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REPRESENTATION OF THE VISUAL FIELD IN THE SUPERIOR COLLICULUS OF THE GREY SQUIRREL (SCIURUS CAROLINENSIS) ANDI THE TREE SHREW (TUPAIA GLIS)

Jbull I RONALD H LANE JOHN M ALLMAN AND JON H KAAS

I Laboratory of Neurophysiology University of Wisconsin Madison Wise 53706 (USA)

I (Accepted September 7th 1970)

t I I INTRODUCTION

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1 General resemblances between tree shrew and squirrel in size appearance and I behavior are readily apparent and have been noted by various investigatorss2942

Both are small arboreal diurnal mammals with all cone retinas3bull3o The two groups have been evolving independently since their common divergence from ancestral

I insectivores and they seem to offer an excellent opportunity for detailed comparisons

1 of the visual system in order to evaluate the role of adaptation to similar environshyments in brain evolution Such comparisons between squirrels and tree shrews have f

j already been madel and the results suggest considerable parallel or convergent evolution of the visual system of the two groups

t The superior colliculus is sometimes considered rather stable in vertebrate evolution since the topological organization is remarkably similar in fish 19 31I amphibians1018 reptiles l6 birds14 and mammals26813323S-3743 However signifshy

t icant variations occur in the magnification of a region of the retinal projection2843

t and in the formation of a substantial uncrossed pathway in some mammals941 The superior colliculus in both tree shrewS and squirrel40 is large and the lamishy

nation is clear and well developed LeGros ClarkS noted that the superior colliculus i17 ~-n is proportionately larger in the tree shrew than in any other mammal but the superior

i colliculus of the squirrel is riearly as large By using electrophysiological mapping 4 j I techniques we sought to determine the topology of the representation of the visual 1

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field in the superior colliculus and obtained evidence for the representation of the j II ~ complete retina of one eye in the contralateral superior colliculus There was no i evidence for representation of any portion of the retina in the ipsilateral superior I shy

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~ The topology of the representation of the visual field in the superior coIliculus r was determined by relating the positions of receptive fields for single neurons or

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small clusters of neurons to the locations of the corresponding recording sites The procedure in general was similar to that used by others in determining the represenshytation of the visual field in the superior colliculus32 and lateral geniculate28 of the rat

Animal preparation

The results were obtained from 12 grey squirrels (Sciurus carolinensis) and 4 tree shrews (Tupaia gUs) Each animal was anesthetized with urethane (125 mg 100 g body wt) fitted with a tracheal cannula and placed in a headholder with minimal obstruction of the visual field The lids of both eyes were removed and the right eye was fixed by suturing the sclera to a metal ring anchored to the headholder The pupils were dilated with 20 cycJopentolate hydrochloride and the corneal surface was protected with a thin layer of silicone fluid The occipital cortex of both cerebral hemispheres was exposed the dura removed and the brain surface protected by mineral oil retained in a chamber of acrylic plastic Stimuli were presented on a translucent plastic hemisphere which corresponded to the visual field of one eye The right eye was centered in the hemisphere equidistant from all points on the surface and the plane of the open side of the hemisphere was aligned with the plane of the corneal limbus of the eye

Stimuli

Receptive field boundaries were defined as the margins of the area in which visual stimuli produced an increase in the activity of the recorded neurons The usual stimulus was a narrow slit of light 5 in length projected on the surface of the plastic hemisphere in a dimly lit room and moved repeatedly through the visual field from a number of intersecting directions The boundaries of most receptive fields were checked with small moving shadows produced by backlighting small targets

Recording

Tungsten micro electrodes were used with a tip exposure of 5 pm or more so that the activity of a number of neurons was usually recorded and single neurons usually were not isolated The superior colliculus was approached by penetrating with microshyelectrodes from the dorsal surface of the brain through the cortex to the tectum below Recording depths were noted and microlesions were made (20-30 pA for 10 sec) to mark depths in the electrode tracts The recording sites were later identified in frozen or paraffin-embedded brain sections cut in the coronal plane parallel to the electrode penetrations and stained with cresyl violet for cells The superior collicshyulus was reconstructed from the serial sections and the recording sites were indicated on the reconstruction

Estimating the projection of the line of decussation of the retina

The portion of retina projecting to striate cortex of the ipsilateral hemisphere

Brain Research 26 (1971) 277-292

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Ibull Fig 1 The superior colliculus of grey squirrel (left) and tree shrew (right) The 30 um brain sections I

stained with thionin are in the sagittal (top) and coronal (bottom) planes I

t f and the portion projecting to the contralateral hemisphere can be determined by

recording from striate cortex of both hemispheres while stimulating one eye Previous experiments have indicated that approximately the most temporal 30deg of the retina project to the ipsilateral striate cortex of the squirrel and the tree shrew while close

t to 1500 of nasal retina project to the contralateral striate cortex22 23 Receptive fields determined for recording sites in the contralateral or ipsilateral striate cortex are located in the temporal or nasal visual field respectively and overlap at most ( only a few degrees for recording sites at the lateral borders of striate cortex22 bull23bull Thus receptive fields for a few recording sites along the lateral boundary of striateI


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cortex of each hemisphere can define the projection into the visual field of the retinal line of decussation

In the present experiments at the beginning of each recording session receptive fields were determined for cortical points along the lateral margins of striate cortex (V I) of each cerebral hemisphere and these receptive fields were used to define the line of decussation As in previous experiments22 bull23 the standard or zero horizontal reference was a line corresponding to the horizontal meridian or equator of the retina and was estimated by projecting the optic nerve head onto the surface of the plastic hemisphere Measurements from retinas removed and mounted whole indicate that the nerve head which forms a horizontal band in the squirrel is about 16deg above the ltequator of the retina and about 5deg above in the tree shrew Therefore the horizontal meridian was placed 16deg above the projection of the nerve head into the visual field in the squirrel and 5deg above in the tree shrew

RESULTS

Normal appearance

The superior colliculus in tree shrew and grey squirrel is a large structure with distinct and well-developed lamination The histological appearance of the superior colliculus in coronal and sagittal sections stained with thionin is shown in Fig 1 and the close resemblance of the superior colliculus of the tree shrew to that of the squirrel is apparent In both the stratum griseum superficiale is an easily identifiable lamina approximately 600 m in thickness and it is possible to identify several substrata The stratum opticum is also distinct and is characterized by loosely packed neurons

Electrophysiological mapping

The results of the experiments in which recording sites in the superior colliculus were related to the positions of corresponding receptive fields resulted in the followshying conclusions for both the squirrel and tree shrew (I) the complete visual field of the one eye is represented in the contralateral superior coUiculus (2) the representation is topological and similar in orientation to that reported for other mammals (3) the region of the visual field corresponding to the intersection of the line of decussation and the horizontal meridian receives a greater degree of representation than other segments (4) the receptive fields for recording sites in the deeper layers of the collicshyulus are larger than receptive fields for more superficial layers and (5) an ipsilateral projection if present is minuscule

Representation of the visual field in the squirrel

Before recording from the superior colliculus of each animal the projection of the line of decussation into the visual field was estimated from the locations of receptive fields for neurons in the first visual area (striate cortex) The results of one


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Fig 2 The location of receptive fields for cortical recording sites in grey squirrel 70-101 The visual field of the right eye is represented by an internal view of a hemisphere divided by horizontal parallels and vertical meridians The nasal visual field is left temporal visual field is right The circumscribed areas marked by a continuous line are receptive fields for sites in striate cortex of the contralateral cerebral hemisphere The dashed lines mark receptive fields for sites in the ipsilateral striate cortex The zero vertical meridian indicated by a heavy line is the estimated projection into the visual field of the line of decussation of the retina The horizontal bar indicates the projection of the elongated horizontal optic nerve head of the squirrel

experiment are illustrated in Fig 2 where receptive fields are shown for neurons from the lateral margins of striate cortex both ipsilateral and contralateral to the stimulated eye These receptive fields were used to define the zero vertical meridian or line of decussation Receptive fields from neurons in ipsilateral cortex are marked by dashed lines to the right of the zero vertical meridian and were used to estimate the most temporal extent of the smaller segment of the visual field that corresponds to the uncrossed projection from the retina Receptive fields from neurons in contrashylateral striate cortex are on the left of the zero vertical meridian and were used to estimate the most nasal extent of the larger segment of the visual field that corresponds to the completely crossed projection from the retina Receptive fields near the zero vertical meridian and a number of degrees i1 the lower visual field or upper field were determined from neurons in rostral striate cortex or striate cortex of the posterior


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Fig 4 Receptive fields for recording sites in the contralateral superior colliculus (areas circumshyscribed by a thin line) and the ipsilateral striate cortex (shaded areas) of grey squirrel 70-189 Note the overlap of the contralateral projection to the superior colliculus with ipsilateral projection to striate cortex The vertical line represents the line of decussation the horizontal line the horizontal meridian The nasal visual field is on the left

pole and ventral surface respectively In other experiments similar recordings from striate cortex were used to determine the projection of the line of decussation

After receptive fields were det~rmined for recording sites in striate cortex the contralateral superior colliculus was explored Fig 3 shows positions of the reshyceptive fields for the electrode penetrations indicated on the dorsal view of the left superior colliculus Receptive field locations did not change as the electrode peneshytnited deeper into the colliculus when the penetrations were perpendicular to the layers of cells However penetrations such as 1 2 8 17 etc continued obliquely some distance within a layer of cells and receptive fields for successive recording depths progressed toward the periphery of the visual field The results depicted in Fig 3 provide clear evidence that the entire visual field of one eye including the portion of the field beyond the line of decussation is represented in the contralateral superior colliculus Thus neurons in the depths of penetration 22 for example had receptive fields almost 30deg nasal to the line of decussation


284 R H LANE et al v

Further evidence that the contralateral projection to the superior colliculus extends past the line of decussation and overlaps the projection to the ipsilateral geniculo-striate system is presented in Fig 4 In this experiment the striate cortex of the ipsilateral hemisphere was more fully explored and the locations of the resulting receptive fields are shown as lightly shaded areas Receptive fields which are not shown were also obtained from the contralateral striate cortex and these fields were to the left of the estimated line of decussation in the illustration The areas circumshyscribed by thin lines represent receptive fields for electrode penetrations in the rostralshylateral portion of the superior colliculus Again it is easy to see that the representation of the visual field of one eye in the contralateral superior colliculus is more extensive than in contralateral striate cortex and includes the nasal sector of the visual field which is represented in ipsilateral striate cortex

In all other experiments in which the rostral-lateral margin of the superior colliculus was explored receptive fields were found to extend up to 30deg past the estimated line of decussation The same result was obtained in two experiments in which receptive fields were determined for recording sites in the dorsal lateral genicshyulate nucleus as well as striate cortex and superior colliculus Receptive fields for neurons in the contralateral superior colliculus were found to extend almost 30deg past the most nasal receptive fields for neurons in the contralateral geniculate nucleus or in the contralateral striate cortex

The topology of the representation of the visual field in the superior colliculus is indicated in Fig 6 The lower visual field is represented laterally and caudally and the region of the line of decussation is represented rostrally and laterally There is a noticeable expansion of the representation of the portion of the visual field correshysponding to the intersection of the line of decussation and the horizontal meridian We have found that this sector of the retina in both grey squirrel and tree shrew has the highest density of ganglion cells but there is no suggestion of a fovea or area centralis

Receptive fields near the intersection of the zero horizontal and zero vertical meridians were usually somewhat smaller than those elsewhere The receptive fields also increased in size as the recording electrode progressed from the deep levels of the stratum griseum superficiale into the dorsal stratum opticum At deep levels of the stratum opticum the receptive fields were so enlarged they became poorly defined The size of a deep receptive field is indicated by the large receptive field for peneshytration 18 in Fig 3

In all the recordings from the superior colliculus neurons were activated only from the contralateral eye Even though the ipsilateral eye was systematically stimushylated there was no evidence of an ipsilateral projection to any area or stratum of the superior colliculus from which recordings were obtained

In one experiment penetrations immediately rostral and deep to the superior colliculus revealed a second area which also responded to visual stimuli This area histologically confirmed as the lateral portion of the posterior pretectal area was activated by both contralateral and ipsilateral retinal stimulation The receptive fields were temporal to the zero vertical meridian near the zero horizontal meridian


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Fig 6 Dorsal views of the superior colliculus of the grey squirrel and tree shrew with horizontal parallels and vertical meridians of the contralateral eye

and progressed lower in the visual field with deeper recording sites These results suggest that the pretectal area of the squirrel isin general organized like that of the rat and receives input from both eyes in as the rat33bull

Representation of the visual field in the tree shrew

The same procedure was employed in studying the tree shrew as with the grey squirreL The line of decussation was defined by determining receptive fields at the border of V I and V II for both the contralateral and ipsilateral visual cortex The contralateral superior colliculus was then explored Fig 5 illustrates the relative positions of the receptive fields for the recording penetrations as indicated on the dorsal view of the tectum

As in the grey squirrel the results indicated that the portion of the visual field nasal to the projection of the line of decussation is represented in the contralateral superior colliculus Receptive fields for neurons in the depths of penetrations 22 282726 and 23 were close to 30deg nasal to the line of decussation The locations of the recording sites for penetration 22 are shown in Fig 5 In other experiments receptive fields for neurons in the rostral and lateral margins of the colliculus were also nasal to the line of decussation

The topological organization of the superior colliculus of the tree shrew is I I

similar to the organization in the grey squirreL The vertical and horizontal meridians are positioned similarly on the tectum in both species The upper visual field is

represented rostro-medially and the lower visual field is represented caudo-Iaterally on the tectum The area of visual field near the intersection of the zero horizontal and vertical meridians receives a greater representation than the other areas (see Fig 6)


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Fig 7 The representation of the visual field in the right superior coIliculus (SC) and striate cortex (V I) of grey squirrel The complete visual field of the left eye is represented in the right superior colliculus Only the most temporal 1500 of the visual field of the left eye are represented in right striate cortex The most nasal 30deg of the right eye are indicated by the dashed arrow and are represented in ipsilateral striate cortex overlapping in part the larger projection from the contralateral eye No ipsilateral projection to the superior colliculus was disclosed but the expected location is indicated L F lower visual field U F upper visual field L D line of decussation

As in the squirrel there was no evidence for any input from the ipsilateral retina in any lamina or area of the superior colliculus of the tree shrew from which recordings were obtained The size of the receptive fields increased as the fields were centered more distal to the intersection of the zero horizontal and zero vertical meridians and as the recording electrode penetrated into the stratum opticum

DISCUSSION

The results suggest that there is a topological projection of the complete contrashylateral retina to the superior colliculus that the ipsilateral projection if present is minuscule and that a portion of the retina receives an expanded representation These conclusions are summarized in Figs 6 and 7

The conclusion that there is a complete representation of the contralateral retina in the superior colliculus may raise the question whether or not the receptive fields nasal to the zero vertical meridian are a consequence of undetected change in the position of the eye or an incorrect estimate of the line of decussation In each exshyperiment the contralateral eye was sutured in place and the animal deeply anestheshytized In addition the possibility of eye movement was checked by periodically redetermining the location of receptive fields for recording sites in both the striate cortex and tectum In the experiments reported we found no evidence of eye moveshyments extensive enough to be detected by a significant change in the position of a redetermined receptive field We also believe that the projection of the line of deshycussation into the visual field was estimated correctly within a few degrees in each case After extensive experiments determining the representation of the visual field


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in striate and prestriate cortex in the grey squirrel22 and the tree shrew23 it is clear that receptive fields from only a few recording sites near the lateral boundary of striate cortex from both the ipsilateral and contralateral hemisphere can be used to accurately estimate the position of the line of decussation at least near its intersection with the horizontal meridian

Since the receptive fields determined for the rostral-lateral margin of the superior colliculus were found to extend nasally past the most nasal receptive fields determined for neurons in the contralateral striate cortex and overlapped receptive fields for neurons in the ipsilateral striate cortex over the complete horizontal extent of 30deg we conclude that all portions of the retina project to the contralateral tectum It is necessary to admit that this conclusion extends beyond the direct evidence since the complete superior colliculus was not explored The representation of a sector of the upper temporal visual field was not established in the tree shrew because the parts of the medial wall and the medial-caudal portions of the tectum that underlie the midshysagittal and transverse venous sinuses were not explored However the medial wall was explored by a lateral approach in one squirrel and the representation of the visual field was found to extend 1500 temporal to the line of decussation The representation of the most nasal visual field was not established in either the tree shrew or grey squirrel since this segment of the visual field is blocked by the head of the animal during the normal resting eye positions maintained during the present experiments

The reports of other workers suggest that a complete representation of the contralateral retina may exist in the superior colliculus of other species In an earlier study of the ground squirrel by Woolsey et al 43 the line of decussation was not defined but close to 1800 of visual field were found represented in the contralateral tectum Likewise Siminoff et af32 did not define the line of decussation in the rat but also found close to 180deg of visual field represented in the superior colliculus In recording from single cells in the superior colliculus ofthe cat McIlwain and Buser27

reported large receptive fields which extended across the vertical meridian well into the ipsilateral visual field Sprague et al 3s also found receptive fields for neurons in the superior colliculus of the cat which crossed the vertical meridian or line of deshycussation and were partly or wholly in the ipsilateral hemifield Recently a more detailed investigation of the representation of the visual field in the superior collicshyulus of the cat defined a rostral area in which the neurons had receptive fields nasal to the vertical meridian and were activated only by the contralateral eye8 These electrophysiological results in the cat are supported by the experiments of Stone38

with optic tract section and by the results of experiments depicting the terminal degeneration of optic tract fibers after focal lesions of the retina25 bull After cutting the optic tract in the cat Stone38 found that only 75 of the ganglion cells temporal to the line of decussation of the retina projected to the ipsilateral hemisphere while 100 of the ganglion cells nasal to the line of decussation projected to the contrashylateral hemisphere The remaining cells in the temporal retina were found to proshyject as do cells in the nasal retina to the contralateral side and Stone suggested that they terminate in the superior colliculus Subsequently Laties and Sprague25 found that lesions of the temporal retina in cat are followed by a small number of degen-


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A SUMMARY OF ANATOMICAL REPORTS OF IPSILATERAL PROJEcnONS FROM THE RETINA TO THE SUPERIOR

COLLICULUS OF THE TREE SHREW AND SQUIRREL

Amount Location Investigator

Tree shrew Tree shrew Tree shrew Squirrel (ground) Squirrel (flying) Squirrel (ground)

None Distinct group Greatly reduced Less than J of total Less than 1of total Probably none (myelin stain)

Not stated Not stated Lateral half Throughout

Tigges39

Campbell et al 4

Laemle24

Tigges3~

Tigges39

Johnston and Gardner21

erating fibers to the contralateral superior colliculus In view of these results it seems reasonable to expect a complete representation of the visual field of one eye in the superior colliculus in a number of mammalian species

It is interesting that we have found no electrophysiological evidence of an ipsilateral input to the superior colliculus of the squirrel and tree shrew Likewise slow waves in the superior coIliculus of the ground squirrel were evoked only by light flashes to the contralateral eye43bull After a careful search Siminoff et al 32 found no neurons in the superior colliculus of the rat which were influenced by input from the ipsilateral eye However the activation of neurons in the superior colliculus by stimulation of the ipsilateral eye has been reported for the cat2835 monkey1 and opossum12 The lack of electrophysiological evidence for ipsilateral activation in the rat is puzzling in view of the anatomical evidence for ipsilateral input although the ipsilateral input is sparse and limited to the deeper layers15 26 There is also anatomshyical evidence for ipsilateral input to the superior colliculus in both the tree shrew and squirrel but it is clear that the ipsilateral input consists of only a small portion of the total (see Table 1) and this limited input appears to terminate mainly in the stratum opticum Since in the main our recordings were from the stratum griseum there may be a small ipsilateral projection in the tree shrew and squirrel that was undetected by our recording methods If ipsilateral input has any role in stereoshyscopic vision one would expect the termination to be confined to the rostral-lateral segment of the colliculus between the placement of the 0deg and 30deg vertical meridians Such a rostral-lateral restriction of ipsilateral input has been reported for rabbitl1

and rat15 26

The topology of the representation of the visual field in the superior colliculus of tree shrew and grey squirrel supports the view that there has been some convergent evolution in the development of the two structures In both groups the representation of a comparable part of the visual field is significantly expanded That is the region of the visual field corresponding to the area of the intersection of the line of decusshysation and the horizontal mericJjan of the retina receives a disproportionately large representation (see Fig 6) This sector of the visual field of one eye overlaps the visual field of the other eye and therefore stereoscopic vision is possible in both the tree


290 v R H LANE et al

shrew and grey squirrel However in view of the lack of evidence for any substantial ipsilateral projection to the superior colliculus that structure appears to have little to do with stereoscopic vision There must be other reasons for the development of expanded representation of frontal vision in the superior colIiculus of the tree shrew and squirrel It is known that depriving the tree shrew or grey squirrel of the geniculoshystriate system leaves many discriminative capacities iRtact20 34 and these remaining capacities presumably depend on tectothalamocortical systems In contrast unilateral ablation of the superior colliculus in the tree shrew produces an animal that appears to be blind in the contralateral eye20

SUMMARY

Microelectrodes were used to map the representation of the visual field in the superior colliculus in two arboreal diurnal mammals the grey squirrel and the tree shrew in which the superior colliculus is extremely well developed For comparison portions of lateral striate cortex of both hemispheres were mapped in the same animals The results suggest that the projection of the visual field to the superior colliculus both in tree shrew and squirrel differs from that to striate cortex in two ways (1) the comshyplete visual field of each eye appears to be represented in the contralateral superior colliculus while the most nasal 30deg of the visual field of each eye is represented in ipsilateral striate cortex and (2) neurons in the superior colliculus are activated only by stimuli to the contralateral eye while the lateral striate cortex receives input from both the ipsilateral eye and the contralateral eye The projection to the superior colliculus in tree shrew and squirrel resembles that to striate cortex in that the region of the visual field corresponding to the intersection of the line of decussation and the horizontal meridian of the retina is represented in a larger area of the superior collicshyulus than other portions of the visual field

ACKNOWLEDGEMENTS

We thank Prof C N Woolsey for helpful comments on the manuscript Mrs Jo Ann Ekleberry for preparation of histological material Mr Terrill Stewart for photography and Mr Timothy Yolk for illustration 7

Supported by Grant 5-POI-NS-06225 to the Laboratory of Neurophysiology Vniv of Wisconsin R H Lane is a Rehabilitation Service Administration Trainee (HEW 161-T-70) in the Department of Communicative Disorders J M Allman is a National Science Foundation Predoctoral Fellow in the Department of Anthroshypology Dniv ofChicago and J H Kaas is supported by I-POI-HD-03352

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2 APTER J T Projection of the retina on superior colliculus of cats J Neurophysiol 8 (1945) 123-134


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3 ARDEN G B AND TANSLEY K The spectral sensitivity of the pure-cone retina of the grey squirrel (Sciurus carolinensis leucotis) J Physiol (Lond) 127 (1955) 592-602

4 CAMPBELL C B G JANE J A AND YASHON D The retinal projections of the tree shrew and hedgehog Brain Research 5 (1967) 406-418 CLARK W E LBG The Antecedents ofMan Edinburgh Uolv Press Edinburgh 1959 pp 1-388

6 COOPER S DANIEL P M AND WHITTERIDGE D Nerve impulses in the brainstem and cortex of the goat Spontaneous discharges and responses to visual and other afferent stimuli J Physiol (Lond) 120(1953) 514--527

7 DIAMOND I T AND HALL W c Evolution of neocortex Science 164 (1969) 251-262 8 FELDON S FELDON P AND KRUGER L Topography of the retinal projection upon the superior

colliculus of the cat Vision Res 10 (1970) 135-143 9 GARY L J AND POWELL T P S The projection of the retina in the cat J Anat (Lond)

102(1968)189-222 GAZE R M The representation of the retina on the optic lobe of the frog Quart J expo Physiol 43(1958)209-214

II GIOLLI R A AND GUTHRIE M D The primary optic projections in the rabbit An experimental degeneration study J compo Neurol 136 (1969) 99-126

12 GOODWIN H E AND HILL R M Receptive fields of a marsupial visual system 1 The superior colliculus Amer J Optom 45 (1968) 358-363

13 HAMDI F A AND WHrTTERIDGE D The representation of the retina on the optic lobe of the pigeon and the superior colliculus of the rabbit and goat J Physiol (Lond) 121 (1953) 44

14 HAMDI F A AND WHITTERIDGE D The representation of the retina on the optic tectum of the pigeon Quart J expo Physiol 34(1954) 111-119 HAYHOW W R SEFTON A AND WEBB C Primary optic centers of the rat in relation to the terminal distribution of the crossed and uncrossed optic nerve fibers J comp Neurol 118 (1962) 295-321

16 HERIC T M AND KRUGER L Organization of the visual projection upon the optic tectum ofa reptile (Alligator mississippiensis) J compo Neurol 124 (1965) 101-111

17 HUMPHREY N K Responses to visual stimuli of units in the superior colliculus of rats and monkeys Exp Neurol 20 (1968) 312-340

18 JACOBSON M The representation of the retina on the optic tectum of the frog Correlation between retinotectal magnification factor and retinal ganglion cell count Quart J expo Physiol 47 (1962) 170-178

19 JACOBSON M AND GAZE R M Types of visual response from single units in the optic tectum and optic nerve of goldfish Quar J expo Physiol 49 (1965) 199-209 JANE J A CARLSON N J AND LEVEY N A comparison of the effects of lesions of striate cortex and superior coIliculus on vision in the Malayan tree shrew (Tupaia glis) Anat Rec 163 (1969) 306-307

21 JOHNSON P J AND GARDNER E Central connections of the optic nerves in mammals with pure-cone retinae Ana Rec 134 (1959) 205-216

22 KAAS J DIAMOND I T HALL W C AND KILLACKY H Topographic representation of the visual field in the neocortex of the grey squirrel Ana Rec 163 (1969) 207

23 KAAS J H KILLACKY H HALL W c AND DIAMOND I T Cortical visual areas in the tree shrew (Tupaia glis) In preparation

24 LAEMLE L K Retinal projections of Tupaia gUs Brain Behav Evol I (1968) 473-499 LAnES A M AND SPRAGUE J M The projection of optic fibers to the visual centers in the cat J camp Neurol 127 (1966) 3570

26 LUND R D Uncrossed visual pqtnways of hooded albino rats Science 149 (l965) 1506-1507 27 McILWAIN J T AND BUSER P Receptive fields of single cells in the cats superior colliculus

Exp Brain Res 5 (1968) 314--325 28 MONTERO V M BRUGGE J G AND BEITEL R E Relation of the visual field to the lateral

geniculate body of the albino rat J Neurophysial 31 (1968) 221-236 29 POLYAK S D The Vertebrate Visual System Univ of Chicago Press Chicago 1957 pp 1-1390

SAMORAJSKl T ORDY J M AND KEEFE J R Structural organization of the retina in the tree shrew (Tupaia glis) J Cell Bioi 28 (1966) 489-509

31 SCHWASSMANN H 0 AND KRUGER L Organization of the visual projection upon the optic tectum of some fresh water fish J comp Neural 124 (1965) 113 126

32 SIMINOFF R SCHWASSMANN H 0 AND KRUGER L An electrophysiological study of the visual projection to the superior colliculus of the rat J compo Neurol 127 (1966) 435-444


292 R H LANE et al

33 SIMINOFF R SCHWASSMANN H 0 AND KRUGER L Unit analysis of the pretectal nuclear group in the rat J camp Neural 130 (1967) 329-342

34 SNYDER M AND DIAMOND LT The organization and function of the visual cortex in the tree shrew Brain Behav Eva I (1968) 244-288

35 SPRAGUE J M MARCHlAFAVA P L AND RIZZOLAlTl G Unit responses to visual stimuli in the superior colliculus of the unanesthetized mid-pontine cat Arch ital BioI 106 (1968) 169-193

36 STERLING P AND WICKELGREN B G Visual receptive fields in the superior colliculus of the cat J Neurophysiol 32 (1969) I-IS

37 STRASCffiLL M AND HOFFMANN K P Functional aspects of localization in the cats tectum opticum Brain Research 13 (1969) 274-283

38 STONE J The naso-temporal division of the cats retina 1 camp Neural 126 (1966) 585-600 39 TIGGES I Ein experimenteller Beitrag zum subkortikalen optischen System von Tupaia glis

Folia primatol 4 (1966) 103-123 40 TIGGES I Retinal projections to subcortical optic nuclei in diurnal and nocturnal squirrels

Brain Behav Evol (1970) in press 41 TIGGES M AND TIGGES I The retinofugal fibers and their terminal nuclei in Galago crassishy

caudatus (primates) J camp Neural 138 (1970) 87-102 42 WALKER E P Mammals of the World Johns Hopkins Press Baltimore 964 pp 1-1500 43 WOOLSEY C N CARLTON T G KAAS J R AND EARLS F The projection of the visual field

upon the superior colliculus of the ground squirrel (Citelus lridecemlinealus) Vision Res in press

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R H LANE et al

small clusters of neurons to the locations of the corresponding recording sites The procedure in general was similar to that used by others in determining the represenshytation of the visual field in the superior colliculus32 and lateral geniculate28 of the rat

Animal preparation

The results were obtained from 12 grey squirrels (Sciurus carolinensis) and 4 tree shrews (Tupaia gUs) Each animal was anesthetized with urethane (125 mg 100 g body wt) fitted with a tracheal cannula and placed in a headholder with minimal obstruction of the visual field The lids of both eyes were removed and the right eye was fixed by suturing the sclera to a metal ring anchored to the headholder The pupils were dilated with 20 cycJopentolate hydrochloride and the corneal surface was protected with a thin layer of silicone fluid The occipital cortex of both cerebral hemispheres was exposed the dura removed and the brain surface protected by mineral oil retained in a chamber of acrylic plastic Stimuli were presented on a translucent plastic hemisphere which corresponded to the visual field of one eye The right eye was centered in the hemisphere equidistant from all points on the surface and the plane of the open side of the hemisphere was aligned with the plane of the corneal limbus of the eye

Stimuli

Receptive field boundaries were defined as the margins of the area in which visual stimuli produced an increase in the activity of the recorded neurons The usual stimulus was a narrow slit of light 5 in length projected on the surface of the plastic hemisphere in a dimly lit room and moved repeatedly through the visual field from a number of intersecting directions The boundaries of most receptive fields were checked with small moving shadows produced by backlighting small targets

Recording

Tungsten micro electrodes were used with a tip exposure of 5 pm or more so that the activity of a number of neurons was usually recorded and single neurons usually were not isolated The superior colliculus was approached by penetrating with microshyelectrodes from the dorsal surface of the brain through the cortex to the tectum below Recording depths were noted and microlesions were made (20-30 pA for 10 sec) to mark depths in the electrode tracts The recording sites were later identified in frozen or paraffin-embedded brain sections cut in the coronal plane parallel to the electrode penetrations and stained with cresyl violet for cells The superior collicshyulus was reconstructed from the serial sections and the recording sites were indicated on the reconstruction

Estimating the projection of the line of decussation of the retina

The portion of retina projecting to striate cortex of the ipsilateral hemisphere


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DISCUSSION




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SUMMARY


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REFERENCES




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SUMMARY


ACKNOWLEDGEMENTS



REFERENCES




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SUMMARY


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REFERENCES




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DISCUSSION




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SUMMARY


ACKNOWLEDGEMENTS



REFERENCES




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DISCUSSION




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288 R H LANE et al







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SUMMARY


ACKNOWLEDGEMENTS



REFERENCES




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2

2

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2 2

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DISCUSSION




1

288 R H LANE et al







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SUMMARY


ACKNOWLEDGEMENTS



REFERENCES




)

2

2

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DISCUSSION




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288 R H LANE et al







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SUMMARY


ACKNOWLEDGEMENTS



REFERENCES




)

2

2

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2

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DISCUSSION




1

288 R H LANE et al







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289

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Campbell et al 4

Laemle24

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SUMMARY


ACKNOWLEDGEMENTS



REFERENCES




)

2

2

2

2

2 2

2 2

2

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5

10

15

20

25

30

291



























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DISCUSSION




1

288 R H LANE et al







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289

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Campbell et al 4

Laemle24

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SUMMARY


ACKNOWLEDGEMENTS



REFERENCES




)

2

2

2

2

2 2

2 2

2

t

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5

10

15

20

25

30

291



























292 R H LANE et al











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DISCUSSION




1

288 R H LANE et al







1 l l I

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289

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Tigges39

Campbell et al 4

Laemle24

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SUMMARY


ACKNOWLEDGEMENTS



REFERENCES




)

2

2

2

2

2 2

2 2

2

t

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5

10

15

20

25

30

291



























292 R H LANE et al











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288 R H LANE et al







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289

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Tigges39

Campbell et al 4

Laemle24

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and rat15 26





SUMMARY


ACKNOWLEDGEMENTS



REFERENCES




)

2

2

2

2

2 2

2 2

2

t

~

5

10

15

20

25

30

291



























292 R H LANE et al











B

5 (

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289

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Tigges39

Campbell et al 4

Laemle24

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SUMMARY


ACKNOWLEDGEMENTS



REFERENCES




)

2

2

2

2

2 2

2 2

2

t

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5

10

15

20

25

30

291



























292 R H LANE et al











B

5 (

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SUMMARY


ACKNOWLEDGEMENTS



REFERENCES




)

2

2

2

2

2 2

2 2

2

t

~

5

10

15

20

25

30

291



























292 R H LANE et al











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291



























292 R H LANE et al











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292 R H LANE et al











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Documents

REPRESENTATION OF THE VISUAL FIELD IN THE … of the visual field in the superior i . ... visual field representation in superior colllculus 279 . i . i . i . ... planes. t . f