Cortical Projections of Posterior Parietal Cortex in Owl Monkeys1 J. H. KAAS, C. S. LIN

AND E. WAGOR2 Departments of Psychology and Anatomy, Vanderbilt University, Nashville, Tennessee 37240

ABSTRACT Efferent cortical projections of posterior parietal cortex were determined by degeneration and autoradiographic methods in owl monkeys. Intraregional connections were to the immediate surround of the injection or lesion site, and to distinct foci within the posterior parietal region. The extraregional ipsilateral connections were with (1) previously established subdivisions of visual association cortex (the Dorsomedial Area, the Medial Area, the Dorsolateral Area, and the Middle Temporal Area), (2) other locations in caudal neocortex, and (3) frontal cortex. The callosal projections were to separate foci in posterior parietal cortex of the contralateral cerebral hemisphere. The separate foci of both ipsilateral and contralateral terminations in posterior parietal cortex raise the possibility that this region contains more than one functional subdivision. The connections with visual association cortex suggest a role for parietal cortex in visual behavior. Other foci in caudal neocortex indicate the possible locations of additional subdivisions of association cortex.

The posterior portion of the parietal lobe of primates is currently a region of considerable research interest. Recent electrophysiological studies of single neurons of posterior parietal cortex of macaque monkeys (Lynch et al., '75; Mountcastle, '75; Mountcastle et al., '75; Yin et al., '75; Hyvarinen and Poranen, '74; Hyviirinen et al., '74) have revealed neurons that discharge when the monkey reaches for an object it desires but are not active during other movements; other neurons can be classified in a broad sense as visual, and respond best when the animal visually fixates on a desired object, or visually tracks desired objects. A few neurons are most active when eye and hand tracking of an object are combined. In view of these electrophysiological findings, it is interesting to reconsider the behavioral consequences of parietal lobe lesions. Effects of parietal lobe damage have been described repeatedly in humans (e.g., Critchley, '66; Hecaen et al., '56; DennyBrown, and Chambers, '58; Denny-Brown and Banker; '54; Mountcastle, '75). While J. COMP. NEUR., 171; 387-408

the alterations in behavior following damage to posterior parietal association cortex vary somewhat according to the hemisphere affected, the size of the lesion, and perhaps other factors, a unilateral lesion is likely to produce a defect in the perception of the contralateral half of the body and visual space expressed by neglect of objects and the body on the side contralateral to the lesion. Mountcastle et al. ('751, have summarized the earlier reports by concluding that the common feature of the posterior parietal syndromes is an alteration "in the perception of the body form and its relation to surrounding space, and in stereotactic exploration of that space." In macaque monkeys, removal of posterior parietal cortex produces similar alterations in behavior with neglect of the contralateral limbs, a lack of spontaneous movements with the contralateral limbs, and less accurate reaching for targets or objects with the contralateral arm (Et1

Supported by NIH Grant R01-NS-12377.

* Present address: School of Medicine, Washington University, St. Louis, Missouri 63110.

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tlinger and Kalsbeck, '62; Hartje and Ettlinger, '74; Mountcastle, '75). After considering the electrophysiologicaland behavioral observations, Mountcastle et al. ('75) suggest that posterior parietal cortex functions in primates as a center for eliciting or "commanding" the visual or manual exploration of the contralateral hemifield of space. Presumably, the mediation of visual and manual exploration of space in posterior parietal cortex would require the integration of neural input related to the somatosensory and the visual modalities. The relay of somatosensory information from the anterior primary somatosensory areas to intermediate parietal cortex and then to posterior parietal cortex has been described in macaque monkeys (Jones, '69; Jones and Powell, '69, '70; Pandya and Kuypers, '69). The source of the visual input into posterior parietal cortex of macaque monkeys is unknown. However, in a New World monkey, the owl monkey, a dense fiber projection from the Dorsomedial Area (DM) of visual association cortex in the occipital lobe to a portion of the posterior parietal cortex has been described (Wagor et al., '75). Thus, indirect anatomical pathways allow posterior parietal cortex of primates to be influenced by both the visual and the somatosensory modalities, although it is uncertain whether or not these two inputs converge in the same area or terminate in adjacent but separate areas, since there are questions of homology in the two primates. The cortico-cortical efferents from posterior parietal cortex in macaque monkeys are to the frontal lobe, adjoining portions of the parietal lobe, caudal portions of temporal cortex, and cortex on the medial wall of the cerebral hemisphere (Jones and Powell, '70; Pandya and Kuypers, '69).The efferent connections of posterior parietal cortex in New World monkeys have not been established, and the functional subdivisions of this region remain uncertain (RESULTS). The goal of the present study was to determine efferent projections of the

sector of posterior parietal cortex of the owl monkey that is defined by input from DM. It was hoped that these studies would further the understanding of the organization and functions of posterior parietal cortex in primates. METHODS

The efferent projections of posterior parietal cortex were determined by tracing degenerating or labeled axons after cortical lesions or injections of H3-proline using methods similar to those described previously (Wagor et al., '75). In order to produce axonal degeneration, small shallow lesions restricted to the grey matter were placed by aspiration in parietal cortex of five adult owl monkeys, Aotus trivirgatus. In three other owl monkeys, small amounts of tritiated proline (0.3 to 0.15 p1 at a concentration of 25 pmC/p1) were injected into parietal cortex. The lesions and injections were made under aseptic conditions in monkeys anesthetized with ketamine HCl. After survival times of three to seven days, the animals were re-anesthetized with sodium pentobarbital, and perfused with 10%formalin in 0.9%saline. The removed brains were placed for several days in a solution of 30% sucrose dissolved in 10% formalin. Next, the brains were frozen and 25 p sections were cut in the frontal or parasagittal plane. Brains with lesions were stained by the Wiitanen ('691silver method and counterstained with cresyl violet. The brains injected with tritiated proline were processed according to the procedure of Cowan et al. ('72) and the processed brain sections were stained with cresyl violet. Additional sections from each brain were stained with hematoxylin for myelinated fibers. The results were analyzed by indicating areas of degeneration or radioactivity on detailed drawings of serial brain sections. These drawings were used to reconstruct dorsolateral, medial, and dorsal views of the cerebral hemispheres on which areas of axonal termination and architectonic boundaries could be indicated. Photographs of the experimental

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brains in standard views guided the reconstructions. RESULTS

Lesions or injections in posteriorparietal cortex revealed intraregional connections within parietal cortex, callosal projections to parietal cortex of the opposite hemisphere, and ipsilateral projections to subdivisions of visual association cortex and to frontal cortex. Subcortical projections included the caudate nucleus, putamen, claustrum, reticular nucleus of the thalamus, zona incerta, pregeniculate nucleus, ventrolateral nucleus, lateral posterior nucleus, a subdivision of the inferior pulvinar complex, pretectum, superior colliculus, and pons. These subcortical connections are not described in this report.

1. The subdivisions of visual association cortex and the extent of the posterior parietal cortex (PP) Describing the projections of posterior parietal cortex starts with the problem of subdividing cortex. In any study of cortical connections it is desirable to identify both the specific area in which the lesion or injection is placed and as many as possible of the subdivisions of cortex where terminations take place. This identification is conveniently done in terms of architectonic boundaries if the boundaries are clear and the significance of the boundaries has been established. For purposes of determining some cortical connections, the owl monkey offers some advantage, since many of the subdivisions of visual association cortex have been indicated by electrophysiological mapping studies, and these subdivisions have been correlated with cortical architecture (Allman and Kaas, '71, '74a,b, '75, '76).For example, it is possible to routinely determine the boundaries of Area 17 (VI), the Middle Temporal Visual Area (h4T1, and the Dorsomedial Visual Area (DM)because of the histological distinctiveness of these areas. Furthermore, the inner borders of Area 18 (VII) and the Dorsolateral Area (DL) are distinct from Area 17 and

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MT respectively, and the outer borders of Area 18 and DL can be reasonably estimated from the widths of these areas as determined in electrophysiologicalstudies. The criteria for distinguishing these areas have been discussed elsewhere (Wagor et al., '75) and were used in the present study to designate borders in the illustrated material. However, we do not yet have a comparable way for determining borders for posterior parietal cortex. It is presently difficult to delimit posterior parietal cortex in owl monkey by architectonic criteria. A lack of agreement as how to subdivide posterior parietal cortex by architectonic criteria in New World monkeys is apparent when one compares the classical map of Brodmann ('09) with the more recent study of Peden and von Bonin ('47) in figure 1. However, some architectonic distinctions can be made in posterior parietal cortex of the owl monkey. In particular, much of the region is moderately myelinated, and a sharp boundary exists on the medial wall of the cerebral hemisphere where a junction occurs with a lightly myelinated region (see fig. 2 of Wagor et al., '75). Other borders are not as apparent, and since we do not know the significance of any of the architectonic changes, we are reluctant to depend upon them. Unfortunately, the properties of neurons in posterior parietal cortex of the owl monkey have not been studied and related to regional differences in cortical structure. Furthermore, although many of the neurons of posterior parietal cortex respond to visual stimuli and have receptive fields (Allman and Gas, '71 and fig. 11, no single clear area with a retinotopic organization has been identified. However, there did seem to be one way in which preliminary studies of the connections of posterior parietal cortex could be initiated. A zone of input from the visual association cortex, DM, was established in an earlier study (Wagor et al., '75 and fig. 1).While, the exact boundaries of the projection zone had not been determined, it

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seemed that lesions or injections could be present experimental cases, an attempt was placed well within the projection zone in made to somewhat center the lesion or inmost cases. Therefore, we decided to jection within the previously identified define posterior parietal cortex (PP) by the projection zone, often just at the medial expected locution of input from DM rather edge of the Sylvian fissure where the most than by architectonic criteria, and lesions dense projections from DM terminate (fig. and injections were placed within the re- 1). While we felt this procedure would region previously defined as the projection strict the lesion or injection site to the prozone of DM. Since, the exact projection jection zone of DM in all or most cases, we zone of DM was not known for any of the had no way of knowing whether or not the

Fig. 1 The posterior parietal cortex in New World Monkeys. Peden and von Bonin ('47) described a small upper posterior parietal region, PE, and a larger anterior region, PC. Brodmann's ('09)posterior parietal division, Area 7, is more comparable in location and size to the parietal projection zone of the Dorsomedial Visual Area, DM, of the owl monkey (Wagor et al., '75). The projection zone of DM also appears to overlap one of the projection zones of the Middle Temporal Visual Area, MT, i.e., focus 5 of Spatz and Tigges ('72).Posterior parietal cortex has been shown to respond to visual stimuli (Allman and Kaas, '71).

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projection zone from DM represented a single functional subdivision of parietal cortex, or several. 2. lntraregional connections and emerging

efferent pathways After looking at the brain sections in the vicinity of the lesion or injection sites in the present cases, it was apparent that (1)the superficial layers of cortex connect profusely with layer V, (2)there are horizontal connections to adjoining and nearby portions of parietal cortex, and (3)major fiber pathways leave parietal cortex to course to distant cortical and subcortical structures. The projections from the superficial layers to layer V of parietal cortex were best seen in owl monkey 74-71 where the injection of tritiated proline was limited to the supergranular layers of cortex. As a result, silver grains were clearly concentrated in layer V immediately beneath the injection site. There were fewer silver grains in layers IV and VI and many of these grains were oriented along lines suggesting the pathways of fibers emerging from the injection sites (fig. 2 and plate 1).Evidence

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for connections from superficial layers to layer V was also noted in other cases where part or all of the injection or lesion was superficial to layer IV. Short horizontal connections to the cortex immediately surrounding the lesion or injection sites are suggested by the dense label or degeneration product around the sites (i.e., fig. 2). Although, much of this label could be from diffusion of the proline or degeneration of parts of cells other than axons, the orientation of some of the silver granules argues for short horizontal interconnections within parietal cortex. Proline was also transported to portions of posterior parietal cortex, more distant than the immediate surround. For example, in brain section A of figure 2, a focus of label is illustrated near the medial wall several millimeters from the injection site. Labeled fibers can be traced from the injection site through the deeper layers of cortex and the adjoining white matter to this medial focus where label is somewhat concentrated in layer IV. A second focus on the medial wall is seen in section B of figure 2; this focus is at the border of the densely

Owl Monkey 74-71

PP Ini.

Fig. 2 Intraregional connections and emergingefferent pathways of posterior parietal cortex in owl monkey 74-71. The frontal brain sections were cut at 25 p and numbered consecutively from the posterior pole. The densely labeled injection site is in black. The proportional amounts and locations of labeled axon terminals and fibers are indicated by dots and dashes, respectively. CC, corpus callosum; Cd, caudate nucleus; F, fornix. Fiveday survival.

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Fig. 3 A drawing of a part of a parasagittal section of owl monkey 75-3, showing the lesion site (black) in posterior parietal cortex and the resulting degeneration (dots and dashes), in adjoining cortex and in the Dorsomedial Visual Area (DM).Areas 17,18, and the IV layer of cortex are indicated. The section number is from a consecutive medialward series cut at 25 p. Three-day survival.

myelinated portion of posterior parietal cortex, possibly outside PP. A third focus is located on the medial bank of the Sylvian fissure. More rostrally in PP (section C ) , two separate puffs of label are seen in the Sylvian fissure. The upper puff is clearly a continuation of the label in the third focus shown in section B. The lower puff may be a branch of a separate focus. Pathways to the termination sites within posterior parietal cortex, but rostral to the lesion, were best seen in the two cases cut in the parasagittal plane. Figure 3 illustrates the distribution of the rostral degeneration in a representative brain section after a small lesion of PP near the caudal end of the medial wall of the Sylvian fissure. Some degenerating fibers leave the lesion site and travel largely within layer IV to cortex immediately rostral to the lesion both on the dorsal surface and on the

medial (dorsal) bank of the Sylvian fissure. In other sections, fibers pass from the lesion into the white matter to terminate more distantly along the medial bank of the Sylvian fissure where concentrations of silver particles occur mainly in layer IV. Projections within parietal cortex of other animals are illustrated in figures 4, 5, and 6. Besides these short connections within parietal cortex, two major fiber bundles emerge from PP and course ventrally in the white matter (figs. 2, 8, 9). The more lateral of these bundles is less concentrated (plate 1: fig. 3) and forms the pathways to the lateral termination sites in visual association areas. The larger more medial bundle soon subdivides into one component that crosses in the corpus callosum and another portion that extends rostrally and laterally to descend into subcortical centers (plate 1: fg. 3). Other less im-

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Fig. 4 The cortical projections of posterior parietal cortex in owl monkey 74-18 as revealed by an injection of tritiated proline. The injection site is black and dots indicate the locations and proportional amounts of axon terminations. Arrows mark terminations hidden on the middle wall or the banks of the Sylvian fissure. Areas 17 and 18 are indicated. DL, Dorsolateral Visual Area; DM, Dorsomedial Visual Area; h4T, Middle Temporal Visual Area. Five-day survival.

pressive pathways extend in the white mat- DM. While the input from DM to PP is conter caudally to DM, and rostrally, perhaps centrated in layer IV (see &. 9 of Wagor et al., '751, the returning axons from PP termito frontal cortex (see below). nate largely in layers I and V. Fibers from the lesion or injection sites in PP pass 3. lpsilateral projections caudally in the deeper layers of cortex and The posterior parietal cortex projects to the adjacent white matter to reach DM several subdivisions of visual association (&.3). In the injection cases, silver grains cortex, to locations in parietal cortex, and were seen in all layers of DM, but they to several locations in the frontal lobe (figs. were concentrated in layers I and V (&.7). 4, 5, 6). These connections are described Only a few silver grains were found in below. layer IV and many of these grains could be labeled fibers passing to layer 1. After lea. The Dorsomedial Area sions of parietal cortex, degenerating fibers DM is located immediately behind the were seen in DM, but these cases did not posterior parietal cortex and provides a reveal the same predominance of input to substantial input to PP (Wagor et al., '75). layer I, perhaps because of the relatively The present results indicate that posterior long survival times. The locations of the parietal cortex, in turn, projects back to terminations in DM after injections or le-

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A

B \ Fig.5 The cortical projections of posterior parietal cortex in owl monkey 74-76. L, lesion site; FC, frontal cortex. The portion of the corpus callosum occupied by degenerating transcallosal fibers is marked by X s . Other conventions as in figure 4. A, dorsolateral view; B, medial view. Six-day survival.

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A L

Owl Monkey 75-2-

B Fig. 6 The cortical projections of posterior parietal cortex in owl monkey 75-2. Conventions as in figures 4 and 5. A, dorsolateral view; B, medial view. Six-day survival.

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DM

Fig. 7 A drawing of a frontal section of owl monkey 75-38 showing labeled axons and terminals in the Dorsomedial (DM)Visual Area after an injection of tritiated proline into posterior parietal cortex. The IVth layer of cortex is indicated. The section number is from a consecutive rostralward series cut at 25 p, Four-day survival.

sions of posterior parietal cortex varied (figs. 4, 5, 61, but there were too few cases to disclose a clear pattern to this variation.

b. The Middle Temporal and Dorsolateral Visual Areas MT and DL are located laterally in occipital-temporal cortex. MT projects to the posterior parietal region (fig.1, Spatz and Tigges, '721, and PP reciprocates by projecting back to MT and DL (figs.4,5,6). The fibers to MT and DL travel in the white matter near the margin of the cortex of the medial bank of the Sylvian fissure (figs. 2, 8, 91. They are lateral and somewhat caudal to the emerging subcortical and transcallosal pathways. Some of the fibers of the pathway to MT and DL pass through layer IV of the cortex in the depths of the Sylvian fissure but most remain in the white matter immediately adjacent to the cortex. This pathway could be traced to terminations in the occipital-temporal cortex in each case except.the one with the most superficial injection (even in this case, the lateral pathway was obvious near the injection site, fig. 2: section 635). Terminations in occipital-temporal cortex

appeared to be concentrated in layer IV, although label or degeneration product was seen in all cortical layers (plate 21. In most cases, brain sections stained for myelin allowed a clear architectonic distinction between MT and DL. In these cases, it was apparent that some of the terminations were in MT and some were in DL. The terminations were located in the upper to middle portion of MT and the central to upper parts of DL (figs. 4-6, 8, 9). In one case, a few fibers were noted in the region of the lower wing of DL. c. Other regions of caudal ipsilateral terminations The lateral pathway consistently contributed to terminations in cortex between the upper wing of DL and the Sylvian fissure (figs.4-61. This region of cortex is responsive to visual stimuli (Allman and G a s , '711, but the retinotopic organization, if any, is unknown. Another focus of terminations was noted in the cortex of the lateral bank of the Sylvian fissure in two cases (fig. 4). In three of the cases, terminating fibers were seen more caudally in cortex that appeared to be just lateral to DM (fig.41, i.e., in the Dorsointermediate Area (Allman and Kaas, '76). Other terminations were found on the medial wall of the cerebral hemisphere in cortex just ventral to DM (figs. 5,61 in the region of the Medial Visual Area (Allman and b a s , '761, and more rostrally in two separate foci in parietal cortex (figs.2,4-6,8,9).The more rostral terminations on the medial wall suggest further subdivisions of parietal cortex.

d. Frontal cortex The posterior parietal cortex projects to the two or more separate locations in the frontal lobe (figs. 5, 6, 10). The pathway from the lesion or injection sites to terminations in frontal cortex has not been completely traced. The conspicuous and rostrally coursing pathway located deep in the white matter and labeled SC in figures 8 and 9 appears to contribute only to subcortical structures. Another pathway of scattered fibers travels rostrally in the

P P Lesion

Fig. 8 Drawings of frontal sections showing projection pathways from posterior parietal cortex in owl monkey 75-2. SC, subcortical pathway; HP, Hippocampus; other conventions as in figure 4. The section numbers are from a consecutive rostralward series cut at 25 p.

Owl Monkey 75-2

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Fig. 10 Drawings of two frontal sections of owl monkey 74-76 showing terminations in two locations of frontal cortex (see figure 51. The section numbers are from a caudalward series cut at 25 p. Layer IV is indicated.

white matter just ventral to parietal cortex. These fibers were not obvious in the cases cut in the frontal plane, but they could be seen clearly in the two cases cut in the parasagittal plane in which they were traced to the frontal lobe, but could not be followed all the way to termination sites. Terminations in frontal cortex were concentrated in layer IV (&. 10) and formed at least two separate foci, one more dorsal and caudal than the other (figs. 5, 6). In several cases, the dorsal and ventral foci were subdivided so that up to four separate locations of terminations could be identified. These termination sites are somewhat caudal and dorsal to those we have observed after lesions of DM in the owl monkey (Wagor et al., '75). 4. Transcallosal connections The posterior parietal region projects to two or more separate foci in the posterior parietal cortex of the opposite hemisphere. The course of the transcallosal pathway can be seen in figures 2, 8 and 9. A dense band of fibers leaves the injection or lesion site and passes ventrally and somewhat rostrally in the white matter to reach the region of the caudal end of the corpus callosum. Here, this fiber band separates

into a lateral component of fibers that courses further rostrally to terminate subcortically, and a medial component that crosses to the opposite hemisphere in the caudal third of the corpus callosum. These callosal fibers do not form a compact bundle as do the crossing axons from DM (Wagor et al., '75). After crossing, the fibers ascend and move caudally to terminate in several locations of posterior parietal cortex (plate 2: fig. 7). Some transcallosal fibers terminate in a location in parietal cortex that is homotopic or nearly homotopic to the lesion or injection site. Thus, in figures 4, 5, and 9 many terminations are concentrated in the location corresponding to the lesion or injection site in the opposite cerebral hemisphere. In case 75-2 (figs. 6, 81, the major contralateral focus is somewhat rostral to the precisely symmetrical location, and this suggests that the organization of posterior parietal cortex of the two sides is not always perfectly matched. Besides, the homotopic focus of terminations, there are other transcallosal foci of terminations in the parietal lobe that are slightly displaced from the position that is symmetrical to the injection or lesion site. In figure 4, for example, there are three

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separate foci of contralateral terminations, and the contralateral terminations on the bank of the Sylvian fissure (see arrow) are in heterotopical locations. Likewise, in case 75-2 (fig.61, the medial and the rostra1 contralateral foci of degeneration are heterotopic. In case 74-76 (fig.51, the degeneration in the opposite parietal lobe occupies an extensive region without completely separate foci, but the degeneration extends forward along the medial bank of the Sylvian fissure to include cortex that does not correspond to the injection site. Finally, it may be significant that at least some of the separate foci of contralateral terminations are matched by ipsilateral terminations in approximately the corresponding locations. DISCUSSION

Several issues are raised by the present results. First, the separate foci of terminations within posterior parietal cortex suggest that this region may be subdivided into several interconnected but functionally distinct areas. Second, the observations that many of the connections of posterior parietal cortex are to subdivisions of visual association cortex is consistent with the view that part of the parietal lobe is important in some types of visual behavior. Third, some of the terminations in caudal neocortex point out the possible locations of presently unexplored association areas. Fourth, the projections to frontal cortex add to the evidence that frontal cortex receives input from many subdivisions of association cortex. Finally, there are uncertainties in the comparison of the present results with similar anatomical studies of posterior parietal cortex of Old World monkeys. These issues are considered further below.

Zpsilateral and contralateral terminations within PP and the major emerging pathways Lesions or injections in PP resulted in extensive degeneration or label within parietal cortex, and usually separate foci of terminations could be seen. Likewise, the

transcallosal connections were to several separate locations in the parietal lobe. Although in many reports posterior parietal cortex, as Brodmann's Area 7, is considered a single area, there is presently insufficient information as to whether the region we have called PP is a single functional subdivision of cortex, or several. Single lesions or injections within such functional areas as Area 17, Area 18, MT or DM do not appear to produce multiple foci of terminations within the same area either ipsilaterally or contralaterally (Spatz et al., '70; Spatz and Tigges, '72; Kaas and Lin, '77; Wagor et al., '75);however, Tigges et al., ('741, report a separate focus of degeneration within Area 18 after a lesion of Area 18. In contrast, connections from one functional subdivision of cortex to several others are common. For example, MT projects to a total of nine separate ipsilateral foci in other areas of cortex (Spatz and Tigges, '72).In a similar manner, callosal connections may be with several subdivisions of cortex. Thus, t h e callosal connections of DM are homotopic to DM and heterotopic to MT and PP (Wagor et al., '75). Since both ipsilateral and callosal connections between heterotopic parts of the same area are uncommon and connections between different areas prevail, the separate ipsilateral and contralateral foci of terminations within PP argue that PP is not a single area of cortex. In addition to connections between parts of PP, the upper layers of posterior parietal cortex connect strongly with layer V. Such connections appear to exist in many areas of cortex and in many species of mammals (Nauta et al., '73; Levey and Jane, '75). Similar connections from supragranular layers to layer V were observed in DM of the owl monkey (Wagor et al., '75) and Areas 17 (Spatz et al., '70; Martinez-Milltin and Holliinder, '75) and 18 (Tigges et al., '74) in the squirrel monkey.

Projections to the visual areas DM, MT, DL, and M Perhaps the major source of visual input into posterior parietal cortex is from the

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adjoining visual area, DM (Wagor et al., '751, and posterior parietal cortex projects back to DM in an interesting manner. While the pathway from DM to PP appears to terminate largely in layer IV, the returning pathway appears to mainly effect layers I and V. Thus, the input from DM has the potential of feeding into the early steps of the processing in PP, while the feedback from PP to DM may terminate on the ends of apical dendrites in layer I and the basal dendrites in layer V of pyramidal cells. Such feedback has the potential of directly modulating the activity of those cells producing the final output of DM. A similar role has been postulated (Allman and Kaas, '74a) for the feedback from Area 18 to layer I of Area 17 (Tigges et al., '73). Cortical areas MT, DL, and M also receive input from the posterior parietal region. MT receives input from Area 17 (Spatz et al., '701, DM [Wagor et al., '741, as well as the inferior pulvinar (Lin et al., '731, and projects widely to a number of other subdivisions of posterior neocortex, including the posterior parietal region (Spatz and Tigges, '72).DL receives connections from MT (Spatz and Tigges, '721,but other connections remain to be established. Posterior parietal cortex also projects to cortex immediately ventral to DM on the medial wall of the cerebral hemisphere. This is the location of the medial area M, which is less devoted to representing the central visual field and more to paracentral visual field than other visual areas (Allman and Kaas, '76). Area M appears to receive input from DM (Wagor et al., '751, MT (Spatz and Tigges, '721, and perhaps from the parts of Area 17 representing paracentral vision (Martinez-Millh and Holliinder, '75; see Allman and Kaas, '76) In summary, the subdivisions of visual cortex are multiply interconnected, and these interconnections include posterior parietal cortex. Connections with visual association cortex may relate to the observations that posterior parietal cortex has neurons responsive to visual stimuli (Allman and Kaas, '71; Hyviirinen and Poranen, '74; Hyviirinen et al., '74; Mountcastle, '75;

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Mountcastle et al., '751, that electrical stimulation produces eye movements (Fleming and Crosby, '551, and that lesions result in disturbances in visually dependent behavior (see Mountcastle et al., '75, for review).

Other foci of terminations Besides the visual association areas known to contain systematic maps of visual space, terminations were consistently seen in two other locations in caudal neocortex after lesions and injections in PP. One location was in visually responsive cortex (Allman and Kaas, '71) of the superior temporal sulcus just dorsal to MT and DL. This location could be the site of another visual representation, and microelectrode mapping studies would be useful. The second location was on the medial wall of cerebral cortex just ventral to PP. Neurons in this region did not respond to simple visual stimuli in anesthetized owl monkeys (Allman and Kaas, '711, and this may be a subdivision of cortex where non-visual functions predominate. Lesions and injections in PP also resulted in several separate foci of terminations in frontal cortex in a region roughly corresponding to cortex designated in the marmoset as Area 8 by Brodmann ('091 and Area FC by Peden and von Bonin ('471. While we have not attempted to describe this cortex in terms of histological structure, the terminations are in cortex that is characterized by a clear layer of granule cells. The projection zone is probably within the cortex known as the frontal eye field (Smith, '44; see Mott et al., 'lo for electrical stimulations of this region in the marmoset) and the immediately adjacent frontal cortex. In a previous study, DM lesions produced degeneration in a slightly more ventral and rostral location in frontal cortex (Wagor et al., '751, and projections to what appears to be approximately the same region of frontal cortex have been reported from MT in the marmoset (Spatz and Tigges, '721, and Area 18 (VIII in the squirrel monkey (Tigges et al., '741. In macaque monkeys, lesions of the non-primary cortex of the temporal, parietal, and

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occipital lobes all result in projections to the frontal lobe (Jones and Powell, '70; Pandya and Kuypers, '69; Jones, '69; Petras, '71). Thus, frontal cortex may receive input from a large number of different subdivisions of association cortex including visual, somatic, and auditory areas (for further discussion see Nauta, '71; Jones and Powell, '70).

Comparisons with Old World monkeys It is difficult to compare in detail the present results with studies of the projections of the parietal lobe in Old World monkeys because there is uncertainty about the identification of homologous areas. We have described the projections of part of the parietal lobe of the owl monkey, i.e., the part that receives projections from a visual area, DM. Since DM has only been described in the owl monkey, its projection zone is not known for any other primate. However, on the basis of genetic relationships and preliminary recording experiments (Wagor et al., '751, it seems reasonable to presume the existence of D M and thereby the parietal projection zone of DM in other primates, and it is likely, though uncertain, that the homolog of PP in macaque monkeys is within the cortex designated as Area 7 by Brodmann. The cortico-cortical projections of the parietal lobe in macaque monkeys have been reviewed and described by several recent investigators (Jonesand Powell, '70; Petras, '71; Pandya and Kuypers, '69; Pandya and Vignolo, '69). In brief, the rostra1 primary sensory areas project to intermediate parietal cortex in the region of Brodmann's ('09)Area 5, which in turn projects to the caudal portion of the parietal lobe (Area 7 ) .The cortex in the region of Area 7 of the macaque monkey projects to temporal cortex in the region of the superior temporal nucleus, to the medial wall of the cerebral hemisphere, and to frontal cortex. Possibly, some of these connections were revealed as a result of damage to the homolog of PP. For example, pp projects to Win the owl monkey, and the projection of Area 7 in macaque

monkeys to the superior temporal sulcus is to the expected location of MT (Allman and Kaas, '71). However, the projections from parietal cortex in macaque monkeys do not appear to include input to the occipitai cortex in the expected location of DM. Unfortunately, it is presently difficult to account for dissimilarities in connections for they could simply reflect different observations, procedures, lesion location and size, or the more basic issue of the existence of homologous areas and species differences in connections. ACKNOWLEDGMENTS

We are grateful to Dr. Leon Schmidt, Southern Research Institute, Birmingham, Alabama, for the owl monkeys. Histological materials were prepared by Ms. L. Symonds and Ms. L. Farrell. LITERATURE CITED Allman, J. M., and J. H. Kaas 1971 A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey (Aotus trivirgatus). Brain Res., 31: 85-105. 1974a The organization of the second visual area (VII) in the owl monkey: A second order transformation of the visual hemifield. Brain Res., 76: 247-265. 1974b A crescent-shaped cortical visual area surrounding the middle temporal area (MT) in the owl monkey (Aotus trivirgatusl. Brain Res., 81: 199-213. 1975 The dorsomedial cortical visual area: A third tier area in the occipital lobe of the owl monkey (Aotus trivirgatusl. Brain Res., 100: 473-487. 1976 Representation of the visual field on the medial wall of occipital-parietal cortex in the owl monkey. Science, 191: 572-575. 1909 Vergleichende LokalisaBrodmann, K. tionslehreg der Grosshirnrinde. Verlag V. A. Barth, Leipzig, 324 pp. Cowan, W. M., D. I. Gottlieb, A. E. Hendrickson, J. L. Price and T. A. Woolsey 1972 The autoradiographic demonstration of axonal connections in the central nervous system. Brain Res., 37: 21-51. Critchley, M. 1953 The Parietal Lobes. New Hafner Publishing Co. Denny-Brown, D., and R. A. Chambers 1958 The parietal lobes and behavior. Res. Publ. Assoc. Res. Nerv. Ment. Dis., 36: 35. Denny-Brown, D., and B. Banker 1954 A morphosynthesis from left parietal lesion. Arch. Neurol. and Psvchiatr., 71: 302-313. Doty, R.*W., and N. Negrb 1973 Forebrain commissures and vision. In: Handbook of Sensory Physi-

-

-

POSTERIOR PARIETAL CORTEX CORTICAL PROJECTIONS

ology. Vol. VII/3B. R. Jung, ed. Springer-Verlag, New York. Ettlinger, G., and J. E. Kalsbeck 1962 Changes in tactile discrimination and in visual reaching after successive and simultaneous bilateral posterior parietal ablations in the monkey. J. Neurol. Neurosurg. Psychiat., 25: 256-268. Fleming, J. F. R., and E. C. Crosby 1955 The parietal lobe as an additional motor center. J. Comp. Neur., 103: 485-512. Geschwind, N. 1965 Disconnection syndromes in animals and man. Brain, 88: 237-294 and 585-644. Hartje, W., and G. Ettlinger 1974 Reaching in light and dark after unilateral posterior parietal ablations in the monkey. Cortex, 9: 346-354. Hecaen, H., W. Penfield, C. Bertrand and R. Malmo 1956 The syndrome of apractognosia due to lesions of the minor cerebral hemisphere. Arch. Neurol. and Psychiat., 75: 400-434. H y v h e n , J., and A. Poranen 1974 Function of the parietal associative Area 7 as revealed from cellular discharges in alert monkeys. Brain, 97: 673-692. Hyviirinen, J., A. Poranen, and Y. Jokinen 1974 Central sensory activities between sensory input and motor output. In: The Neurosciences Third Study Program. F. D. Schmitt and F. G. Worden, eds. M. I. T. Press, Cambridge, Massachusetts, pp. 311-318. Jones, E. G. 1969 Interrelationships of parieto-temporal and frontal cortex in the rhesus monkey. Brain Res., 13: 412-415. Jones, E. G., and T. P. S. Powell 1969 Connexions of the somatosensory cortex of the rhesus monkey: Ipsilateral cortical connexions. Brain, 92: 477-502. 1970 An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain, 93: 793-820. Kaas, J.H., and C. S. Lin 1977 Cortical projections of area 18 in owl monkeys. Vision Res., in press. Levey, N. H., and J. A. Jane 1975 Laminar thermocoagulation of the visual cortex of the rat. Brain Behav. and Evol., 1 1 : 257-274. Lin, C. S., E. Wagor and 1. H. Kaas 1973 Projections from the pulvinar to the middle temporal visual area (MT) in the owl monkey, Aotus triuirgatus. Brain Res., 76: 145-149. Lynch, J. C., T. C. T. Yin, W. H. Talbot and V. B. Mountcastle 1975 A cortical source of command signals for visually evoked saccadic movements of the eyes in the monkey. Neuroscience Abst., 1 : 59. Martinez-Millh, L., and H. Hollander 1975 Corticocortical projections from striate cortex of the squirrel monkey (Saimiri Sciureus), a radioautographic study. Brain Res., 83: 405-417. Mott, F. W., E. Schuster and W. D. Halliburton 1910 Cortical lamination and localization in the brain of the marmoset. Proc. Roy. Soc. (London), B82: 124-134. Mountcastle, V. B. 1975 The view from within: Path-

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ways to the study of perception. Johns Hopkins Med. J., 136: 109-131. Mountcastle, V. B., J. C. Lynch, A. Georgopoulos, H. Sakata and C. Acuna 1975 Posterior Parietal Association cortex of the monkey: command functions for operations within extrapersonal space. J. Neurophysiol., 38: 871-908. Nauta, W. J. H. 1971 The problem of the frontal lobe: a reinterpretation. J. Psychiat. Res., 8: 167-187. Nauta, H. J. W., A. B. Butler and J. A. Jane 1973 Some observations on axonal degeneration resulting from superficial lesions of the cerebral cortex. J. Cornp. Neur., 150: 349-360. Pandya, D. N., and H. G. J. M. Kuypers 1969 Corticocortical connections in the rhesus monkey. Brain Res., 13: 13-36. Pandya, D. N., and L. A. Vignolo 1969 Interhemispheric projections of the parietal lobe in the rhesus monkey. Brain Res., 15: 49-65. Peden, J. H., and G. von Bonin 1947 The neocortex of Hapale. J. Comp. Neur., 86: 37-63. Petras, J. M. 1971 Connections of the parietal lobe. J . Psychiat. Res., 8: 189-201. Smith, W. K. 1944 The frontal eye fields in: The precentral motor cortex. P. C. Bucy, ed. Univ. of Illinois Press, Urbana, pp. 307-342. Spatz, W. B. 1975 Thalamic and other subcortical projections to area MT (visual area of superior temporal sulcus) in the marmoset, (Callithrir jacchus). Brain Res., 99: 129-134. Spatz, W. B., and J. Tigges 1972 Experimental-anatomical studies on the “middle temporal visual area (MT)” in primates. Efferent cortico-cortical connections in the marmoset (Catlithn‘x jacchus). J. Comp. Neur., 146: 451-463. Spatz, W. B., J. Tigges and M. Tigges 1970 Subcortical projections, cortical associations, and some intrinsic interlaminar connections of the striate cortex in the squirrel monkey ISaimiri). J. Comp. Neur., 140: 155-174. Tigges,J., W. B. Spatz and M. Tigges 1973 Reciprocal point-to-point connections between parastriate and striate cortex in the squirrel monkey (Sairniri).J. Comp. Neur., 148: 481-489. 1974 Efferent cortico-cortical fiber connections of Area 18 in the squirrel monkey (Sairniri).J. Comp. Neur., 158: 219-236. Wagor, E., C. S. Lin and J. H. Kaas 1975 Some cortical projections of the Dorsomedial Visual Area (DM) of association cortex in the owl monkey, (Aotus triuirgatus). J. Comp. Neur., 136: 227-250. Wiitanen, J. T. 1969 Selective silver impregnation of degenerating axons and axon terminals in the central nervous system of the monkey (Macaca mulatta). Brain Res., 14: 546-548. Yin, T. C. T., J. C. Lynch, W. H. TaIbot and V. B. Mountcastle 1975 Neuronal mechanisms of the parietal lobe for directed visual attention studied in waking monkeys. Neuroscience Abst., 1: 59.

PLATE 1 EXPLANATION OF FIGURES

Darkfield Photomicrographs of labeled tissue after injection of tritiated proline into posterior parietal cortex.

1 Distribution of silver grains in DM after injection into PP of owl monkey 74-18. The cortical layers are numbered. Five-day survival. Marker bar, 100 Pm.

2 The injection site in the supragranular layers of posterior parietal cortex of

owl monkey 74-71. Note label in layer V. Five-day survival. Marker bar, 1 mm.

3 Three efferent pathways from posterior parietal cortex as seen in the white matter of a frontal section about 6 mm ventral to an injection site in posterior parietal cortex of owl monkey 74-18. Compare with section 665 of iigure 8 and 595 of figure 10. LC, the fibers to lateral cortex (MT and DL); SC, the pathway to subcortical structures; CC, the pathway crossing in the corpus callosum. Marker bar, 0.5 mm.

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PLATE 1

J. H. Kaas, C. S. Lin and E. Wagor

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PLATE 2 EXPLANATIONS OF FIGURES

Projection areas of posterior parietal cortex. 4

A darkfield photomicrograph showing silver granules in DL after injection of tritiated proline in PP of owl monkey 74-18. Cortical layers are numbered. Five-day survival. Marker bar, 0.25 mm.

5 The degeneration product in layer IV of posterior parietal cortex of the medial bank of the Sylvian fissure after an aspiration lesion of nearby tissue (see section 525 of figure 8). Owl monkey 75-2: Wiitanen stain. Six-day survival. Marker bar, 60 pm.

6 Degenerating fibers in layer IV of frontal cortex of owl monkey 75-2 after a lesion of PP. Wiitanen stain. Marker bar, 60 pm.

7 Degeneration product on layer IV of PP after an aspiration lesion of area PP of the opposite cerebral hemisphere. Owl monkey 74-76, Wiitanen stain. Sixday survival. Marker bar, 60 pm.

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POSTERIOR PARIETAL CORTEX CORTICAL PROJECTIONS J. H. Kaas, C. S. Lin and E. Wagor

PLATE 2

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