Functional roles of the lateral suprasylvian cortex in ocular near response in the cat

162

Neuroscience Re~earch, t5 (1992) 162-178 ~t~ 1992 Elsevier Science Publishers Ireland, Ltd. All rights reserved (1168-0102/92/$05.1)11

N E U R E S 00558

Review article

Functional roles of the lateral suprasylvian cortex in ocular near response in the cat T. Bando, M. Takagi, H. Toda and T. Yoshizawa Department of Physiology, Niigata Unit,ersity School of Medicine, Asahi-Machi l, Niigata, Nt)gata 951, Japan (Received 23 July 199t; revised 21 May 1992; accepted 28 July 1992)

Key words: Extrastriate cortex; Visual cortical area; Eye movement; Ocular near response; Lens accommodation; Vergence eye movement; Cat; Pupillary constriction

Summary The lateral suprasylvian (LS) area, an extrastriate visual area in the cat, has been suggested to play an important role in processing motion in 3-dimensional visual space. In addition, the LS area is related to all three components of the ocular near response, i.e. lens accommodation, pupiltary constriction, and ocular convergence: microstimulation in this area evoked these intra- and extraocular movements, and neuronal discharges associated with these movements were also found. Anatomical pathways, direct and indirect, from this area to premotor nuclei in the brainstem are known to exist. The present p a p e r reviews studies useful for assessing the functional roles played by the LS area in triggering and modulating component movements in the ocular near response.

Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Retinotopical organization in the LS area . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Visual properties of LS neurons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. General properties . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Visual properties of the LS area related to either lens accommodation or ocular convergence . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Afferent and efferent fiber connections of the LS area . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. I. Cortico-cortical and thalamo-cortical connections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Efferent connections to the brainstem nuclei . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Efferent connection with the striatum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4. Connection with the cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Effect of lesion in the LS area on visual and oculomotor functions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Changes in orientation behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Changes in eye movement or eye movement-related neuronal activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Correspondence to: Dr. T. Bando, Department of Physiology, Niigata University School of Medicine, Asahi-Machi 1, Niigata, Niigata 951, Japan

163 164 164 164 164 165 165 166 166 166 166 16h 1()7

Abbreciations: ALLS, antero-lateral lateral suprasylvian area; AMLS, antero-medial lateral suprasylvian area; PLLS, postero-lateral lateral suprasylvian area; PMLS, postero-medial lateral suprasylvian area; DLS, dorsal lateral suprasylvian area; VLS, ventral lateral suprasylvian area; LP, lateral posterior nucleus of the thalamus; LPI, lateral division of the lateral posterior nucleus; LPm, medial division of the lateral posterior nucleus; LS area, lateral suprasylvian area; MSS, middle suprasylvian sulcus; PSS, posterior suprasylvian sulcus: PT, pretectum; SC, superior colliculus.

163 6. Lens accommodation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1. Unit activities related to lens accommodation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2. Possible efferent pathways responsible for lens accommodation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.3. The cerebellum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.4. Time spent in the efferent pathway . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7. Vergence eye movement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1. Effect of microstimulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2. Unit activities related to ocular convergence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.3. Relation of evoked lens accommodationand vergence eye movement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8. Pupillary constriction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.1. Effect of microstimulation and unit activities related to pupillary movement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.2. Possible output pathway from cortical pupillo-constrictorarea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.3. Projection from pupillo-constrictor region to lens accommodation-relatedregion:intracortical fiber connections . . . . . . . . . . . . . 9. Possible functions of the LS area in relation to component movementsof the near response . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.1. Expected roles of the LS area related to oculomotorresponses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.2. Differencesin oculomotorresponses among different parts of the LS area: representations of central vs. peripheral visual field . . 9.3. Possible candidates of the central correlate for ocular near response . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10. Concludingremarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I. Introduction Ocular convergence, lens accommodation and pupillary constriction form the triad of the ocular near response, which provides a single and clear retinal image, and builds an essential basis for fine vision (Alpern, 1969). It has been suggested that the visual cortex plays an important role in the ocular near response (for example, Campbell and Westheimer, 1959), a suggestion supported by some circumstantial evidence: (1) the near response is elicited when a visual target approaches the observer. A m o n g visual cues accompanied by motion in depth, binocular disparity, changes in size of the target, and retinal blur provide important cues for triggering the near response (Fincham, 1951; Campbell and Westheimer, 1959, 1960; Stark, 1965; Kruger and Pola, 1987). It is known that these cue signals are extracted by early visual processing in the cerebral cortex both in the cat and the monkey: neuronal activities sensitive to binocular disparity or changes in it are recorded in areas 17 and 18 (Poggio and Fischer, 1977; Cynader and Regan, 1978; Regan et al., 1979; Poggio and Talbot, 1981; Ferster, 1981; Regan and Cynader, 1982) and the lateral suprasylvian (LS) area (Toyama et al., 1986a, 1986b). (2) When movement of a target was periodic, ocular convergence and lens accommodation often showed a smaller phase lag or even a phase lead.(Zuber, 1971; Kruger and Pola, 1987) These predictive features are not specific but are common to cerebral function. (3) Jampel (1960) elicited all three components of the near response by stimulating the surface of the parieto-oc-

167 167 167 168 168 168 168 169 170 170 170 170 171 172 172 173 173 174 174

cipital cortex surrounding the superior temporal sulcus (STS) in the monkey, although the localization of the responsible region was not known. Recently, several higher-order visual areas were discovered in and around the STS, including the middle temporal (MT) and medial superior temporal (MST) areas (Zeki, 1974; Maunsell and Van Essen, 1983a; Saito et al., 1986; Tanaka et al., 1986; Desimone and Ungerleider, 1986; Tanaka and Saito, 1989). Furthermore, non-visual neurons, whose activities were related to the velocities of either lens accommodation or vergence eye movement, were also found in the medial bank of the STS and in the lateral bank of the intraparietal sulcus adjacent to the STS (Gnadt and Mays, 1989). The lateral suprasylvian (LS) area in the parieto-occipital cortex of the cat is an extrastriate visual area (Van Essen, 1979; Spear, 1991), which has visual properties analogous to the higher-order visual areas surrounding the STS in the monkey (Zeki, 1974). Neurons in both the M T / M S T , and the LS areas have rather large receptive fields, prefer moving stimuli with direction selectivity, and are binocularly activated. Some of them are sensitive to movement of a target in depth. It has been suggested that these areas play a role in analyzing relative motion between an object and an observer in the visual space (Spear and Baumann, 1975; Camarda and Rizzolatti, 1976; Maunsell and Van Essen, 1983b; Saito et al., 1986; Toyama et al., 1986a; Rauschecker et al., 1987; Di~rsteler and Wurtz, 1988). Each of the three components of the ocular near response could be elicited by intracortical microstimulation of the LS area (Bando et al., 1984b; Bando,

164 1985; Toda et al., 1991a). Neuronal activities of some LS neurons were also accompanied by either spontaneously occurring lens accommodation or pupillary constriction (Bando et al., 1984b, 1988). Neurons which discharged in correlation with the peak velocity of ocular convergence were also found in this area (Toda et aI., 1991b). It is also noted that cats are capable of lens accommodation and vergence eye movement (Elur and Marchiafava, 1964; Hughes, 1972; Stryker and Blakemore, 1972). This knowledge favors the concept (Bando and Toda, 1991; Bando et al., 1991) that the LS area contributes to visuomotor integration in each of the component movements of the near response, and possibly plays a role in composing the link between them. In this paper, we review the physiological and anatomical bases useful in assessing the roles of the LS area in controlling and modulating these intra- and extraocular movements.

2. Retinotopical organization in the LS area

The LS area was divided into 6 subareas (Palmer et al., 1978; Van Essen, 1979), each of which had a retinotopic map of the contralateral hemifield. The rostral two subareas (antero-medial and antero-lateral lateral suprasylvian areas, AMLS and ALLS) are located in the medial and lateral banks of the rostral one third of the middle suprasylvian sulcus (MSS, see Fig. 6, inset), respectively. The middle two subareas (postero-medial and postero-lateral lateral suprasylvian areas, PMLS and PLLS) are located in the medial and lateral banks of the caudal two-thirds of the MSS, respectively. The posterior two subareas (dorsal and ventral lateral suprasylvian areas, DLS and VLS) are in the dorsal and ventral banks of the posterior suprasylvian sulcus (PSS, see Fig. 6, inset). Because the knowledge related to intra- and extraocular movements is limited to the middle subareas (PMLS and PLLS areas), we will concentrate on them in this paper. In the PMLS and PLLS, the visual field along the horizontal meridian is represented in the fundus of the sulcus, while the peripheral part of the lower contralateral quadrant is represented in the upper parts of the medial and lateral banks of the MSS. The vertical meridian is represented rostrally in the border between the rostral (AMLS and ALLS areas) and middle (PMLS and PLLS areas) subareas, including the central visual field. The central visual field is again represented in the caudal extremes of the PMLS and PLLS areas.

Therefore two representation of the central visual field are found in the middle subareas of the LS area: in the rostral and caudal extremes (see Fig. 3). Later studies (Spear and Baumann, 1975; Zumbroich et al., 1986; Rauschecker et al., 1987) revealed that the LS area is not as symmetrically and systematically organized as initially proposed. However, we refer to the original retinotopic map because the overall topographic order is still found reasonably well in the middle subareas.

3. Visual properties of LS neurons

3.1. General properties The visual properties of LS neurons have been well studied by presenting spots or bars of light or drifting sine-wave gratings (Hubel and Wiesel, 1969; Spear and Baumann, 1975; Camarda and Rizzolatti, 1976; Di Stefano et al., 1985; Morrone et al., 1986; Zumbroich et al., 1986; von Grfinau et al., 1987; Blakemore and Zumbroich, 1987; Zumbroich and Blakemore, 1987: Guido et al., 1990). LS neurons have rather large receptive fields (mean 154 deg: in the PMLS, and 442 deg 2 in the PLLS), which are similar in nature to the complex cells of area 17. The size of the receptive field is smaller in the central/paracentral visual field than in the peripheral visual field. The optimal spatial frequencies of both PMLS- and PLLS-neurons are lower than those found in area 17, when drifting sine-wave gratings were presented. Most LS neurons (80-90%) respond maximally to a spot of light moving in the fronto-parallel plane a n d / o r in depth with a single preferred direction (Hubel and Wiesel, 1969; Spear and Baumann, 1975; Camarda and Rizzolatti, 1976; von Griinau et al., 1987). Although a considerable number of these neurons (40% in the PMLS area, 15% in the PLLS area) could also respond to stationary flashing spots or bars, only 5% of LS neurons preferred stationary flashing stimuli to moving ones (Spear and Baumann, 1975; Blakemore and Zumbroich, 1987; Zumbroich and Blakemore, 1987). Velocity tuning of each LS neuron is broad (from 5 to even 200 deg/s): the optimal speeds are 15-20 d e g / s in the PMLS area, but higher than 20 d e g / s in the PLLS and AMLS areas (Spear and Baumann, 1975; Camarda and Rizzolatti, 1976; von Griinau et al., 1987; Toyama et al., 1990). The majority of them (65-80%) are activated both binocularly and monocularly, especially in the

165 central representation of the visual field (Hubel and Wiesel, 1969; Spear and Baumann, 1975; Toyama et al., 1986b; von Griinau et al., 1987; Blakemore and Zumbroich, 1987; Zumbroich and Blakemore, 1987). Binocular interactions occur within a few degrees around zero positional disparity (Toyama et al., 1986b). 3.2. Visual properties o f the L S area related to either lens accommodation or ocular convergence

A sharp retinal image is maintained by lens accommodation under feedback control which keeps the retinal blur to a minimum (Stark, 1965). Vergence eye movement is triggered by binocular disparity; single vision is maintained by feedback control which keeps binocular disparity to a minimum (Zuber, 1971). Change in target size is another important visual cue of lens accommodation and ocular convergence (Fincham, 1951; Erkelens and Regan, 1986; Kruger and Pola, 1987). These visual cues are accompanied by changes in distance between the observer and a visual target, and are analyzed in the early stages of processing in visual cortical areas (Regan et al., 1979; Poggio and Poggio, 1984). Of these cortical visual areas, the LS area is thought to analyze motion in a 3-dimensional (3-D) visual space, and to contribute to the assessment of changes in the spatial relationship between the observer and the visual environment. A population of LS neurons responded selectively to a particular motion in depth (Toyama and Kozasa, 1982; Toyama et al., 1986b): (1) AP cells (30% of 369 cells tested) responded selectively to a target approaching the animal. Correspondingly they responded selectively to divergent movement of the retinal images in both eyes which were presented using a pair of Risley prisms; (2) RC cells (10%) responded selectively to movement away from the animal, and to convergent movement of the retinal images in both eyes. Both AP and RC cells were sensitive to motion disparities rather than positional disparities. Other LS neurons (20%) responded both to a motion in depth and to a motion in a fronto-parallel plane. In another study, changes in target size activated about half of the 118 LS neurons tested, independently of the initial size of the stimulus (Toyama et al., 1986a). The majority of them responded to both changes in size of the target and changes in motion disparity, and were activated maximally to the combination of two cues (Toyama et al. 1990).

4. Afferent and efferent fiber connections of the LS area 4.1. Cortico-cortical and thalamo-cortical connections

Three input pathways from the retina to the LS area are known: retino-geniculo-cortico-cortical, retinothalamo-cortical and retino-tecto-thalamo-cortical pathways: (1) the LS area is connected bilaterally with areas 17, 18 and 19 (Heath and Jones, 1971; Shoumura, 1972; Kawamura, 1973; Kawamura et al., 1974; Symonds and Rosenquist, 1984; Sherk, 1986; Lowenstein and Somogyi, 1991), which receive retinal inputs through the lateral geniculate nucleus (LGN). (2) The LS area (except areas AMLS and ALLS) is also connected directly with the parvocellular C-layer of the LGN and the medial interlaminar nucleus (MIN), both of which receive direct retinal inputs (Heath and Jones, 1971; Rosenquist et al., 1974; LeVay and Gilbert, 1976; Raczkowski and Rosenquist, 1980; Tong, et al., 1982, Sherk, 1986). (3) The retina projects to the LS area through the superficial layers of the superior colliculus (SC), and then the medial division of the lateral posterior nucleus (LP) of the thalamus (LPm). The LP connected strongly with the PLLS, and weakly with the PMLS. The PMLS area is also strongly connected to the lateral division of the LP (LP1) and the posterior nucleus of the thalamus, and weakly with the pulvinar (Graybiel, 1972; Kawamura et al., 1974; Updyke, 1981; Raczkowski and Rosenquist, 1983). The LS area is not only connected reciprocally with cortical visual areas, but also indirectly via the visual thalamus (Fig. 1). In addition to visual inputs, LS neurons are activated by a stretch of extraocular muscles (Donaldson, 1979). The afferent pathway, however, is not known. Extrastriate Cort,cal A. . . .

LP

/

CerebeHum ,~

~ . ~ ~ Port; ~

Brainstem

~

Eye

propriocept ire Fig. 1. Schematic diagram of inputs and outputs of the postero-medial and antero-medial lateral suprasy]vian area (PMLS and A M L S areas). LP, lateral posterior nucleus of the thalamus. See text for details.

166 4.2. Efferent connections to the brainstem nuclei

4.4. Connection with the cerebellum

Cortico-tectal projections of the LS area are mostly ipsilateral (Garey et al., 1968; Kawamura et al., 1974; Cohen et al., 1981; Ogasawara et al., 1984). Cells of origin of the crossed corticotectal pathway are, however, also found especially in the lateral bank of the MSS (ALLS and PLLS areas) (Baleydier et al., 1983; Segal and Beckstead, 1984). All six subareas project to both superficial and deep layers of the SC, the strength of the connection varying (Berson and McIlwain, 1983; Berson, 1985). Subareas in the medial bank of the MSS (PMLS and AMLS areas), and those along the PSS (DLS and VLS areas) have more connections with the superficial layers of the SC, while those in the lateral bank (PLLS and ALLS areas) project more to the deep layers (Segal and Beckstead, 1984). Both the PMLS and AMLS areas project to the nuclei of the pretectum (PT): the anterior and posterior pretectal nuclei (NPA and NPP) and the nucleus of the optic tract (NOT). The projection to the NPA is strongest (Kawamura et al., 1974; Hutchins et al., 1983). Both subareas also project to another pretectal nucleus, the pretectal olivary nucleus (OPN) (Hutchins et al., 1983). The N O T and OPN are related to pupillary light reflex (Trejo and Cicerone, 1984; Clarke and Ikeda, 1985), and the NOT, also to the optokinetic nystagmus (Hoffmann and Schoppmann, 1981; Maekawa and Kimura, 1981; Clement and Magnin, 1984; Simpson et al., 1988). Subareas in the lateral bank of the MSS (areas PLLS and ALLS) project weakly to the NPA, NPP and NOT. The AMLS and PMLS areas also project to all three nuclei of the accessory optic system (AOS), i.e., the medial, lateral and dorsal terminal accessory nuclei (MTN, LTN and DTN) (Berson and Graybiel, 1980; Marcotte and Updyke, 1982), while the PLLS area projects to only one of them, the LTN. The AOS is related to the horizontal optokinetic nystagmus and also to the vestibulo-ocular reflex (Simpson, 1988).

The cerebellum receives inputs from the LS area via the rostral pontine nuclei (Baker et al., 1976; Albus et al., 1981; Cohen et al., 1981; Robinson et al., 1984; Bjaalie, 1986; Kato et al., 1988), and projects back to the rostral LS area (the AMES and probably the rostral PMLS) through the thalamus (Kato et al., 1987). Many of cortico-pontine neurons (70%) are activated antidromically not only from the rostral pons but also from the SC, i.e., they send collaterals both to thc pontine nuclei and the SC (Baker et al., 1983). Cortico-pontine neurons are found predominantly in the medial bank of the rostral half of the MSS: the AMLS and the rostral PMLS (Bjaalie, 1986). Smaller numbers of cortico-pontine ceils are found in the ALES and PLLS areas.

No prominent deficit in the static pattern or form discrimination was found when the LS area alone was removed (Hara et al., 1974; Wood et al., 1974; Sprague et al., 1977; Pitto and Lepre, 1983), although combined lesions with other visual cortical areas revealed severe deficits in discrimination tasks (Baumann and Spear, 1977). On the other hand, discrimination of the difference in speed of drifting gratings of low contrasts was impaired especially at high spatio-temporal frequencies in cats with bilateral lesions in the LS area (PMLS, PLLS and a part of AMLS, ALLS, VLS and DLS) (Pasternak et al., 1989), in agreement with dynamic visual properties of LS neurons. Deficits in visuo-motor behavior or eye movement were observed after the lesion in the LS area as described below. These results suggest that the LS area may also provide spatio-temporal visual information to perform eye (and probably head) movements properly.

4.3. Efferent connection with the striatum

5.1. Changes in orientation behat'ior

Direct projections from the LS area to the striatum (caudal parts of the head of the caudate nucleus and the putamen) are also known (Norita et al., 1991). Cells of origin of these projections are much more concentrated in the PLLS than in the PMLS. Because the striatum projects through the substantia nigra to the deep layers of the SC, the lateral bank of the MSS projects to the deep layers of the SC both directly, and indirectly via the striatum and the substantia nigra.

Impairment of a visually-guided behavior was observed after the lesion of the middle and posterior subareas of the LS area (PMLS, PLLS, VLS and DLS) (Hardy and Stein, 1988). In this task, cats were initially held by an experimenter while they fixated the food in front of them. Simultaneously with their release, a white ball was introduced from the side. They had to orient the head and eyes quickly to the ball, and move towards it. The deficit was only revealed when the ball

5. Effect o f lesion in the LS area on v i s u a l and oculomotor functions

167 was presented into the visual field contralateral to the side of the lesion. Visual neglect in the contralateral visual field was also found during an orientation and discrimination task after unilateral ablation of the lateral bank of the MSS (Naito and Sasaki, 1991). In this task, cats first fixated the center of a perimeter. They then discriminated two model objects presented in a wide window in the front panel, and shifted the gaze to one of them. No comparable deficit was found after the lesions in areas 17 and 18, or after unilateral ablation of the frontal eye field (Itouji and Naito, 1990). These tasks differ in many aspects, but common features are the initial fixation of a target followed by an abrupt shift of the gaze (by eye and head movements) to a new object in the contralateral visual field. 5.2. Changes in eye movement or eye movement-related neuronal activities Eye velocities in the slow-phase of the optokinetic nystagmus (OKN) were reduced by lesioning areas PMLS, AMLS, VLS and 21 unilaterally (Tusa et al., 1989). After the lesion, the slow-phase peak velocities toward the side of the lesion decreased: the gain of the OKN (eye velocity/drum velocity) decreased at all drum speeds, and upper limits of retinal-slip velocities which could activate the OKN were also lowered. No comparable change was observed by lesioning areas 17 and 18, although similar changes were found by the combination of lesions in areas 17 and 18 and the corpus callosum. The deficits were suggested to be caused by a loss of cortical influence on the brainstem nuclei, e.g. the nuclei of the accessory optic system (AOS). The projections from the PMLS as well as area 21 to the AOS are known (Marcotte and Updyke, 1982). A change in saccadic-excitation of neurons in the striate cortex is also found by the LS lesion. A group of LS neurons were excited in association with saccadic eye movement either during whole-field stimulation (Komatsu et al., 1983) or following spontaneous or vestibular-induced horizontal saccades in total darkness (Kennedy and Magnin, 1977). Similar saccade-excitation was also found in the striate cortex (Kimura et al., 1980; Toyama et al., 1984a). By lesioning the ipsilateral medial bank of the MSS (areas A M L S / P M L S ) , saccade-excitation in the striate cortex in the dark disappeared (Toyama et al., 1984b). On the other hand, even when eye movement was eliminated by retrobulbar paralysis, saccade-excitation in the striate cortex survived. Based on these results, it was suggested that

the LS area transferred "the efference copy of the oculomotor command signal (Guthrie, 1983)" to the striate cortex.

6. Lens accommodation

6.1. Unit activities related to lens accommodation A group of LS neurons (27% of 180 units sampled, ac-units) discharged in the dark before the onset of spontaneously occurring lens accommodation in cats under chloralose/urethane anesthesia and with immobilization (Bando et al., 1981b; Bando et al., 1984b). Dioptric power of the eye was monitored using an infrared high-speed optometer (Campbell and Robson, 1959). Modulation of discharges preceded the onset of lens accommodation by an average of 360 ms. This lead was likely to be spent mostly in the peripheral structures (muscular contraction and deformation of the lens), because lens accommodation was evoked with an average latency of 240 ms by stimulating either preganglionic fibers to the ciliary ganglion, or the parasympathetic oculomotor nucleus (Bando et al., 1981a; Bando et al., 1984a). In a preliminary study, neuronal activities 0.7 s before the onset of spontaneous lens accommodation in darkness were correlated with the maximum rate of rise of lens accommodation in 9 out of 15 ac-units tested (Bando and Toda, 1989a). These ac-units responded to changes in size of a visual target (Bando and Toda, 1989b). In addition, dioptric power of the eye increased by microstimulation at the recording sites of ac-units (with a train of 30 bipolar pulses; intensity, 50-100 ~ A ) (Bando et al., 1984b). The acunits were located mostly in the PMLS area but a minority was found in the PLLS area. 6.2. Possible efferent pathways responsible for lens accommodation About 70% of PMLS ac-units were antidromically activated through electrodes placed in the pretectum (PT) a n d / o r the superior colliculus (SC) with average latencies of 2.4-2.5 ms (Bando et al., 1984b). More than half (65%) of them were also activated by stimulation through electrodes placed in the posterior lateral nucleus of the thalamus (LP). It is, therefore, suggested that many ac-units send their axon collaterals both to the P T / S C and the LP, although this does not eliminate the possibility that the current which spread from the LP electrodes activated descending fibers from the PMLS area to the dorsal midbrain. Fiber projections

168 from the PMLS area to the LP, SC and PT are known anatomically, and the superficial layer of the SC projects to the PT (Kubota et al., 1989), which are connected with the parasympathetic oculomotor nucleus (Breen et al., 1983). In the brainstem of the cat, lens accommodation-related areas were mapped using microstimulation. Lens accommodation was indirectly assessed by monitoring the early potential of the short ciliary nerve (SCN), which innervated the ciliary muscle (Hultborn et al., 1978a). The early SCN potential was evoked with a latency of about 6 ms by stimulating the PT. Iris bulging due to lens accommodation was occasionally observed by stimulating the same part of the PT. It is likely, therefore, that the PT is a key structure which mediates the projection from PMLS ac-units to the parasympathetic oculomotor nucleus. Another possible relay neuron of cortical signals to parasympathetic oculomotor neurons is known in the mesencephalic reticular formation. In alert monkeys trained to fixate a target, mesencephalic reticular neurons were found which discharged in association with lens accommodation, ocular convergence, or both (Judge and Cumming, 1986; Mays, 1984). In cats, neurons which discharged before spontaneous lens accommodation in the dark were found in the mesencephalic reticular formation dorsotateral to the oculomotor nuclear complex (Bando et al., 1984a).

6.3. The cerebellum The cerebellum may play a role in the mediation of the information processed in the LS area to parasympathetic oculomotor neurons. By stimulating the cerebellar nuclei, lens accommodation was evoked which was monitored directly using an infrared high-speed optometer (Hosoba et al, 1978), or indirectly by assessing the early potential in the short ciliary nerve (Hultborn et al., 1978b). Stimulation of the fastigial and interpositus (IP) nuclei on either side was effective, but no response was evoked by stimulation of the lateral nucleus of the cerebellum. When IP-stimulation was preceded by paravermal (lobule VII) cortical stimulation, IP-evoked lens accommodation was depressed, suggesting that the cerebellar nuclear cells, and not cerebellar afferents, were stimulated. It is known that the IP projects to the parasympathetic oculomotor neurons with a short (mono- or disynaptic) latency (Hultborn et al., 1978b). Lens accommodation elicited by PMLS-stimulation did not change significantly, even after IP-induced lens accommodation was blocked by cooling the cerebellar

peduncles (Bando et al., 1984b). The cerebellum, therefore, is not likely to be a major mediator of the information from the LS area to the parasympathetic oculomotor neurons. However, the cerebro-cerebellar interaction may play an important role in controlling lens accommodation, because cerebro-ccrebellar projection through visual pontine nuclei, and back projection from the cerebellum to the LS area through the thalamus are known (Fig. 1).

6.4. Time spent in the efferent pathway Evoked electromyographic changes (EMGs) were recorded from both intraocular (ciliary and iris sphincter muscles) and extraocular muscles (bilateral medial rectus muscles) by stimulating the PMLS area in enc6phale-isol6 preparations (a train of 6 pulses; intensity, 200-300 /xA) (Hiraoka and Shimamura, 1989). The latencies of the EMGs were 20-30 ms in the ciliary and sphincter muscles, and about 20 ms in the medial rectus muscles. When the rostral part of the oculomotor nucleus was stimulated, the latencies of the EMGs recorded in the intraocular muscles were 5 - 6 ms. Therefore time spent in the brain was calculated as 15-25 ms. The central times so calculated were 10-20 ms longer than those estimated from the sum of the shortest latencies in the PMLS-PT-parasympathetic oculomotor pathway obtained in the electrophysiological experiments (about 5 ms) (Bando et al., t984b; Hultborn et al., 1978a). These extra delay times may be spent in synaptic transmission in the brainstem.

7. Vergence eye movement

7.1. Effect of microstimulation Slow disjunctive eye movement similar to ocular convergence was evoked by microstimulation in the LS area while monitoring eye movements using the magnetic search-coil method in chronically-operated alert cats (Toda et al., 1991a). Medial and lateral banks of the MSS (PMLS, PLLS, AMLS and ALLS areas) were mapped by stimulation using a tungsten-in-glass microelectrode. Disjunctive eye movements of 0.2 deg or larger (mean amplitude, 0.8 deg) were evoked by microstimulation with the threshold currents of 30-50 /~A (a train of 200 bipolar pulses) in the rostral parts of the P M L S / P L L S areas, and also in the caudal part of the PMLS area (Fig. 2). Distribution of effective sites roughly corresponded to the rostral and caudal representations of the central visual field in the standard

169 ocular convergence evoked by presenting a target moving in depth. However, the amplitude-velocity relationship of these two disjunctive eye movements closely resembled each other (Fig. 2) (Toda et al., 1991a). It is suggested that disjunctive eye movements evoked by intracortical microstimulation share parts of the neuronal circuitry responsible for ocular convergence.

retinotopic map (Palmer et al., 1978), in agreement with psychophysical studies in which slow ocular convergence was triggered only by visual stimuli presented in the central visual field (Semmlow and Tinor, 1978; Enright, 1986). Disjunctive eye movement was evoked independently of the eye position just before stimulation. The mean latency of evoked disjunctive eye movement was about 70 ms (SD, 50 ms, n = 53) in the caudal part of the PMLS and was longer (mean and SD, 310 + 160 ms, n = 92) in the rostral PMLS (Fig. 3). The minimal latencies of disjunctive eye movements evoked in the caudal part of the PMLS area were much shorter than the mean; they were as short as 20-30 ms, roughly comparable to the latency of the E M G in the medial rectus muscle evoked by PMLS stimulation. The amplitudes of disjunctive eye movements evoked by LS stimulation were much smaller than those of

7.2. Unit activities related to ocular convergence

A group of neurons which discharged in association with ocular convergence were also found in a preliminary study in alert cats, rewarded for ocular convergence (Toda et al., 1991b). Eye movement was monitored by the magnetic search-coil method, and unit activities were recorded through a chamber attached to the head at least one week prior to the first experiment. Disjunctive eye movement was evoked by microstimulation (less than 50 /xA, a train of 200 pulses) at

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170 the recording site. In 426 units isolated in the caudal part of the PMLS area, eight units increased their activities in correlation with the maximum velocities of ocular convergence. In most of them, the number of spike potentials in 200-ms bins started to increase one or two bins before the time at which the maximum velocity of ocular convergence was observed.

7.3. Relation of evoked lens accommodation and L~ergence eye mot~,ement Lens accommodation and vergence eye movement are closely linked with each other in the ocular near response (Alpern, 1969; Miles, 1985). It is, therefore, interesting to ascertain that these two ocular movements could be elicited independently. To perform this test, lens accommodation and eye movements were simultaneously monitored during intracortical microstimulation in the LS area (Toda et al., 1991a). Both responses were evoked by stimulation of many of the effective sites in the LS area, but in a few sites either lens accommodation or disjunctive eye movement could be evoked separately (Fig. 4). The latter result supports the notion that the LS area provides information for performing lens accommodation a n d / o r vergence eye movement rather than contributing to both of them together, for example, by forming a sensation of nearRcss.

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8.1. Effect of microstimulation and unit activities related to pupillary movement Pupillary constriction was evoked by stimulating the upper part of the medial bank of the MSS, an area representing the peripheral visual field (Bando, 1985). This pupillo-constrictor area extended 2-3 mm along the MSS. Some PMLS units (3% of 146 units sampled) discharged in association with spontaneous pupillary constriction but much less with lens accommodation under chloralose/urethane anesthesia and immobilization (Fig. 5B). Other types of PMLS units (13%) discharged prominently before spontaneous lens accommodation but not before pupillary constriction (Fig. 5A) (Bando et al., 1988). At the recording sites of the former neurons, pupillary constriction (and occasionally lens accommodation as well) was evoked by microstimulation. Lens accommodation alone was evoked at the recording sites of the latter neurons. Pupillary constriction is caused either by strong light stimuli (light reflex) or by approaching movement of a visual target (near reflex). It is known that pupillary light reflex is mediated by brainstem nuclei (Trejo and Cicerone, 1984), and that it is not changed by cortical lesion (Shoumura et al., 1984). On the other hand, pupillary near reflex has a latency which is 100 ms longer than that of pupillary light reflex, and comparable to that of lens accommodation (Campbell and Westheimer, 1960). It is then likely that the pupillary constriction elicited by PMLS stimulation is related to pupillary near reflex, a part of the ocular near response. 8.2. Possible output pathway from cortical pupillo-constrictor area

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For some time, people have been aware of the existence of a potent pupillo-constrictor area in the postero-lateral occipital cortex (Barris, 1936; Shoumura et al., 1982), an area corresponding to area 20 in the cat (Heath and Jones, 1971; Tusa and Palmer, 1980). By cooling the surface of the occipital cortex overlying area 20, pupillary constriction evoked by PMLS stimulation was reversibly reduced to about 50% of the original value (Bando, 1987). One of the probable hypotheses is that neurons in the PMLS pupillo-constrictor area project to area 20. It is also possible that background activity in the PMLS area, which might be maintained through the reciprocal connection with area

171 20, was reduced by cooling area 20. The former hypothesis was supported by an H R P study as follows. The projection from the PMLS pupilloconstrictor area to area 20 was tested by injecting W G A - H R P (wheatgerm agglutinin-conjugated horseradish peroxidase) into a part of area 20, from which pupillary constriction was evoked by microstimulation (Bando et al., 1989). Retrogradely labeled neurons were found in high density in the upper parts of the medial bank of the MSS, an area corresponding to the pupillo-constrictor area in the PMLS. The efferent from area 20 to the parasympathetic oculomotor nucleus is possibly mediated in the ventral nucleus of the lateral geniculate body (Shoumura et al., 1984). However, it is also possible that neural signals related to pupillary conA1

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8.3. Projection from pupillo-constrictor region to lens accommodation-related region: intracortical fiber connections The fiber connection between two regions, one related to lens accommodation and another related to pupillary constriction was studied (Yoshizawa et al., 1991) using an anatomical tracer, Phaseolus vulgaris leucoagglutinin (PHA-L). A tungsten-in-glass microC AI AZ,BI

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172 electrode was inserted into the medial bank of the MSS, and the site was sought at which lens accommodation was evoked by microstimulation. The electrode was then replaced by a glass pipette filled with PHA-L, and the tracer injected. Labeled fibers and terminal-like structures were found in the upper part of the medial bank of the MSS, an area corresponding to the pupillo-constrictor area (Fig. 6c). The labeled terminallike structures were also found in the fundus of the

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In lens accommodation and ocular convergence, the cue signals to trigger and modulate eye movements, i.e., binocular disparity and changes in target size, are processed in visual cortical areas including the LS area. Then the primary role of the LS area, in relation to component movements of the near response, may provide some (but probably not all) visual information to control lens accommodation and ocular convergence. The LS area may play a further role in providing optimal control of lens accommodation and ocular convergence. Both lens accommodation and ocular convergence rise rather rapidly in spite of their long delays. Therefore, depending on feedback-control alone, these movements may be unstable when the

173 target position is changed continuously and rapidly (O'Neill et al., 1969). It is, however, known that both movements are quite stable. It has been suggested, therefore, that the control system of lens accommodation and ocular convergence have both an open-loop fast component and a closed-loop slow component (Hung et al., 1986; Kruger and Pola, 1987; Semmlow et al., 1986). For example, lens accommodation with a phase lead was triggered by changes in target size alone, while that with a phase lag was triggered by retinal blur (Kruger and Pola, 1987). Because the size of the target is not changed significantly by lens accommodation itself, the system must be controlled in an open-loop condition by a central program in the former case. The LS area may contribute in manipulating these dual components and controlling them optimally, i.e., improving dynamic properties of the system without causing instability.

single slit to a large-field stimulus were also reported (Toyama et al., 1990). It was not known whether or not they were localized in parts of the LS area, which represented either central or peripheral visual fields. However, it is likely that different roles are played by different parts of the LS area. For example, both lens accommodation and disjunctive eye movement were evoked by microstimulation in the LS area which represented the central visual field (Toda et al., 1991a), while pupillary constriction was evoked by stimulation of another part of the LS area representing the peripheral visual field (Bando, 1985). A difference was also found between areas representing the central visual field: the latency of evoked disjunctive eye movement was shorter in the caudal PMLS than that obtained in the rostral PMLS. Parts of the LS area may, therefore, play different roles in controlling intra- and extraocular movements. The hierarchial order among these subareas, if any, remains to be determined.

9.2. Differences in oculomotor responses among different parts of the LS area: representations of central us. peripheral visual field

9.3. Possible candidates of the central correlate for ocular near response

In M T / M S T areas in the monkey, it was suggested that subareas representing the central visual field contribute to keep the visual target in the fovea during pursuit eye movement, and also in accelerating eye movement in the late slow-phase of the optokinetic nystagmus (OKN). On the other hand, it was suggested that subareas representing the peripheral visual field play a role in initiating pursuit eye movement, and also in accelerating eye movement in the initial slow-phase of the OKN. These suggestion were based on the effects of chemical lesions in areas representing central and peripheral visual fields (Diirsteler et al., 1987; Diirsteler and Wurtz, 1988) and the effects of electrical stimulation in comparable areas during pursuit eye movement (Komatsu and Wurtz, 1989). They were further supported by properties of pursuit-related neurons (Sakata et al., 1983) in these areas (Komatsu and Wurtz, 1988a; Newsome et al., 1988). Because neurons in the MT mainly depended on visual stimuli, and those in the MST also received extraretinal inputs, it was suggested that both visual signals (processed in the MT area) and extraretinal signals were integrated in the MST area (Komatsu and Wurtz, 1988b). Some LS neurons responded with directional selectivity to a large field stimulus such as a visual randomdot pattern of Julesz (grains, 1.6-4.8 deg) or the lightdark stripes with random spacing presented binocularly (Hamada, 1987). They preferred a large-field stimulus to a slit of light. Other LS neurons which preferred a

Lens accommodation, vergence eye movement and pupillary constriction, i.e. all of the component movements of ocular near response were evoked by microstimulation in the LS area. Neurons related to these movements were also recorded. In addition, the intracortical fiber connection in the LS area was found: the connection between the sites effective in evoking lens accommodation and those effective in evoking pupillary constriction. Based on this circumstantial evidence, it is suggested that the LS area provides the basis for the link between component movements in the ocular near response. Another correlate of the link in the near response is known to be in the primate mesencephalic reticular formation: a group of premotor neurons in the mesencephalic reticular formation of alert monkeys carried neuronal signals related to either lens accommodation, ocular convergence or both (Mays, 1984; Judge and Cumming). Components of the near response may be integrated in multiple stages. The LS area may also play a role in modulating the link among components of the near response. The link between lens accommodation and ocular convergence could be changed both in human and monkey when the visual environment surrounding them is changed (AIpern, 1969; Fincham, 1951). For example, the link between ocular convergence and lens accommodation was adaptively changed by using prisms or a periscope (Miles, 1985; Miles et al., 1987). However, the central

174 correlate of the adaptive link in the near response has not yet been found (Judge, 1987). Although it is not known whether similar adaptive changes in the near response occur in cat, the LS area is one of the plausible candidates for producing adaptive changes, if any, in the link between component movements of the near response.

10. Concluding remarks The LS area is one of the best-studied cortical visual area in the cat. Recently, the LS area has also been related to various types of eye movement (Toyama et al., 1984b; Tusa et al., 1989; Vanni-Mercier and Magnin, 1982; Yin and Greenwood, 1992). In the present paper, we concentrated on studies related to component movements of ocular near response. The resuits of these studies favor the working hypothesis that the LS area plays an important role in controlling these intra-and extraocular movements, in addition to other visual and oculomotor functions. However, some results reported in this paper are preliminary and await confirmation by future work. Other data are found to be lacking, especially those on the effects of the lesion in the LS area on lens accommodation and vergence eye movement, and those on the relative contribution of a single neuron to either lens accommodation or vergence eye movement. These matters are currently under study. The mechanism of the adaptive link between components of the near response remains to be elucidated.

Acknowledgements This work was supported by a Grant-in-Aid for Special Projects Research (03251212 and 04246215) from the Japanese Ministry of Education, Science and Culture, and a grant from the Brain Science Foundation. We thank Prof. M. Norita for valuable comments, K. Kunihara for photographic work, and S. Wakui for animal care.

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