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The Role of the Superior Colliculus in Visually Guided Locomotion and Visual Orienting in the Hamster

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The Role of the Superior Colliculus in Visually Guided Locomotion and Visual Orienting in the Hamster Physiological Psychology 1980, Vol. 8 (1),20·28 The role of the superior colliculus in visually guided locomotion and visual orienting in the hamster ELIZABETH MORT, SARA CAIRNS, HELEN HERSCH, and BARBARA FINLAY Cornell University, Ithaca, New York 14853 Visually guided locomotion toward goal doors designated by various cues was assessed in normal hamsters, hamsters with undercuts of the superior colliculus, and hamsters with neonatal lesions of the superior colliculus. Scanning of visual arrays, orientation to novel stimuli, and orientation to sunflower seeds were assessed in the same animals. Collicular lesions produced no deficit in accuracy of choice of goal door, type of route taken, or speed of locomotion. By contrast, the same hamsters showed major deficits in spontaneous scan· ning and orientation to stimuli in the visual periphery. Hamsters with neonatal and adult collicular lesions performed identically on every task except orientation to sunflower seeds presented at various locations in the visual field; adult operates were somewhat more vari· able in their performance. The implications of these results for the concept of encephalization of function and the phylogeny of the optic tectum are discussed. In every vertebrate that has been studied, the mid­ 1969, 1970) has shown a deficit both in visu1ll orienting, brain tectum plays some role in visuomotor behavior as measured by head turns to sunflower seeds, and in (Ingle & Sprague, 1975). In highly visual animals visually guided locomotion consequent to a collicular with marked retinal specializations for pattern vision, undercut, and has characterized these symtoms as the superior colliculus has been implicated in acqui­ indicative of a general disability in spatial localization, sition of visual targets, particularly peripheral ones knowing where things are. In the rat, Dyer, Marino, (Butter, Weinstein, Bender, & Gross, 1978; Keating, Johnson, and Kruggel (1976) and Goodale and 1974) mediating movement of the fovea or area Murison (1975) find no evidence of such a general centralis to a target. In nonmammalian predatory deficit in spatial localization consequent to tectal species both with and without retinal specializations ablation, finding only a disability in attention and (Ewert, 1970; Ingle, 1973), the tectum has been im­ the "orienting reflex," defined as cessation of loco­ plicated principally in prey acquisition, mediating a motion, rearing, and head turning toward a novel ballistic movement of body midline and mouth to a stimulus. Since these studies differ on at least three prey object. In addition, the tectum has also been important dimensions-type of lesion, species of ani­ implicated in a variety of other visual functions, mal, and behavioral assessment-accounting for the including optomotor responses (Springer, Easter, difference has been problematic. & Agranoff, 1977), visually guided locomotion In this study, we have undertaken to replicate the (Schneider, 1969), and pattern vision (Casagrande & experimental paradigm of Goodale and Murison & Diamond, 1947). Construction of the phylogeny of (1975), in which animals must locate and find their the optic tectum requires understanding of these way to a goal door designated by brightness in an divergences in tectal function as well as commonalities array of doors, using hamsters in which the colliculi in species with diverse visuomotor behavior. had been undercut by the method of Schneider (1969). Foraging animals without marked retinal special­ Particular attention was paid to the way the animals izations, such as rodents and herbivores, would add learned and performed the task, using videotape anal­ an interesting piece of information to understanding ysis. In addition, the orienting capacities of these of tectal evolution, and some information has been same animals to novel stimuli and sunflower seeds gathered. However, a coherent account of tectal were studied. function in rodents has been unavailable, due to the Schneider has also presented evidence that hamsters conflicting reports of the visuomotor deficit produced given collicular ablations on the day of birth do not by collicular lesions. In the hamster, Schneider (1967, show as profound a deficit in general visuomotor ca­ pacity as do animals receiving collicular undercuts This work was supported by NSF Grant BNS 77·077066 AO!. at maturity (1970). We have assessed a group of ani­ Requests for reprints should be sent to B. Finlay, Department of mals receiving collicular ablations at birth on the Psychology, Cornell University, Ithaca, New York 14853. various visuomotor tasks described above, with par- Copyright 1980 Psychonomic Society, Inc. 20 0090·5046/80/010020-09$01.15/0 ROLE OF THE SUPERIOR COLLICULUS 21 ticular attention to whether classes of visuomotor be­ r------------------- :~ ------------------~ havior may be dissociated by their differential impair­ T ment or sparing with adult vs. neonatal lesions. 12 A preliminary report has been published (Finlay, em Mort, Berg, Hersch, & Falino, 1979). )-~~1 ------~----- -----~------ METHODS Subjects Twenty golden hamsters of both sexes were used in this study; in any testing situation, males and females were run in separate but identical apparatus to minimize olfactory distractions. Ani­ mals were housed in individual clear plastic cages with pine bedding and hamster chow available ad lib. During testing, the animals were maintained on a 24-h water-deprivation schedule. Of the 20 animals, 6 normal animals were trained to criterion on a brightness discrimination problem, whereupon 3 received collicular undercuts and 3 had sham operations. Another 12 animals were run as normal/neonatal operate pairs. Each pair received identical handling, and the experimenter was not aware which animal was normal and which was the neonatal operate. When both members of the pair reached criterion, they were Figure 1. Overhead view of apparatus design used to train and identified, and the normal animal then received a collicular under­ test a\l subjects. The arena was uncovered, whereas the start­ cut. These animals were also assessed for distractibility and orienta­ box was enclosed. The three lines (not present In the actual box) tion to sunflower seeds. represent direct approach routes to the open doors. Each door The remaining two normal animals were trained to do a pattern was 8 x 8 cm and directly beneath an indicator light. Removable discrimination and then were given collicular undercuts. The visual clear plastic doors were used to cover incorrect doors. The orienting capacities of these two animals were assessed in detail water reward was behind each door at all times. by videotape analysis. Surgery access to two drops of water on a glass slide behind the goal Neonatal collicular lesions were performed in the manner opening and a lO-sec reinforcement period; incorrect choices described by Schneider (1970). Within 24 h of birth, a litter of resulted in a firm nose bump against the clear plastic barrier to hamsters was removed from the mother and cooled to provide the two other openings and termination of the trial. Water was anesthesia and reduce mobility. A slit was made in the scalp always present behind all three doors. The position of the illu­ overlying the colliculi, which are visible through the cartilagenous minated door was changed in a pseudorandom sequence so that cranium and whose boundaries are marked by the transverse no door was designated correct for more than three consecutive sinuses and the occipitointerparietal suture. The colliculi were trials. Each animal was run through 30 trials a day for 5 days destroyed by heat lesion directly through the cranium, using an a week until a criterion of 800/0 correct choices was achieved. appropriately shaped heated wire. The scalp incision was then For each trial during training the following were recorded: closed with one or two sutures. Upon completion of surgery, the time to door (from when the hamster's rear legs left the startbox animals were returned to the mother and allowed to mature to the time its vibrissae touched the plastic of the incorrect door normally. or its head entered the correct opening), method of approach In adult hamsters, the superior colliculi were undercut stereo­ (classified as "direct," "edge" if by way of the box perimeter, taxically by the method described by Schneider (1967). The or "indirect"), scanning (as defined by the hamster directing animals were anesthetized with thiopental (Nembutal, .08 mg/l00 g). its nose toward at least two different openings, before traveling A slit, 7 mm wide, was made in the cranium 1.8 mm posterior more than one body-length from the start box), and door of choice. to the lambda point. Into this slit, a specially formed scapel A choice was judged incorrect and the trial terminated if the blade was introduced at an angle 55 deg from the vertical, and animal came within vibrassae-Iength of the incorrect doors. A drawn back and forth to undercut the superior colliculi bilaterally. quantitative analysis of these same parameters was made from the Sham operations were identical, but without the scalpel insertion. videotapes of criterion and postlesion runs. All results presented for time to door, approach, path length, and scanning during Apparatus and Training Procedures for the Brightness training were taken from the 12 normal/neonatal operate pairs. and Pattern Discrimination The data from the remaining three adult operates and three sham The apparatus, shown in top view in Figure 1, consisted of an operates were added only to the results for scanning at criterion open box with a floor space of 45 x 90 em with walls 28 cm high. and accuracy of the postoperative brightness discrimination. The floor and three walls were painted white. Three 8 x 8 cm Since two possible cues to correct door were available-the retangular openings were evenly spaced, 30 em apart, on the indicator light and the clear plastic barriers on the incorrect fourth wall; this wall was painted black. An indicator light doors-animals that had reached criterion were run on 2 separate (Sylvania No.
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