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Topography of Visual Cortex Connections with Frontal Eye Field in Macaque: Convergence and Segregation of Processing Streams

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Topography of Visual Cortex Connections with Frontal Eye Field in Macaque: Convergence and Segregation of Processing Streams The Journal of Neuroscience, June 1995. 15(6): 4464-44137 Topography of Visual Cortex Connections with Frontal Eye Field in Macaque: Convergence and Segregation of Processing Streams Jeffrey D. Schall,’ Anne Morel,* Dana J. King,’ and Jean Bullier3 ‘Department of Psychology, Vanderbilt University, Nashville, Tennessee 37240, *Laboratory for Functional Neurosurgery, University Hospital, CH-8091 Zurich, Switzerland, and 3Cerveau et Vision, INSERM 371, 69500 Bron, France The primate visual system consists of at least two pro- (Ungerleider and Mishkin, 1982; Morel and Bullier, IWO; Baiz- cessing streams, one passing ventrally into temporal cor- er et al., I99 I ; Young, 1992). How information from the various tex that is responsible for object vision, and the other run- cortical areas is combined to generate perception and action is ning dorsally into parietal cortex that is responsible for not known. The investigation of visually guided eye movements spatial vision. How information from these two streams is may be a domain in which this issue can be examined effectively combined for perception and action is not understood. Vi- because information about both object identity and spatial lo- sually guided eye movements require information about cation must be combined to produce accurate eye movements. both feature identity and location, so we investigated the During natural viewing, saccades of less than IO” amplitude, topographic organization of visual cortex connections with which are by far the most common (Bahill et al., 1975), direct frontal eye field (FEF), the final stage of cortical processing gaze to conspicuous and informative features in the scene (re- for saccadic eye movements. Multiple anatomical tracers viewed by Viviani, 1990; Rayner, 1992). Thus, both object vi- were placed either in parietal and temporal cortex or in dif- sion and spatial vision are needed for these saccades. Larger ferent parts of FEF in individual macaque monkeys. Con- amplitude saccades, however, being guided less by object rec- vergence from the dorsal and ventral processing streams ognition processes because of reduced peripheral visual acuity, occurred in lateral FEF but not in medial FEF. Certain ex- are involved in orienting responses to peripheral visual as well trastriate areas with retinotopic visual field organizations as to acoustic stimuli and therefore are more closely related to projected topographically onto FEF. The dorsal bank of the spatial vision. This study examined the pattern of connections superior temporal sulcus projected to medial FEF; the ven- tral bank, to lateral FEF, and the fundus, throughout FEF. of frontal eye field (FEF) and surrounding prefrontal cortex with Thus, lateral FEF, which is responsible for generating short extrastriate visual areas and other postcentral cortical areas be- saccades, receives visual afferents from the fovea1 repre- cause FEF represents a final stage of cortical processing for vi- sentation in retinotopically organized areas, from areas sually guided, purposive saccades (Bruce and Goldberg, 1985: that represent central vision in inferotemporal cortex and Segraves and Goldberg, 1987; Schall, 1991 b; Dassonville et al., from other areas having no retinotopic order. In contrast, 1992; Segraves, 1992). medial FEF, which is responsible for generating longer A number of studies have investigated FEF connectivity (re- saccades, is innervated by the peripheral representation of viewed by Leichnetz and Goldberg, 1988). This study departs retinotopically organized areas, from areas that emphasize from previous work in several ways. First. two or three tracers peripheral vision or are multimodal and from other areas were injected simultaneously in the same animal. The tracers that have no retinotopic order or are auditory. were placed either within functionally distinct areas-posterior [Key words: frontal eye field, saccade, eye movement, parietal and inferior temporal cortex-or within different zones visual system, extrastriate cortex, oculomotor system, vi- of one functionally identified area-the frontal eye tield. This sual cortex, parallel pathways, frontal cortex] method makes it possible for the first time to examine directly the convergence and segregation of visual processing streams in Visual processing in the cerebral cortex proceeds through mul- tiple visual areas into a dorsal pathway responsible for spatial frontal cortex. Second, the description of architectonic and func- vision and into a ventral pathway responsible for object vision tional areas in prearcuate cortex (Bruce et al., 1985; Stanton et al., 1989: Preuss and Goldman-Rakic, 1991) and in extrastriate visual cortex has become more refined (reviewed by Colby and Rrccivcd July 20. lYY3: r&ml Jan. IY. IYYS: accepted Jan. 23. lYY5. We thallh Sandrinc Bcnumont, Noelle Bayer. Judy Ives. Lmrn Trite, and Duhamel, 1991; Fellernan and Van Essen, 1991). The locations Rcnw Wall l)r skilled technicnl ahsistancc. S;mh Adcrholt. Sarah Laborde, of tracer injections and the spatial distribution of labeled ter- Frmk Tu. ;ml Chl-i\ty Whalley for a\~\tnnce with data acquisition and nnnl- minals and neurons were analyzed in relation to these improved ysis, md the rcvicwcr~ lor helpful comments. J. Scholl wx suppwtetl by ROI EYOXXYO. il t’cllmvship l’rm~ the Alfred P Sloan Fwndation, :I grmt f’nm the architectonic descriptions. Finally, prearcuate cortex has a rough McDonnell-Pew Prqr;m it1 Cognitivr Neuroscience, P30-EYOX 126 to the retinotopic organization of saccade amplitude and visual tield Vanderhllt Vision Rewarch Center. and PX-HDlSOS2 to the John E Kennedy Ccntel- lx Rewarch 011 Educntim and Humun Development. A. Morel was eccentricity. Shorter saccades are generated by lateral FEE and wpportcd hy the Fmtkltion pwr la Recherchc h4Gtlic;dc and by ROI -EYO26Xh longer saccades, by medial FEF (Robinson and Fuchs, 1969; to J. KxI\. Bruce et al., 1985). Also, the receptive fields of visual cells in C~rrc\p~ndence hhoultl hr xldre\sed to Dr. Jcfltey D. Schnll. Department 01 Psychology, Wilwn Hall, Vmderbilt IJniverGty, Nashville. TN 37240. lateral prearcuate cortex represent the central visual tield. and Copyright 0 I YY5 Society for Neuroscience 0270-6474/%/l 54464-24%05.00/0 dorsomedial cells, the peripheral visual tield (Suzuki and Azu- The Journal of Neuroscience, June 1995, 15(6) 4465 ma, 1983). There is little information about the topography of rescent dyes were injected in 3% aqueous solution. WGA-HRP was visual afferents to FEE For example, it is not known whether injected in 2% saline. The injections were made with a I or S PI Han- ilton syringe onto which a pulled micropipette was attached. Injections retinotopically organized visual areas such as MT project topo- were placed at a rate of 0.1 ~I/20 min/mm along 4-6 mm long pene- graphically onto FEE Nor is it known whether areas that have trations into the rostra1 bank of the arcuate sulcus. an overrepresentation of the central or of the peripheral visual Hisfologicd prowssing. Conventional histological procedures were tield project differentially onto medial or lateral FEE The results used (Huerta et al., 1987; Morel and Bullier, 1990; Schall et al., 1993b). of this investigation provide information that is necessary for Animals that received only fluorescent dyes recovered for a period of IO-IS d, and animals that received WGA-HRP + NY or WGA-HRP interpreting the functional properties of neurons in FEF in re- + tritiated amino acids survived 3 d. In one case (AM8). Huorescent lation to saccades guided by different kinds of visual informa- dyes were injected IO d before the injection of WGA-HRI? After per- tion. fusion, the brains were removed, photographed, and separated into two Preliminary reports of these data have appeared (Morel and blocks by a coronal section rostra1 to the central sulcus. Only the hem- Bullier, 1987; Schall et al., 1991, 1993a). sphere ipsilateral to the injections was studied. The rostra1 blocks were sectioned coronally in all cases except AM5.5 in which parasagittal sec- tions were used. The caudal blocks were sectioned coronally except for Materials and Methods AM4, which was cut instead horizontally. Sections were 40 or SO km thick, and those containing Huorescent material were immediately Three Mrrcrrccr rnulutttr and four Mucwrr ,firsciculuris monkeys, weigh- mounted, coverslipped, and stored at 4°C. An alternate series of sections ing 2-8 kg. provided the data for this study. All animals were cared for were stained for Nissl (cresyl violet or thionin) or myelin (GaIlyas, in accordance with the National Institutes of Health Guide for the Care 1979). In cases with WGA-HRP injections (e.g.. AM8 and AM2S), a and Use of Laboratory Animals. Data from the four cynomolgus mon- series of sections was processed for HRP histochemistry with the low keys were collected at Vision et Motricite, INSERM 94, where multiple artifact tetramethyl benzidine (TMB) method (Gibson et al.. 1984). In tracer injections were made into posterior parietal and inferior temporal AM2, a series was processed for autoradiography; sections were mount- cortex; we have already described the organization of connectivity ed and dipped in Ilford emulsion, exposed at 4°C for l&24 weeks, and among prestriate visual areas (Morel and Bullier, 1990). Data from the developed in Kodak PLl2, fixed, and counterstained with cresyl violet. three rhesus monkeys in which multiple tracer injections were made Sections containing fluorescent labeling were observed under ultra- into FEF were collected
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