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The Superior Colliculus and Visual Function

Peter H. Schiller

10.1002/cphy.cp010311

Source: Supplement 3: Handbook of Physiology, The Nervous System, Sensory Processes

Originally published: 1984

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Anatomy of Superior Colliculus
1.1 Methods
1.2 Intrinsic Organization
1.3 Inputs to Superior Colliculus
1.4 Outputs of Superior Colliculus
1.5 Summary
2 Physiology of Superior Colliculus: Electrical Recording Studies
2.1 Methods
2.2 Recordings from Paralyzed Animals
2.3 Recordings from Alert Animals
2.4 Summary
3 Physiology of Superior Colliculus: Stimulation Studies
3.1 Methods
3.2 Electrical Stimulation of Primate Superior Colliculus
3.3 Electrical Stimulation of Cat and Rodent Superior Colliculi
3.4 Summary
4 Physiological Studies of Inputs to Superior Colliculus
4.1 Methods
4.2 Retinal Input
4.3 Cortical Input
4.4 Subcortical Input
4.5 Summary
5 Physiological Studies of Outputs of Superior Colliculus
6 Behavioral Effects of Superior Colliculus Ablation
7 Developmental Studies of Superior Colliculus
7.1 Methods
7.2 Development of Mammalian Superior Colliculus
7.3 Effect of Surgical Interference on Retinotectal Pathway
7.4 Effect of Selective Rearing on Collicular Functions
7.5 Summary
8 Concluding Remarks
Figure 1. Figure 1.

Sagittal sections of toad, rabbit, and monkey brain. Arrows, location of superior colliculi. Note the significant difference among these three species in the relative amount of brain tissue devoted to telencephalon and to colliculus.
Figure 2. Figure 2.

Projection drawing of a transverse section through superior colliculus of the cat (cresyl violet stain) to show development of laminae. I1,2, sublaminae of stratum zonale; II1,2,3, sublaminae of stratum griseum superficiale; III, stratum opticum; IV, stratum griseum intermediale; V, stratum lemnisci; VI, stratum griseum profundum; VII, stratum album profundum; PAGL, periaquiductal gray, pars lateralis.

From Kanaseki and Sprague 125
Figure 3. Figure 3.

Representative types of neurons in frog optic tectum shown in a combined cytoarchitectonic diagram obtained from staining with hematoxylin‐eosin and reduced silver. Numerals at extreme left indicate the different layers; z, stratum zonale; p, plexiform sheets in layer 9. Golgi picture begins with a truncated ependymoglial cell. Numerals at right: 1, large pyramidal neuron with type 1 dendritic arborization pattern; 2 and 3, large pear‐shaped neurons with type 2 and 3 dendritic arborization patterns, respectively; 4, optic terminals; 5, ascending axon; 6, large ganglionic neuron; 7, small pear‐shaped neuron with descending axon; 8, small pear‐shaped neuron with a beaded axonlike process; 9, stellate neuron; 10, amacrine cell; 11, assumed endings of diencephalic afferent fibers.

From Sźekely et al. 257
Figure 4. Figure 4.

Cell types in cat superior colliculus. Superior colliculus is divisible into two laminar divisions based on cell types seen in Golgi‐stained material. Superficial division (I, II, and upper portion of III) is characterized by neurons with vertically elongated (narrow‐field vertical cells, C) or horizontally elongated (horizontal cells, B) dendritic fields or by dendritic fields eccentrically distributed about the cell body (piriform cells, D; wide‐field vertical cells, F; inverted ganglion cells, E). The cat is unusual in apparently lacking marginal cells but having small stellate granule cells, A, in upper part of its superficial division. Stellate cells, G, are rarely seen in the middle of superficial division but become increasingly more frequent in its deep portion as it becomes transitional with deep division. Neurons of deep division (lower portion of III, IV, V, VI) are predominantly small‐ and medium‐sized stellate multipolar neurons, H, with occasional large or massive stellate neurons, I, usually in middle regions of layers IV and VI.

Courtesy of T. P. Langer
Figure 5. Figure 5.

Topographic layout of visual field on surface of superior colliculus of mouse, rabbit, and cat. Derivation of 0° vertical meridian is different in each of these maps. In the mouse map the 0° vertical meridian is the vertical plane that intersects the projection of the long axis of the mouse's head. In the rabbit map the 0° vertical meridian intersects the perpendicular to the long axis of the head, which passes through the corneal vertex. In the cat map the 0° vertical meridian intersects the projection line of area centralis. In all three maps the 0° horizontal meridian intersects each of the described projection lines in the horizontal plane. Horizontal meridians run in the anteroposterior direction. The maps represent the contralateral retinal projection. A, anterior; P, posterior; M, medial; L, lateral.

Mouse data from Dräger and Hubel 44; rabbit data from Hughes 108; cat diagram courtesy of H. Sherk from data of Berman and Cynader 21 and Feldon et al. 53
Figure 6. Figure 6.

Retinotectal transformation. Top left: polar isograms for retinal surface of rabbit. The 0° vertical meridian intersects the perpendicular to the long axis of the head, which passes through the corneal vertex. The 0° horizontal meridian intersects the projection line in the horizontal plane. Stippled area, visual streak. Bottom left: approximate density distribution of retinal ganglion cells along horizontal, H, and vertical, V, meridians. Top right: collicular topography, polar coordinates. Stippled area, visual streak. Bottom right: collicular topography, rectilinear coordinates; transformation of circular spot on retina (black disk) is shown in colliculus by black oval area.

Bottom left, data from Hughes 108
Figure 7. Figure 7.

Location of transported protein in superior colliculi of rabbit, cat, and rhesus monkey after injection of labeled amino acids into right eye. In rabbit the projection is mostly contralateral. In the cat the ipsilateral projection is less dense than the contralateral projection. In monkey the ipsi‐ and contralateral projections are almost equal.

Courtesy of J. K. Harting
Figure 8. Figure 8.

Schematic drawing of cat superior colliculus showing possible neuronal linkages in visuomotor transform. Thick arrows, major path; boxes outline representative slices of terminal fields from optic (retinal) tract and corticotectal tracts from areas 17, 18, 19, 21, C‐B, and 7; shaded areas, major foci of degeneration after lesions to these areas. MBSC, medial brachium of superior colliculus; LBSC, lateral brachium of superior colliculus; NIC, interstitial nucleus of Cajal and adjacent reticular formation; C‐B, Clare‐Bishop area; D, nucleus of Darkshevitch; OC, oculomotor nuclei; PAG, periaquiductal gray matter. Roman numerals represent the seven collicular laminae.

From Ingle and Sprague 117
Figure 9. Figure 9.

A: directionally selective unit in superior colliculus. Upper trace, microelectrode recording; lower trace, potentiometer recording of mirror movements indicating time course of moving light spot; solid arrows, direction of stimulus movement; ±, on‐off response to flashed light spot; ○, no response to light spot; large open arrow, preferred direction. B: distribution of direction‐selective neurons in cat superior colliculus. Number at end of each arrow gives percentage of cells in total sample of 317 cells that responded best in direction shown by arrow. Relative length of each line is proportional to percentage of cells represented by that line. Pooled data from left and right colliculi are computed in terms of directions relative to vertical meridian; directional preferences of majority of cells are for movement away from vertical meridian.

A: from McIlwain and Buser 157. B: data from results of Berman and Cynader 21, Gordon and Gummow 73, and Sterling and Wickelgren 243
Figure 10. Figure 10.

Distribution of ocular dominance of cells in cat superior colliculus. Total number of cells, 316. Numeral above each bar, number of cells per category. Cells in group 1 can be activated only through the contralateral eye, cells in group 4 are equally driven by either eye, and cells in group 7 are activated only by the ipsilateral eye. Groups 2, 3, 5, and 6 represent in‐between gradations.

Data from Berman and Cynader 21, Gordon and Gummow 73, and Sterling and Wickelgren 243. Groupings 1–7 from Hubel and Wiesel 105
Figure 11. Figure 11.

A: histograms obtained from a single cell in monkey superior colliculus showing response to stimuli of varying diameters. Stimulus duration, 500 ms, presented once every 1,300 ms, 25 times per histogram. Response field, 18° from fovea; s/b, number of spikes per bin. B: response frequency as a function of stimulus size for four superior colliculus cells in cat superior colliculus. Each data point represents average of 12 repeated stimulus presentations obtained in a randomized order for each cell.

A: from Schiller and Koerner 203; B: data from H. Sherk, unpublished observations
Figure 12. Figure 12.

Representation of different body sections in cat superior colliculus. Coordinates are shown for a map of the visual field of the colliculus and is turned so that the anterior region faces the top of the figure. Note that a disproportionately large area is devoted to the trigeminal and forelimb representations.

From Stein et al. 240
Figure 13. Figure 13.

A: map of somatosensory projection onto tectum of mouse. Letters refer to vibrissae, using notations shown in B; they indicate centers of tectal areas in which responses were recorded. Ovals, five overlapping regions within which the five rows of whiskers were represented. B: vibrissae. C: visual topography.

From Dräger and Hubel 44
Figure 14. Figure 14.

Selective enhancement of on‐response of a cell in monkey superior colliculus. Histograms on the right constructed from same cell discharges as displayed in rasters on left. Bin width, 8 ms; vertical scale, height of a bin if a cell discharged at 250 spikes/s per trial. Vertical scale line below histogram, stimulus onset; time between dots along abscissa on both rasters and histograms, 50 ms. A: cell discharge to receptive‐field stimulus, RF; dashed circle, excitatory central region of receptive field while the monkey was looking at fixation point, FP. B: increased response associated with saccades to receptive‐field stimulus; average latency after stimulus onset, 250 ms. C: saccades to a control stimulus, CON, in contralateral visual field; no enhancement.

From Wurtz and Mohler 276
Figure 15. Figure 15.

Extracellular discharge characteristics of a single cell in oculomotor nucleus of monkey. This cell increases its firing rate in association with downward eye movement. Upper row, spontaneous saccadic eye movement with intervening periods of fixation. Lower row, unit activity during smooth pursuit brought about by moving the object in front of monkey. In each of the two rows: upper trace, unit activity; lower trace, vertical eye movement. Horizontal lines superimposed on eye movement record, coordinates in degrees of deviation from straight‐ahead gaze; upward deflection, elevation of eye; downward deflection, depression of eye.

From Schiller 201
Figure 16. Figure 16.

Discharge characteristics of a unit in intermediate layers of monkey superior colliculus related to eye movement. Recordings obtained in an alert monkey with one eye surgically immobilized. A, B, C: unit discharge and eye movement in the light; moving eye unoccluded; cell discharges prior to small left and upward saccades. D: response to a 0.25° light spot moved back and forth with square wave motion within receptive field of immobilized eye; moving eye occluded. Marker, stimulus movement; HEM, horizontal eye movement record; VEM, vertical eye movement record.

From Schiller and Koerner 203
Figure 17. Figure 17.

Retinotopically coded motor field of a monkey superior colliculus unit. Each mark represents size and direction of a saccade. Open circles, saccades not associated with unit activity; filled circles, saccades preceded by a burst of spikes. Direction and size of saccade shown by quadrants designated left, right, up, down, and by degrees within these areas. Central crossing point, eye position prior to each saccade. Cell discharges only in association with small left saccades.

From Schiller and Koerner 203
Figure 18. Figure 18.

Unit activity associated with eye movement in superior colliculus of trained monkeys. A: standard tracking task: if monkey fixated center dot for 2 s the target was moved to one of the 24 positions indicated by the filled circles. B: burst index as a function of angle of movement (difference between the number of spikes occurring during a 500‐ms time sample for center target fixation and for a similar time period after eye movement to new target location): each point represents the median value of three observations. C: burst index as a function of angle and radius of eye movement. D: response of a superior colliculus unit to a series of saccades with a radius of 1° but varying in direction. Onset of target movement is indicated by arrow below each trace.

From Sparks 218
Figure 19. Figure 19.

Relation between spike burst latency and saccade latency for two neurons in monkey superior colliculus. Abscissa, interval between target onset and onset of spike pulse. Ordinate, saccade latency.

From Sparks and Pollack 221
Figure 20. Figure 20.

Effects of electrical stimulation in abducens nucleus and superior colliculus of monkey as a function of burst duration and frequency. All eye movement records are horizontal, saccades going to the left. Left, stimulating frequency is constant and duration is varied; right, duration is constant and frequency is varied. Long staircase of saccades shown at bottom of figure was elicited by stimulating within the anterior tip of superior colliculus.

From Schiller and Stryker 206
Figure 21. Figure 21.

Electrical stimulation of monkey colliculus: dependence of evoked saccade amplitude and direction on initial eye position. A saccade is represented as a directed line starting at initial eye position and ending at position to which saccade carried the eye. A: examples of colliculus‐evoked saccades that did not depend on initial position. B: hypothetical example of way in which saccades would appear if they had been goal directed.

From Robinson 189
Figure 22. Figure 22.

Results of experiment that paired single‐unit recordings and electrical stimulation at each of several sites in superficial layers of monkey superior colliculus. Map of visual field with receptive fields of 14 units is superimposed on map of motor responses, its arrow representing electrically elicited saccades at each of the 14 sites. Length of each arrow represents mean length of 8–14 stimulation‐elicited saccades; direction of each arrow represents mean direction of saccades. HM, horizontal meridian; VM, vertical meridian; hatched areas, receptive fields of single neurons. Numerals correlate receptive fields and saccades.

From Schiller and Stryker 206
Figure 23. Figure 23.

Effects of simultaneous stimulation at two collicular sites in monkey superior colliculus. Top: schematic for two sets of stimulation sites in colliculus (1 and 2). Bottom: types of saccades elicited to single (1 or 2) or paired (1 and 2) stimulation. Shaded areas, range over which saccades can be elicited by varying amount of current delivered through the two electrodes. A, anterior; M, medial; L, lateral; P, posterior; hm, horizontal meridian.
Figure 24. Figure 24.

Experimental procedures demonstrating that both retinal error and eye position information are used to compute size and direction of saccadic eye movements. A: human subject fixates in total darkness on fixation spot F, which is extinguished when stimulus S1 is flashed. As subject initiates saccade toward S1 (horizontal arrow) a second target, S2, is flashed on at the time the eye is at position marked by x, appearing straight up from fovea. Upon reaching position S1 subject makes second saccade. If second saccade is straight up, only retinal error signal is computed. If second saccade is to S2, both retinal error and eye position information are utilized. Subjects always saccade to S2. B: schematic for experiment in which collicular stimulation in monkey is used to pull the eye to position S after brief appearance of target T to which animal has been trained to saccade. Utilization of retinal error signal alone should generate an eye movement to T′. Utilization of both retinal error and eye position signals should bring eye to T. C: two saccades are shown. For the first, going directly to T, target was flashed but colliculus was not stimulated. For the second, collicular stimulation displaced the eye toward S, but eye still ended up at T, suggesting utilization of both retinal error and eye position information.

B, C: courtesy of L. E. Mays and D. L. Sparks
Figure 25. Figure 25.

Response characteristics of two units in superior colliculus of monkey before, during, and after cooling of visual cortex. A: unit 220 μm below surface of colliculus (stratum griseum superficiale). Bottom trace, time course of presentation of stimulus, a flashing spot centered in receptive field. B: unit 400 μm below surface of colliculus (stratum opticum); stimulus, a moving spot. Bottom trace, movement of stimulus.

From Schiller et al. 207
Figure 26. Figure 26.

Method for testing sensitivity in various parts of the visual field. Cat is restrained, its lateral canthi aligned along the 90° guidelines and its nose pointed along the 0° guideline to the fixation object (a piece of food in forceps). For tests of specific visual responses the novel stimulus (food in forceps or a painted ball at the end of a stiff wire) is introduced along one of the guidelines, after which the cat is freed from restraint and its behavior noted. For control tests of nonspecific responses the novel stimulus either is not introduced or is introduced laterally at approximately 120° (out of the cat's visual field) before the cat is freed.

From Sherman 216
Figure 27. Figure 27.

Development of direction‐selective responses with age in superior colliculus of kitten. Height of each bar, proportion of cells in each age group that gave direction‐selective responses. N, number of cells.

From Norton 173
Figure 28. Figure 28.

Ocular dominance histograms for striate cortex and superior colliculus of cats raised either with eye suture or with induced strabismus. Cells in group 1 can be activated only through the contralateral eye; cells in group 4 are equally driven by either eye; and cells in group 7 are activated only by the ipsilateral eye.

Data from Wiesel and Hubel 106,269,270, Sterling and Wickelgren 243, and Gordon and Gummow 73
Figure 29. Figure 29.

Response characteristics of a cat superior colliculus cell as assessed through rotated (squares) and normal (stars) eye. Twelve directions of movement in 30° steps were presented eight times in a randomized order. Each eye was tested separately. Tuning curves in the two eyes are similar, indicating that this cell responded optimally to the same direction of stimulus movement in visual space through the two eyes despite the 90° rotation of one eye. Stimulus size, 3° square; stimulus velocity, 20°/s.

From Cynader et al. 40


Figure 1.

Sagittal sections of toad, rabbit, and monkey brain. Arrows, location of superior colliculi. Note the significant difference among these three species in the relative amount of brain tissue devoted to telencephalon and to colliculus.



Figure 2.

Projection drawing of a transverse section through superior colliculus of the cat (cresyl violet stain) to show development of laminae. I1,2, sublaminae of stratum zonale; II1,2,3, sublaminae of stratum griseum superficiale; III, stratum opticum; IV, stratum griseum intermediale; V, stratum lemnisci; VI, stratum griseum profundum; VII, stratum album profundum; PAGL, periaquiductal gray, pars lateralis.

From Kanaseki and Sprague 125


Figure 3.

Representative types of neurons in frog optic tectum shown in a combined cytoarchitectonic diagram obtained from staining with hematoxylin‐eosin and reduced silver. Numerals at extreme left indicate the different layers; z, stratum zonale; p, plexiform sheets in layer 9. Golgi picture begins with a truncated ependymoglial cell. Numerals at right: 1, large pyramidal neuron with type 1 dendritic arborization pattern; 2 and 3, large pear‐shaped neurons with type 2 and 3 dendritic arborization patterns, respectively; 4, optic terminals; 5, ascending axon; 6, large ganglionic neuron; 7, small pear‐shaped neuron with descending axon; 8, small pear‐shaped neuron with a beaded axonlike process; 9, stellate neuron; 10, amacrine cell; 11, assumed endings of diencephalic afferent fibers.

From Sźekely et al. 257


Figure 4.

Cell types in cat superior colliculus. Superior colliculus is divisible into two laminar divisions based on cell types seen in Golgi‐stained material. Superficial division (I, II, and upper portion of III) is characterized by neurons with vertically elongated (narrow‐field vertical cells, C) or horizontally elongated (horizontal cells, B) dendritic fields or by dendritic fields eccentrically distributed about the cell body (piriform cells, D; wide‐field vertical cells, F; inverted ganglion cells, E). The cat is unusual in apparently lacking marginal cells but having small stellate granule cells, A, in upper part of its superficial division. Stellate cells, G, are rarely seen in the middle of superficial division but become increasingly more frequent in its deep portion as it becomes transitional with deep division. Neurons of deep division (lower portion of III, IV, V, VI) are predominantly small‐ and medium‐sized stellate multipolar neurons, H, with occasional large or massive stellate neurons, I, usually in middle regions of layers IV and VI.

Courtesy of T. P. Langer


Figure 5.

Topographic layout of visual field on surface of superior colliculus of mouse, rabbit, and cat. Derivation of 0° vertical meridian is different in each of these maps. In the mouse map the 0° vertical meridian is the vertical plane that intersects the projection of the long axis of the mouse's head. In the rabbit map the 0° vertical meridian intersects the perpendicular to the long axis of the head, which passes through the corneal vertex. In the cat map the 0° vertical meridian intersects the projection line of area centralis. In all three maps the 0° horizontal meridian intersects each of the described projection lines in the horizontal plane. Horizontal meridians run in the anteroposterior direction. The maps represent the contralateral retinal projection. A, anterior; P, posterior; M, medial; L, lateral.

Mouse data from Dräger and Hubel 44; rabbit data from Hughes 108; cat diagram courtesy of H. Sherk from data of Berman and Cynader 21 and Feldon et al. 53


Figure 6.

Retinotectal transformation. Top left: polar isograms for retinal surface of rabbit. The 0° vertical meridian intersects the perpendicular to the long axis of the head, which passes through the corneal vertex. The 0° horizontal meridian intersects the projection line in the horizontal plane. Stippled area, visual streak. Bottom left: approximate density distribution of retinal ganglion cells along horizontal, H, and vertical, V, meridians. Top right: collicular topography, polar coordinates. Stippled area, visual streak. Bottom right: collicular topography, rectilinear coordinates; transformation of circular spot on retina (black disk) is shown in colliculus by black oval area.

Bottom left, data from Hughes 108


Figure 7.

Location of transported protein in superior colliculi of rabbit, cat, and rhesus monkey after injection of labeled amino acids into right eye. In rabbit the projection is mostly contralateral. In the cat the ipsilateral projection is less dense than the contralateral projection. In monkey the ipsi‐ and contralateral projections are almost equal.

Courtesy of J. K. Harting


Figure 8.

Schematic drawing of cat superior colliculus showing possible neuronal linkages in visuomotor transform. Thick arrows, major path; boxes outline representative slices of terminal fields from optic (retinal) tract and corticotectal tracts from areas 17, 18, 19, 21, C‐B, and 7; shaded areas, major foci of degeneration after lesions to these areas. MBSC, medial brachium of superior colliculus; LBSC, lateral brachium of superior colliculus; NIC, interstitial nucleus of Cajal and adjacent reticular formation; C‐B, Clare‐Bishop area; D, nucleus of Darkshevitch; OC, oculomotor nuclei; PAG, periaquiductal gray matter. Roman numerals represent the seven collicular laminae.

From Ingle and Sprague 117


Figure 9.

A: directionally selective unit in superior colliculus. Upper trace, microelectrode recording; lower trace, potentiometer recording of mirror movements indicating time course of moving light spot; solid arrows, direction of stimulus movement; ±, on‐off response to flashed light spot; ○, no response to light spot; large open arrow, preferred direction. B: distribution of direction‐selective neurons in cat superior colliculus. Number at end of each arrow gives percentage of cells in total sample of 317 cells that responded best in direction shown by arrow. Relative length of each line is proportional to percentage of cells represented by that line. Pooled data from left and right colliculi are computed in terms of directions relative to vertical meridian; directional preferences of majority of cells are for movement away from vertical meridian.

A: from McIlwain and Buser 157. B: data from results of Berman and Cynader 21, Gordon and Gummow 73, and Sterling and Wickelgren 243


Figure 10.

Distribution of ocular dominance of cells in cat superior colliculus. Total number of cells, 316. Numeral above each bar, number of cells per category. Cells in group 1 can be activated only through the contralateral eye, cells in group 4 are equally driven by either eye, and cells in group 7 are activated only by the ipsilateral eye. Groups 2, 3, 5, and 6 represent in‐between gradations.

Data from Berman and Cynader 21, Gordon and Gummow 73, and Sterling and Wickelgren 243. Groupings 1–7 from Hubel and Wiesel 105


Figure 11.

A: histograms obtained from a single cell in monkey superior colliculus showing response to stimuli of varying diameters. Stimulus duration, 500 ms, presented once every 1,300 ms, 25 times per histogram. Response field, 18° from fovea; s/b, number of spikes per bin. B: response frequency as a function of stimulus size for four superior colliculus cells in cat superior colliculus. Each data point represents average of 12 repeated stimulus presentations obtained in a randomized order for each cell.

A: from Schiller and Koerner 203; B: data from H. Sherk, unpublished observations


Figure 12.

Representation of different body sections in cat superior colliculus. Coordinates are shown for a map of the visual field of the colliculus and is turned so that the anterior region faces the top of the figure. Note that a disproportionately large area is devoted to the trigeminal and forelimb representations.

From Stein et al. 240


Figure 13.

A: map of somatosensory projection onto tectum of mouse. Letters refer to vibrissae, using notations shown in B; they indicate centers of tectal areas in which responses were recorded. Ovals, five overlapping regions within which the five rows of whiskers were represented. B: vibrissae. C: visual topography.

From Dräger and Hubel 44


Figure 14.

Selective enhancement of on‐response of a cell in monkey superior colliculus. Histograms on the right constructed from same cell discharges as displayed in rasters on left. Bin width, 8 ms; vertical scale, height of a bin if a cell discharged at 250 spikes/s per trial. Vertical scale line below histogram, stimulus onset; time between dots along abscissa on both rasters and histograms, 50 ms. A: cell discharge to receptive‐field stimulus, RF; dashed circle, excitatory central region of receptive field while the monkey was looking at fixation point, FP. B: increased response associated with saccades to receptive‐field stimulus; average latency after stimulus onset, 250 ms. C: saccades to a control stimulus, CON, in contralateral visual field; no enhancement.

From Wurtz and Mohler 276


Figure 15.

Extracellular discharge characteristics of a single cell in oculomotor nucleus of monkey. This cell increases its firing rate in association with downward eye movement. Upper row, spontaneous saccadic eye movement with intervening periods of fixation. Lower row, unit activity during smooth pursuit brought about by moving the object in front of monkey. In each of the two rows: upper trace, unit activity; lower trace, vertical eye movement. Horizontal lines superimposed on eye movement record, coordinates in degrees of deviation from straight‐ahead gaze; upward deflection, elevation of eye; downward deflection, depression of eye.

From Schiller 201


Figure 16.

Discharge characteristics of a unit in intermediate layers of monkey superior colliculus related to eye movement. Recordings obtained in an alert monkey with one eye surgically immobilized. A, B, C: unit discharge and eye movement in the light; moving eye unoccluded; cell discharges prior to small left and upward saccades. D: response to a 0.25° light spot moved back and forth with square wave motion within receptive field of immobilized eye; moving eye occluded. Marker, stimulus movement; HEM, horizontal eye movement record; VEM, vertical eye movement record.

From Schiller and Koerner 203


Figure 17.

Retinotopically coded motor field of a monkey superior colliculus unit. Each mark represents size and direction of a saccade. Open circles, saccades not associated with unit activity; filled circles, saccades preceded by a burst of spikes. Direction and size of saccade shown by quadrants designated left, right, up, down, and by degrees within these areas. Central crossing point, eye position prior to each saccade. Cell discharges only in association with small left saccades.

From Schiller and Koerner 203


Figure 18.

Unit activity associated with eye movement in superior colliculus of trained monkeys. A: standard tracking task: if monkey fixated center dot for 2 s the target was moved to one of the 24 positions indicated by the filled circles. B: burst index as a function of angle of movement (difference between the number of spikes occurring during a 500‐ms time sample for center target fixation and for a similar time period after eye movement to new target location): each point represents the median value of three observations. C: burst index as a function of angle and radius of eye movement. D: response of a superior colliculus unit to a series of saccades with a radius of 1° but varying in direction. Onset of target movement is indicated by arrow below each trace.

From Sparks 218


Figure 19.

Relation between spike burst latency and saccade latency for two neurons in monkey superior colliculus. Abscissa, interval between target onset and onset of spike pulse. Ordinate, saccade latency.

From Sparks and Pollack 221


Figure 20.

Effects of electrical stimulation in abducens nucleus and superior colliculus of monkey as a function of burst duration and frequency. All eye movement records are horizontal, saccades going to the left. Left, stimulating frequency is constant and duration is varied; right, duration is constant and frequency is varied. Long staircase of saccades shown at bottom of figure was elicited by stimulating within the anterior tip of superior colliculus.

From Schiller and Stryker 206


Figure 21.

Electrical stimulation of monkey colliculus: dependence of evoked saccade amplitude and direction on initial eye position. A saccade is represented as a directed line starting at initial eye position and ending at position to which saccade carried the eye. A: examples of colliculus‐evoked saccades that did not depend on initial position. B: hypothetical example of way in which saccades would appear if they had been goal directed.

From Robinson 189


Figure 22.

Results of experiment that paired single‐unit recordings and electrical stimulation at each of several sites in superficial layers of monkey superior colliculus. Map of visual field with receptive fields of 14 units is superimposed on map of motor responses, its arrow representing electrically elicited saccades at each of the 14 sites. Length of each arrow represents mean length of 8–14 stimulation‐elicited saccades; direction of each arrow represents mean direction of saccades. HM, horizontal meridian; VM, vertical meridian; hatched areas, receptive fields of single neurons. Numerals correlate receptive fields and saccades.

From Schiller and Stryker 206


Figure 23.

Effects of simultaneous stimulation at two collicular sites in monkey superior colliculus. Top: schematic for two sets of stimulation sites in colliculus (1 and 2). Bottom: types of saccades elicited to single (1 or 2) or paired (1 and 2) stimulation. Shaded areas, range over which saccades can be elicited by varying amount of current delivered through the two electrodes. A, anterior; M, medial; L, lateral; P, posterior; hm, horizontal meridian.



Figure 24.

Experimental procedures demonstrating that both retinal error and eye position information are used to compute size and direction of saccadic eye movements. A: human subject fixates in total darkness on fixation spot F, which is extinguished when stimulus S1 is flashed. As subject initiates saccade toward S1 (horizontal arrow) a second target, S2, is flashed on at the time the eye is at position marked by x, appearing straight up from fovea. Upon reaching position S1 subject makes second saccade. If second saccade is straight up, only retinal error signal is computed. If second saccade is to S2, both retinal error and eye position information are utilized. Subjects always saccade to S2. B: schematic for experiment in which collicular stimulation in monkey is used to pull the eye to position S after brief appearance of target T to which animal has been trained to saccade. Utilization of retinal error signal alone should generate an eye movement to T′. Utilization of both retinal error and eye position signals should bring eye to T. C: two saccades are shown. For the first, going directly to T, target was flashed but colliculus was not stimulated. For the second, collicular stimulation displaced the eye toward S, but eye still ended up at T, suggesting utilization of both retinal error and eye position information.

B, C: courtesy of L. E. Mays and D. L. Sparks


Figure 25.

Response characteristics of two units in superior colliculus of monkey before, during, and after cooling of visual cortex. A: unit 220 μm below surface of colliculus (stratum griseum superficiale). Bottom trace, time course of presentation of stimulus, a flashing spot centered in receptive field. B: unit 400 μm below surface of colliculus (stratum opticum); stimulus, a moving spot. Bottom trace, movement of stimulus.

From Schiller et al. 207


Figure 26.

Method for testing sensitivity in various parts of the visual field. Cat is restrained, its lateral canthi aligned along the 90° guidelines and its nose pointed along the 0° guideline to the fixation object (a piece of food in forceps). For tests of specific visual responses the novel stimulus (food in forceps or a painted ball at the end of a stiff wire) is introduced along one of the guidelines, after which the cat is freed from restraint and its behavior noted. For control tests of nonspecific responses the novel stimulus either is not introduced or is introduced laterally at approximately 120° (out of the cat's visual field) before the cat is freed.

From Sherman 216


Figure 27.

Development of direction‐selective responses with age in superior colliculus of kitten. Height of each bar, proportion of cells in each age group that gave direction‐selective responses. N, number of cells.

From Norton 173


Figure 28.

Ocular dominance histograms for striate cortex and superior colliculus of cats raised either with eye suture or with induced strabismus. Cells in group 1 can be activated only through the contralateral eye; cells in group 4 are equally driven by either eye; and cells in group 7 are activated only by the ipsilateral eye.

Data from Wiesel and Hubel 106,269,270, Sterling and Wickelgren 243, and Gordon and Gummow 73


Figure 29.

Response characteristics of a cat superior colliculus cell as assessed through rotated (squares) and normal (stars) eye. Twelve directions of movement in 30° steps were presented eight times in a randomized order. Each eye was tested separately. Tuning curves in the two eyes are similar, indicating that this cell responded optimally to the same direction of stimulus movement in visual space through the two eyes despite the 90° rotation of one eye. Stimulus size, 3° square; stimulus velocity, 20°/s.

From Cynader et al. 40
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Article Title: The Superior Colliculus and Visual Function
 

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Peter H. Schiller. The Superior Colliculus and Visual Function. Compr Physiol 2011, Supplement 3: Handbook of Physiology, The Nervous System, Sensory Processes: 457-505. First published in print 1984. doi: 10.1002/cphy.cp010311