Perihypoglossal complex (prepositus, intercalates)

DESCENDING PROJECTIONS TO:

Contralateral(Predorsal Bundle) Pons

Dorsolateral pontine grey Nucleus reticularis tegmenti pontis

Nucleus reticularis pontis oralis

Paramedian pontine reticular formation Abducens nucleus and area ventral and lateral to it

Medulla

Medial accessory nucleus of inferior olive

Vestibular nuclei (medial and descending)

Perihypoglossal complex prepositus intercalatus

Supraspinal nucleus

Spinal trigeminal nucleus

Cervical spinal cord (ventral horn)

Ipsilateral Mesencephalon

Perilemniscal Zone

Inferior colliculus (external capsule)

Mesencephalic reticular formation

Cuneiform nucleus

Pons

Dorsal lateral pontine grey Nucleus reticularis tegmenti pontis Nucleus reticularis pontis caudalis Nucleus reticularis pontis oralis Paramedian pontine reticular formation

Figure 3 Inputs and outputs of the intermediate and deep layers of the superior colliculus. Layers of gray matter and optic fibers are indicated (right). Afferent connections are shown on the left side and efferent projections on the right side. Ascending projections are above the section of the superior colliculus and descending connections are below the section. See Table I for abbreviations.

colliculus. Seven alternating fiber and cellular layers make up the superior colliculus. However, the main functional divisions are a superficial visual part (three layers) and a deeper oculomotor part (four layers).

The superficial layers are composed of the stratum zonale (SZ), stratum griseum superficiale (SGS), and stratum opticum (SO) from dorsal to ventral, respectively (Fig. 3). Whereas retinal and cortical afferents innervate the SZ, SGS, and SO, the distribution of inputs to these areas is not even. Indeed, the stratum griseum superficiale can be further subdivided into three sublayers in terms of the distribution of inputs. SGS1 (25-120 mm from the surface) derives much of its input from W-type retinal ganglion cells. SGS2 occupies approximately 300 mm, and much of the input to this region is from areas 17, 18, and 19 of the visual cortex. The Y-type retinal ganglion cells synapse in SGS3. In general, the visual responses of individual superficial layer neurons are binocular, direction-selective, and have discrete retinotopically organized receptive fields. The overall organization of retinal and visual cortical afferents to the primate superior colliculus places neurons with parafoveal receptive fields near the rostral pole, whereas neurons with peripherally located visual fields are located more caudally. The upper contralateral visual field is represented medially and the lower visual field laterally. Whereas the retinal contribution from the contralateral eye is evenly distributed across the colliculus, the input from the ipsilateral eye is densest in the central portion of the colliculus. This distribution leaves the neurons of the rostral pole of the primate colliculus driven solely by the contralateral eye (i.e., these cells are monocular). Furthermore, the contralateral retinal projection to the superficial layers is distributed to the dorsal SZ and SGS than the ipsilateral afferents that target the deeper portions of the SGS and most of the SO. Another aspect of the retinal afferents is that they tend to cluster in patches that extend across one or two of the superficial layers. Interestingly, these puffs or patches in the SZ and SGS receive predominantly contralateral, cholinergic input from the parabigeminal nucleus. Other subcortical afferents to the superficial layers arise from the ventral lateral geniculate nucleus, which primarily targets the ventral portion of the SGS and the SO. These projections are bilateral, but are predominantly ipsi-lateral. Last, the pretectum, especially the nucleus of the optic tract, sends a projection to the superficial layers.

The primary efferents from the superficial layers originate from the L-type neurons, small or medium-sized cells with elaborate dendritic trees. They participate in the ipsilateral descending and dorsal ascending tectofugal bundles. These cells provide synaptic input to the parent neuron through recurrent collaterals as well as more ventrally to the deeper tectal layers including the stratum griseum intermediale. The primary extratectal target of the L neurons is the parabigeminal nucleus. Other efferents arise from superficial layer neurons whose cell types have not been well-described. The stratum zonale provides efferents to the pretectal nuclei, lateral posterior pulvinar complex, and dorsal and ventral lateral geniculate nuclei. The more superficial portions of the SGS (layers 1 and 2) provide afferents to the dorsal lateral geniculate body, whereas the deeper SGS projects to the lateral posterior pulvinar.

The intermediate and deep layers of the superior colliculus (Fig. 3) are called the stratum griseum intermediale (SGI), stratum albican intermediale (SAI), stratum griseum profunda (SGP), and stratum albican profunda (SAP). These layers participate in the control of visually guided movements such as those of the eye, head, and arm. The inputs to the intermediate and deep layers include both descending cortical and subcortical contributions. Distinct from the superficial layers, the intermediate and deeper layers receive somatosensory, auditory, as well as visual inputs. The parietal (area LIP) and frontal cortices (frontal eye fields, supplementary eye fields, dorsolateral prefron-tal cortex) provide much of the cortical, glutaminergic (i.e., excitatory) inputs to the intermediate and deep layers of the superior colliculus. The mesencephalic reticular formation and basal ganglia (primarily the substantia nigra pars reticulata) provide much of the GABAergic input (i.e., inhibitory) input to the superior colliculus. The afferents to the intermediate and deep layers of the superior colliculus from the pedun-culopontine nucleus at the junction of the pons and midbrain are primarily acetylcholinergic (i.e., excitatory). Afferents to the intermediate and deep layers of the superior colliculus from the fastigial nucleus (deep cerebellar nuclei) and the nucleus prepositus hypoglossi are also well-described, but their transmitters have not been identified. For a listing of the afferent and efferent connections of the intermediate and deep layers of the superior colliculus, refer to Fig. 3.

Two types of efferent neurons have been distinguished in the intermediate and deep layers of the superior colliculus on the basis of their axonal branching patterns: X and T cells. Neurons of the X type are large multipolar neurons. Their cell bodies are located primarily in SGI and occasionally in the stratum opticum. They provide an axon that descends ventrally through the stratum albican profunda and then leaves the superior colliculus to reach the underlying periaqueductal gray. The axon circumscribes the periaqueductal gray and then crosses the midline ventral to the medial longitudinal fasciculus to reach the contralateral predorsal bundle. The X neurons do not emit any commissural collaterals to the opposite superior colliculus. In contrast, the cell bodies of the T cells are small to medium in size and reside within the ventral portion of the stratum opticum and the more dorsal portion of stratum griseum intermediale. The axons of T cells have an initial course similar to that of the X cells. Within the stratum griseum profunda, the axons of these cells ramify to provide a large number of recurrent collaterals. The primary axon then descends further to the periaqueductal gray where it bifurcates. For all T cells, one branch is directed across the collicular commissure to ramify upon neurons in the intermediate and deep layers of the opposite superior colliculus. The destination of the second collateral can be variable. In some T cells, the second collateral branch emits collaterals around neurons in the ipsi-lateral mesencephalic reticular formation, whereas the main axon proceeds to circumscribe the periaqueductal gray to eventually join the contralateral predorsal bundle. The axon collaterals of other T neurons contribute to the ipsilateral ascending or descending projections of the superior colliculus. The axons of the X cells are large and probably provide much of the tectal input to cervical levels of the spinal cord. The smaller axons of the T cells probably do not reach spinal levels but end at pontine or medullary levels.

The organization of the neurons in the intermediate and deep layers of the superior colliculus generally follows that of the cells in superficial layers. The neurons in the intermediate and deep layers of the superior colliculus discharge in association with rapid eye movements. This discharge is much greater when the saccade is made in light than in dark. Two primary types of neurons are recognized. Burst neurons begin to fire 30-50 msec before the onset of a rapid eye movement that will bring the fovea within a specific portion of the oculomotor range. The collection of the movements for which the neuron will fire is called the movement field of the cell, in analogy to the visual receptive fields of neurons in the more superficial layers. Build-up neurons begin to discharge at low frequency as long as 130 msec before saccade onset and have a burst of discharges that occurs 30-50 msec before saccade onset. These neurons tend to have larger movement fields than the burst neurons, and the outside edge of their movement fields is less well-defined. With the advent of unrestrained head and eye (i.e., gaze) movement recordings, it is now recognized that neurons in the caudal portion of the intermediate and deep layers of the superior colliculus are best activated for gaze and not the separate eye or head components of the movement. As such the responses of a single neuron in the caudal SC have been described as a "gaze," not a "movement," field, i.e., the group of combined head and eye movements that cause the neurons to discharge. The neurons in the intermediate and deep layers appear to be organized in spatial register with the superficial neurons located just above. Thus, the rostral pole of the superior colliculus contains neurons that fire before small primary to secondary saccades. Cells with larger movement fields are located more caudally. Cells with upward movement fields are located medially, whereas neurons with downward movement fields are located laterally.

Figure 4 Physiological organization of the intermediate and deep layers of the superior colliculus based on electrical stimulation in head-fixed monkeys. Both colliculi are shown from above. The midline is between the two grids. Note that numbers along the sides of the diagrams are the amplitude of the saccade elicited in degrees. The numbers along the bottom indicate the elevation of the elicited eye movement. Positive numbers indicate upward movements found on the medial side of the colliculus, and negative numbers indicate downward movements found toward the lateral side of the colliculus. See Table I.

Figure 4 Physiological organization of the intermediate and deep layers of the superior colliculus based on electrical stimulation in head-fixed monkeys. Both colliculi are shown from above. The midline is between the two grids. Note that numbers along the sides of the diagrams are the amplitude of the saccade elicited in degrees. The numbers along the bottom indicate the elevation of the elicited eye movement. Positive numbers indicate upward movements found on the medial side of the colliculus, and negative numbers indicate downward movements found toward the lateral side of the colliculus. See Table I.

Electrical microstimulation in the SGI of monkeys whose head is restrained elicits saccades at short latency (o 40 msec), whose maximal amplitude is primarily dependent upon the site, not the parameters of stimulation. These stimulation results have been used to generate a map of contralateral eye movement amplitudes that corresponds with the amplitude sensitivity of the cells recorded at each collicular site (Fig. 4). This will surely change in light of current experiments that are examining electrical microstimulation with the head free to move.

The possibility that the activity of the visual, superficial layers could be directly translated into the motor activity of the deeper collicular layers has driven research on the superior colliculus for longer than a century. Features of this concept have been demonstrated in many species of rodent (golden hamster and rat), but the interconnections of the superficial and deep layers have been less extensive in primates. Most likely, the reason for this species difference is dependent on the importance of the superior colliculus in visual processing. In afoveate animals (e.g., rodents), the superior colliculus is probably the primary visual and gaze processing region. Thus, direct projections from the superficial to the deep layers are advantageous. In foveate animals (i.e., monkeys and humans), the superficial layers of the superior colliculus play a much more secondary role in visual processing because of the size and complexity of the visual (occipital) cortex. The intermediate and deep layers, on the other hand, retain considerable importance for the control of oculomotor and gaze-related behaviors, despite their duplication by other cortical bulbar pathways from the frontal eye fields and inferior parietal lobule ofthe parietal cortex. This is the reason that removal of the intermediate or deep layers of the superior colliculus (either by lesion or by reversible inactiva-tion) in primates can produce an increased latency and some change in the trajectory of visually guided eye movements. Similarly, removal of the frontal eye fields alone produces minimal changes in eye movements. Simultaneous removal of both frontal eye fields and the superior colliculus produces a devastating reduction in the amplitude and speed of contralaterally directed saccadic eye movements. This deficit does not recover. In sum, the superficial layers of the superior colliculus in the primate provide visual information that is overshadowed by the amount of information provided by the occipital (visual) cortex. The intermediate and deep layers of the primate superior colliculus provide one of the parallel paths for the supranuclear control of gaze (head and eye movements.)

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