Studies in the greater galago have not provided a comprehensive description of the organization of eye-specific retino-geniculate-cortical projections to the recipient layers in V1. Here we demonstrate the overall patterns of ocular dominance domains in layers III, IV, and VI revealed following a monocular injection of the transneuronal tracer wheat germ agglutinin conjugated with horseradish peroxidase (WGA-HRP). We also correlate these patterns with the array of cytochrome oxidase (CO) blobs in tangential sections through the unfolded and flattened cortex. In layer IV, we observed for the first time that eye-specific domains form an interconnected pattern of bands 200–250 μm wide arranged such that they do not show orientation bias and do not meet the V1 border at right angles, as is the case in macaques. We also observed distinct WGA-HRP labeled patches in layers III and VI. The patches in layer III, likely corresponding to patches of K lateral geniculate nucleus (LGN) input, align with layer IV ocular dominance columns (ODCs) of the same eye dominance and overlap partially with virtually all CO blobs in both hemispheres, implying that CO blobs receive K LGN input from both eyes. We further found that CO blobs straddle the border between layer IV ODCs, such that the distribution of CO staining is approximately equal over ipsilateral and contralateral ODCs. These results, together with studies showing that a high percentage of cells in CO blobs are monocular, suggest that CO blobs consist of ipsilateral and contralateral subregions that are in register with underlying layer IV ODCs of the same eye dominance. In macaques and humans, CO blobs are centered on ODCs in layer IV. Our finding that CO blobs in galago straddle the border of neighboring layer IV ODCs suggests that this novel feature may represent an alternative way by which visual information is processed by eye-specific modular architecture in mammalian V1.

In primates, the cortex adjoining the rostral border of V2 has been variously interpreted as belonging to a single visual area, V3, with dorsal V3 (V3d) representing the lower visual quadrant and ventral V3 (V3v) representing the upper visual quadrant, V3d and V3v constituting separate, incomplete visual areas, V3d and ventral posterior (VP), or V3d being divided into several visual areas, including a dorsomedial (DM) visual area, a medial visual area (M), and dorsal extension of VP (or VLP). In our view, the evidence from V1 connections strongly supports the contention that V3v and V3d are parts of a single visual area, V3, and that DM is a separate visual area along the rostral border of V3d. In addition, the retinotopy revealed by V1 connection patterns, microelectrode mapping, optical imaging mapping, and functional magnetic resonance imaging (fmri) mapping indicates that much of the proposed territory of V3d corresponds to V3. Yet, other evidence from microelectrode mapping and anatomical connection patterns supports the possibility of an upper quadrant representation along the rostral border of the middle of dorsal V2 (V2d), interpreted as part of DM or DM plus DI, and along the midline end of V2d, interpreted as the visual area M. While the data supporting these different interpretations appear contradictory, they also seem, to some extent, valid. We suggest that V3d may have a gap in its middle, possibly representing part of the upper visual quadrant that is not part of DM. In addition, another visual area, M, is likely located at the DM tip of V3d. There is no evidence for a similar disruption of V3v. For the present, we favor continuing the traditional concept of V3 with the possible modification of a gap in V3d in at least some primates.

Partial lesions of striate cortex were made in newborn and adolescent or young adult macaque monkeys, one newborn squirrel monkey, and adult squirrel and owl monkeys. After survival times ranging from 3 1/2 weeks to 8 years, the retinas were examined for transneuronal retrograde ganglion cell loss and retinal projections to the dorsal lateral geniculate nucleus, and other targets were examined for changes. After lesions in infant macaque monkeys and long postoperative survivals, nearly 80% of the ganglion cells were lost in the altered portions of the retinas. The degeneration appeared to be exclusively of ganglion cells projecting to the parvocellular layers of the lateral geniculate nucleus, and the loss of this class of cell appeared to be complete or nearly complete for the affected portions of the retina. Cases with shorter survivals showed that nine-tenths of the potential loss occurred within 6 months, and about half of the potential loss took place within one month. In cases where lesions were placed in adolescent and young adult macaque monkeys, the loss also was of ganglion cells projecting to the parvocellular layers. However, the rate of cell loss was slower so that little or no cell loss was apparent after six months, and only one-third to three-fourths of the potential loss occurred within 12–14 months. A cell loss of 22% was measured in the altered portions of the retina of a squirrel monkey lesioned as an infant and surviving for 6 months, but no regions of ganglion cell loss were apparent in the retinas of owl and squirrel monkeys lesioned as adults and surviving as long as two or more years.

We conclude that nearly 80% of the ganglion cells project to the parvocellular layers in macaque monkeys, and that the ultimate survival of these ganglion cells depends on the presence of target neurons in the parvocellular layers. Age is important in that the loss of ganglion cells proceeds rapidly in infant macaque monkeys, but slowly in older animals. Infant New World monkeys, judging from one squirrel monkey, are also susceptible to ganglion cell loss, although apparently at a rate comparable to older macaque monkeys. Finally, adult New World monkeys do not appear to be susceptible to ganglion cell loss. These age and species differences in rates of loss and susceptibility to loss challenge a “sustaining collateral” hypothesis proposed earlier (Weller et al., 1979), and suggest alternatives and modifications.

Two discrete areas in frontal cortex are involved in generating saccadic eye movements—the frontal eye field (FEF) and the supplementary eye field (SEF). Whereas FEF represents saccades in a topographic retinotopic map, recent evidence indicates that saccades may be represented craniotopically in SEF. To further investigate the relationship between these areas, the topographic organization of afferents to FEF from SEF in Macaco mulatto was examined by placing injections of distinct retrograde tracers into different parts of FEF that represented saccades of different amplitudes. Central FEF (lateral area 8A), which represents saccades of intermediate amplitudes, received afferents from a larger portion of SEF than did lateral FEF (area 45), which represents shorter saccades, or medial FEF (medial area 8A), which represents the longest saccades in addition to pinna movements. Moreover, in every case the zone in SEF that innervated lateral FEF (area 45) also projected to medial FEF (area 8A). In one case, a zone in rostral SEF projected to both lateral area 8A from which eye movements were evoked by microstimulation as well as medial area 8A from which pinna movements were elicited by microstimulation. This pattern of afferent convergence and divergence from SEF onto the retinotopic saccade map in FEF is indicative of some sort of map transformation between SEF and FEF. Such a transformation would be necessary to interconnect a topographic craniotopic saccade representation in SEF with a topographic retinotopic saccade representation in FEF.

The monoclonal antibody Cat-301 was used to stain neurons and neuropil in the visual thalamus and cortex of tree shrews —small, highly visual mammals that are closely related to primates. Previously, this antibody has been found to label neurons associated with the Y-cell stream of processing in cats and the magnocellular or M-cell stream in macaque monkeys. In tree shrews, the antibody selectively labeled layers 1, 2, 4, and 5 of the dorsal lateral geniculate nucleus, layers that are likely to contain neurons previously classified as Y-cells. Of the two layers that contain W-cells, layer 3 was unlabeled and layer 6 was lightly labeled. In area 17, layer 3c was densely stained, as in cats and macaque monkeys. The external half of layer 5 was also densely stained, in contrast to cats where the internal half of layer 5 is stained and macaques where layer 5 is sparsely stained. Area 18 was characterized by dense, uniform staining of inner layer 3 and outer layer 5, but no pattern of alternating light and dense bands crossed the width of area 18 as in macaques. Dense labeling of these same sublayers occurred in cortical areas TA and TD just lateral to area 18. Area TD may be the homologue of area MT of primates, which also stains densely with Cat-301 in macaques. These results indicate that Cat-301 differentially labels layers and areas in the visual system of tree shrews, and raise intriguing issues of comparison among tree shrews, primates, and cats.

To establish the topography of the lateral division of the lateral posterior region (LP1) projections to area 18, up to five different anatomical tracers were injected in separate rostrocaudal locations in area 18 of four adult cats, and patterns of retrogradely labeled LP1 cells were identified. LP1 inputs to area 18 arose from both caudal and rostral nuclei and were topological, organized in patterns that indicate that lower visual space is represented anteroventrally, and more central and upper visual space is represented caudodorsally. In the caudal LP1 nucleus, patches of labeled cells formed bands that ran parallel to the medial and lateral LPI borders and encompassed medial portions of the nucleus. In rostral LP1, the patches of labeled cells formed clusters giving the connections with area 18 a more modular appearance, and were nearer the lateral LP1 border. Injections made nearest area centralis representations in area 18 labeled more neurons than injections in cortex representing more peripheral visual space. Also, neighboring injections in area 18 labeled overlapping patches of cells, but no double-labeled cells were observed. These findings are consistent with previous conclusions based on electrophysiological mapping studies, that two retinotopically organized nuclei constitute LP1.

To characterize the postnatal development of geniculocortical axon arbor morphology in owl monkeys at a series of ages from birth to adulthood, individual arbors were bulk-filled with HRP in brain slice preparations and were reconstructed from serial sections. At all ages, cortical layers and sublayers were obvious. Presumed M or magnocellular arbors were largely confined to layer IVα, but they also extended into layer IIIc (IVB of Brodmann, 1909); presumed P or parvocellular arbors were almost exclusively confined to layer IVβ. Other axons that may reflect feedback projections from MT terminated in layer IIIc. Overall, M axon arbors increased in size and complexity from birth to adulthood with mean surface-view arbor areas ranging from 0.08 ± 0.01 mm2 in newborns to 0.24 ± 0.02 mm2 in adults. The developing P arbor areas were, on average, as large or larger than adult (newborn = 0.07 ± 0.01 mm2, adult = 0.047 ± 0.01 mm2; n.s.) but the arbors were somewhat less complex. Since the brain and area 17 increase in size postnatally, the proportion of area 17 subserved by each P arbor would decrease in postnatal development. Terminal boutons with immature features were evident in both M and P populations at all developmental ages. The results indicate that, while both LGN axon types in monkeys undergo morphological changes postnatally, M arbors appear to mature by increasing arbor size and terminal branching complexity, whereas P arbors increase in complexity but not in size. These distinct programs of axon arbor development suggest that the periods of susceptibility of geniculocortical axon arbors to postnatal influences of the environment, and the types of plastic responses they potentially exhibit, are class-specific.

The middle temporal visual area, MT, is one of three major targets of the primary visual cortex, area 17, in primates. We assessed the contribution of area 17 connections to the responsiveness of area MT neurons to visual stimuli by first mapping the representation of the visual hemifield in MT of anesthetized owl monkeys with microelectrodes, ablating an electrophysiologically mapped part of area 17, and then immediately remapping MT. Before the lesions, neurons at recording sites throughout MT responded vigorously to moving slits of light and other visual stimuli. In addition, the relationship of receptive fields to recording sites revealed a systematic representation of the contralateral visual hemifield in MT, as reported previously for owl monkeys and other primates. The immediate effect of removing part of the retinotopic map in area 17 by gentle aspiration was to selectively deactivate the corresponding part of the visuotopic map in MT. Lesions of dorsomedial area 17 representing central and paracentral vision of the lower visual quadrant deactivated neurons in caudomedial MT formerly having receptive fields in the central and paracentral lower visual quadrant. Most neurons at recording sites throughout other parts of MT had normal levels of responsiveness to visual stimuli, and receptive-field locations that closely matched those before the lesion. However, neurons at a few sites along the margin of the deactivated zone of cortex had receptive fields that were slightly displaced from the region of vision affected by the lesion into other parts of the visual field, suggesting some degree of plasticity in the visual hemifield representation in MT. Subsequent histological examination of cortex confirmed that the lesions were confined to area 17 and the recordings were in MT. The results indicate that the visually evoked activity of neurons in MT of owl monkeys is highly dependent on inputs relayed directly or indirectly from area 17.

Architectonic subdivisions of the inferior pulvinar (PI) complex were delineated in New World owl and squirrel monkeys and Old World macaque monkeys. Brain sections were processed for Nissl substance, myelin, cytochrome oxidase (CO), acetylcholinesterase (AChE), calbindin-D28K (Cb), or with the monoclonal antibody Cat-301. In all three primates, we identified the posterior nucleus (PIp) and the medial nucleus (PIm) of previous reports, and divided the previously recognized central nucleus (PIc) into two subdivisions, medial (PIcm) and lateral (PIcl). Each nucleus had several features that allowed it to be readily distinguished. (1) PIp was dark in Cb, and moderately dark in AChE and CO preparations. (2) PIm was Cb light, and AChE and CO dark. (3) PIcm was Cb dark, and AChE and CO light. (4) PIcl was Cb moderate with a scattering of dark neurons, and moderately dark for AChE and CO. (5) In sections processed for Cat-301, PIm in macaque monkeys and PIcm and PIp in squirrel monkeys stained darkly, while little staining was apparent in owl monkeys. The results allowed subdivisions of the inferior pulvinar to be more clearly defined, homologized, and compared across taxa. All monkeys appear to have the same four subdivisions of the PI, although properties vary.

The goal of the present study was to determine the ascending sources to the pre-supplementary motor area (pre-SMA) in macaque monkeys using multiple labeling techniques. We labeled the pallidothalamic projections using biotinylated dextran amine (BDA) and the cerebellothalamic projections using wheatgerm agglutinin conjugated to horseradish peroxidase. The pre-SMA thalamocortical projections neurons were also labeled using cholera toxin subunit b following identification of the pre-SMA by location, and by movements evoked by intracortical microstimulation. The extent of pre-SMA was later confirmed by identifying characteristics from Nissl cytoarchitecture and SMI-32 immunoreactivity. Thalamic nuclear boundaries were based on Nissl cytoarchitecture, acetylcholinesterase chemoarchitecture and Cat-301 immunoreactivity. Cerebellothalamic afferents were distributed predominantly to ventral lateral posterior nucleus (VLp), including medial and dorsal VLp, while the pallidothalamic afferents projected more rostrally to ventral lateral anterior nucleus (VLa) and ventral anterior nucleus (VA). The pre-SMA thalamocortical projection neurons were primarily found in VA and medial VLp. However, scattered cells were also found in VLa, dorsal VLp, central lateral nucleus (CL) and mediodorsal nucleus (MD). Scattered pre-SMA projecting cells overlapped foci of cerebellar label in medial VLp. Additionally, limited overlap of pre-SMA cells and pallidothalamic labeling was found in caudal VA. These findings suggest that the pre-SMA is uniquely positioned to integrate ascending basal ganglia and cerebellar information after a relay from VA and medial VLp. These anatomical findings are consistent with the recent hypothesis that the pre-SMA acts as the coordinator of visual and motor loops in motor learning [J. Cogn. Neurosci. 13 (2001) 626].

Neither discrete peripheral retinal lesions nor the normal optic disk produces obvious holes in one's percept of the world because the visual brain appears to perceptually “fill in” these blind spots. Where in the visual brain or how this filling in occurs is not well understood. A prevailing hypothesis states that topographic map of visual cortex reorganizes after retinal lesions, which “sews up” the hole in the topographic map representing the deprived area of cortex (cortical scotoma) and may lead to perceptual filling in. Since the map reorganization does not typically occur unless retinotopically matched lesions are made in both eyes, we investigated the conditions in which monocular retinal lesions can induce comparable map reorganization. We found that following monocular retinal lesions, deprived neurons in cat area 17 can acquire new receptive fields if the lesion occurred relatively early in life (8 weeks of age) and the lesioned cats experienced a substantial period of recovery (>3 years). Quantitative determination of the monocular and binocular response properties of reactivated units indicated that responses to the lesioned eye for such neurons were remarkably robust, and that the receptive-field properties for the two eyes were generally similar. Moreover, excitatory or inhibitory binocular interactions were found in the majority of experimental units when the two eyes were activated together. These results are consistent with the hypothesis that map reorganization after monocular retinal lesions require experience-dependent plasticity and may be involved in the perceptual filling in of blind spots due to retinal lesions early in life.

Brain parts can scale independently of the whole brain, and an example is given to point out that the authors underestimate variation that can exist in brains of equal size.

Patterns of terminals labeled after WGA-HRP injections in the superior colliculus (SC) in squirrel monkeys and macaque monkeys, and after DiI application in marmosets, were related to the architecture of the pulvinar and dorsal lateral geniculate nucleus (LGN). In all studied species, the SC projects densely to two architectonic subdivisions of the inferior pulvinar, the posterior inferior pulvinar nucleus (PIp) and central medial inferior pulvinar nucleus (PIcm). These projection zones expressed substance P. Thus, sections processed for substance P reveal SC termination zones in the inferior pulvinar. The medial subdivision of the inferior pulvinar, PIm, which is known to project to visual area MT, does not receive a significant collicular input. Injections in MT of a squirrel monkey revealed no overlap between SC terminals and neurons projecting to area MT. Thus, PIm is not the significant relay station of visual input from the SC to MT. The SC also sends an input to the LGN, however, this projection is sparser than the input directed to pulvinar.