Bihemispheric Collateralization of the Cortical and Subcortical Afferents to the Rat's Visual Cortex

A fluorescent dye (usually fast blue or rhodamine tagged latex microspheres) was injected into cortical area 17 (or area 17 and the lateral part of area 18b) of adult and juvenile (15 - 22 day old) Sprague-Dawley albino rats. Another fluorescent dye (usually diamidino yellow) was injected into cortical areas 17, 18a and 18b of the opposite hemisphere. The injections involved only the cortical grey matter. After postinjection survival of 2 - 14 days the distribution of retrogradely labelled mesencephalic and prosencephalic cells was analysed. Both small and large injections labelled retrogradely a substantial number of cells in specific and nonspecific dorsal thalamic nuclei (lateral geniculate, lateral posterior, ventromedial, several intralaminar nuclei and nucleus Reuniens) as well as a small number of cells in the preoptic area of the hypothalamus and the mesencephalic ventral tagmental area (VTA). While labelled thalamic cells contained only the dye injected into the ipsilateral cortex, a small proportion of hypothalamic and VTA cells was labelled with the dye injected into the contralateral cortex. Virtually none of the cells in these areas were double labelled with both dyes. Both small and large injections labelled cells in the ipsilateral telencephalic magnocellular nuclei of the basal forebrain and the caudal claustrum. A substantial minority of labelled cells in these structures was labelled by the dye injected into the contralateral cortex. Furthermore, a small proportion (about 1%) of claustral cells projecting to the ipsilateral cortex were double labelled with both dyes. In several cortical areas ipsilateral to the injected area 17, associational neurons were intermingled with commissural neurons projecting to the contralateral visual cortex. A substantial proportion of associational neurons projecting to ipsilateral area 17 also projected to the contralateral visual cortex (associational-commissural neurons). Thus, in visual area 18a, the associational-commissural neurons were located in all laminae, with the exception of lamina 1 and the bottom of lamina 6, and constituted about 30% of the neurons projecting to ipsilateral area 17. In paralimbic association area 35/13, associational-commissural neurons were located in lamina 5 and constituted about 20% of neurons projecting to ipsilateral area 17. In the limbic area 29d, the associational-commissural neurons were located in laminae 4, 5 and the upper part of lamina 6 and constituted about 10% of the associational-commissural neurons projecting to ipsilateral area 17. In oculomotor area 8, double-labelled neurons were located in lamina 5 and constituted about 10% of the neurons projecting to ipsilateral area 17. Thus, it appears that the axons of mesencephalic and diencephalic neurons projecting to the visual cortex do not send collaterals into both hemispheres. The bihemispheric projection to the rat's visual cortex originates almost exclusively in the retinotopically organized cortical area 18a and in integrative cortical areas 35/13, 29d and 8.     

Bifurcation of subcortical afferents to visual areas 17, 18, and 19 in the cat cortex

We have examined the pattern of axon bifurcation in the thalamic and claustral afferents to visual areas 17, 18, and 19 in the adult cat neocortex. This was achieved by injecting two fluorescent retrograde tracers, fast blue and diamidino yellow, in retinotopically corresponding regions of two of these three cortical areas. The pattern of single- and double-labelled cells was then examined in subcortical structures and the presence of double-labelled cells was interpreted as indicating that these neurons send bifurcating axons to the two injected areas. The size of the cortical region surrounding the injection site where each fluorescent dye is taken up was studied by making side-by-side injections of the two tracers in area 17 and examining the size and the separation of the two groups of labelled cells in the lateral geniculate nucleus (LGN). From these experiments we conclude that the uptake region is smaller than 1 mm and is included in the region of dense coloring surrounding the track of the injection needle. Injections were made in cortical regions which were in retinotopic correspondence as determined by electrophysiological recording. The double-labelled neurons were always found in the zone of overlap of the two populations of colored cells and no double-labelled neurons were found when there was no overlap between these populations. This indicates that the bifurcating axons send branches to strictly retinotopically corresponding regions in the two cortical areas. After injections in areas 18 and 19, numerous double-labelled cells were observed in laminae C of the LGN, in the medial interlaminar nucleus (MIN), the posterior nucleus (PN), and the lateral part of the lateral posterior nucleus (LP), in the retinorecipient zone of the pulvinar (RRZ-Pul), the intralaminar nuclei (ILN), and the claustrum. The proportions of double-labelled cells with respect to the total number of labelled neurons were computed in the region of overlap of the two populations of labelled cells. These percentages ranged between 5 and 20% and were highest in the C laminae of the LGN, the intralaminar nuclei, and the claustrum. After injection of areas 17 and 18, similar proportions of double-labelled cells were observed in the same structures, as well as in the A laminae of the LGN. Here again, the intralaminar nuclei and the claustrum tended to have slightly higher (20-30%) proportions of double-labelled cells. When the nonadjacent areas 17 and 19 were injected, doubled-labelled neurons were also observed in all these structures, except the A laminae of the LGN.(ABSTRACT TRUNCATED AT 400 WORDS)     

The projection from the lateral geniculate nucleus onto the visual cortex in the cat. A quantitative study with horseradish-peroxidase

Horseradish-peroxidase (HRP) was injected (9-18 μg in 0.03-0.06 μl) into cortical areas 17, 18 or 19 of 11 adult cats. After survival times of 17 hours to 7 days, the thalamus was examined for retrogradely HRP labelled nerve cells in serial transverse sections. From these sections, the percentage of labelled cells occurring in each subdivision of the dorsal lateral geniculate nucleus (LGNd) was calculated for each animal. One case each for injections in areas 17, 18 and 19 was then chosen for nerve cell size measurements in each LGNd subdivision. The peri-karyal area of each labelled cell (N=689), and of representative samples of unlabelled cells (N=1137), was measured by planimetry. Size distribution histograms, mean values, standard deviations, and statistical significance levels were obtained by computer. It was found that area 17 receives a projection almost exclusively from laminae A and Al, and that the projecting cells belong to all cell size classes. Area 18 receives a projection mainly from laminae C and Al, and from the medial interlaminar nucleus (MIN). The projecting cells belong mainly to the large cell size classes. Area 19 receives a projection largely from MIN, and also from the C-laminae and extrageniculate cell groups. The projecting cells belong to all cell size classes, with some emphasis on the large cells of lamina C. A significant projection was found to exist from the parvocellular laminae of LGNd onto area 19 and, to a lesser degree, area 18. In conclusion, as one goes from area 17 to 18 and to 19 the projection source shifts from the A-laminae through the C-laminae on to MIN and extrageniculate cell groups. The cells which project to area 18 are on the whole larger, than those which project to areas 17 and 19. A significant proportion of the contralateral visual input to area 18 is relayed via lamina G. These results provide a quantitative confirmation and extension of previous anatomical findings, and are in close relationship with physiological results regarding parallel channel processing in the visual system.     

Cortical projections of the lateral geniculate nucleus in the cat

A new application of the retrograde transport method designed to demonstrate neurons that project to two cortical areas has been developed. This method depends on the retrograde axonal transport of two markers, each of which is uniquely detectable by histological methods. In this study, horseradish peroxidase (detectable by the enzymatic reation product only) and tritiated proteins (either enzymatically inactive tritiated horseradish peroxidase or tritiated bovine serium albumin, both of which are detectable by the tritium label only) were used. One of these markers was injected into cortical area 17 and the other was injected into area 18. In layers A and A₁ of the lateral geniculate nucleus, 10% of the cells project to both area 17 and area 18 by axons that branch, 70% of the neurons project to area 17 only, less than 1% of the neurons project to area 18 only, and approximately 20% of the cells are probably interneurons. In the C laminae 50% of the cells project to both areas 17 and 18 by axons that branch, approximately 20% of the neurons project to area 17 only, 10% of the cells project to area 18 only, and about 20% of the neurons are unlabeled. The cells in the medial interlaminar nucleus project to area 17 only, to area 18 only, or to both of these areas by axons that branch. In addition the retrograde markers were injected into single cortical areas, either area 17, area 18, or area 19. The injections of area 17 and those of area 18 confirmed the results of the double-label experiments, with 80% of the cells in the A laminae projecting to area 17 and approximately 10% projecting to area 18. Following injections of area 19, labeled neurons were seen in the medial interlaminar nucleus and the C laminae. Therefore, the medial interlaminar nucleus contains cells that project to areas 17, 18, and 19, with some cells projecting to both area 17 and area 18 by axons that branch. In the C laminae the analysis of the projection pattern could be carried further, for it was possible to determine the percentage of labeled neurons in this region. Since 80% of the cells project to areas 17 and 18, and since 60% of the cells of the C laminae were labeled following injections of area 19, many of the cells which project to area 19 must also project to either area 17 or area 18, and some cells must project to all three (areas 17, 18, and 19) by branching axons.     

The Incidence of Bifurcation Among Corticocortical Connections from Area 17 in the Developing Visual Cortex of the Cat

In newborn kittens, cells in the striate cortex (visual area 17) that project to area 18 (part of extrastriate cortex) are distributed with uniform density in the superficial and in the deep layers. During postnatal weeks 2 – 3, some of these corticocortical connections are removed to generate an adult-like projection in which association cells are clustered mainly in the superficial layers of area 17. Axonal elimination, without cell death, is the major factor sculpting patches of corticocortical cells in superficial layers. In adult cats, few cells in area 17 (∼5%) have axons that bifurcate to multiple extrastriate areas. We have studied the possibility that the early exuberant innervation of area 18 by neurons in area 17 is largely from the transient collaterals of axons that also project to other visual areas. Kittens aged 2 – 21 days were each injected with a pair of retrogradely transported tracers, either diamidino yellow and fast blue, or diamidino yellow and a carbocyanine dye, at retinotopically corresponding points in area 18 and either area 19 or the posteromedial lateral suprasylvian cortex (PMLS). As for injections in area 18, those in area 19 and PMLS in kittens aged ≥5 days labelled cells in continuous bands in area 17; in older kittens neurons projecting from area 17 to extrastriate regions were in patches, mainly in superficial layers. In each animal, the labelling from the two injections overlapped by 51–92%. However, at all ages, never more than 4% of cells projecting to area 18 branched to PMLS; ≤6% of area 17-to-18 cells bifurcated to area 19 in kittens aged ≥15 days, although slightly more (10 – 12%) did so at 3 – 5 days. Thus, as in adults, we found no evidence of frequent collateralization among the axons of cells projecting from area 17 to other extrastriate areas in kittens.     

Spatial-frequency tuning and geniculocortical projections in the visual cortex (areas 17 and 18) of the pigmented ferret

We have examined the spatial-frequency selectivity of neurons in areas 17 and 18 of the adult pigmented ferret, by measuring how the amplitude of response depends on the spatial-frequency of moving sinusoidal gratings of optimal orientation and fixed contrast. Neurons in area 17 of the ferret respond optimally to low spatial frequencies [average 0.25 cycles per degree (c/deg)], much lower than the optima for cat area 17. The tuning curves are of the same form as those found in cat and monkey: unimodal with bandwidths in the range 0.8–3.5 octaves. Neurons in area 18 of the ferret respond optimally to even lower spatial frequencies (average 0.087 c/deg) than area 17 neurons, and the distributions of optimal spatial frequency for areas 17 and 18 hardly overlap. In both cortical areas, the bandwidth of the tuning curves is inversely correlated with optimal spatial frequency. This marked difference in tuning between the two cortical areas is probably attributable to differential geniculo-cortical projections. Small injections of fluorescent latex microspheres or horseradish peroxidase (HRP) were made into area 17 or area 18 in order to investigate the populations of geniculate neurons projecting to the two cortical areas. After injections into area 17, labelled neurons are found predominantly in the geniculate A layers, with a few neurons labelled in the C layers. Conversely, after an area 18 injection, similar numbers of labelled neurons are found in the C layers as in the A layers. Soma-size analysis of the neurons in the A-layers suggests the existence of two populations of relay neurons, which project differentially to areas 17 and 18. The different geniculate inputs and the different spatial-frequency tuning in areas 17 and 18 may imply that the two cortical areas process visual information more in parallel than in series.     

Laminar origins of visual corticocortical connections in the cat

The interconnections among visual areas in cat cortex were studied with respect to the specific laminae in which the cortically projecting neurons are located. Single injections of HRP were made through recording micropipettes into nine different visual areas. In 15 cortical areas the laminar distribution of neurons which were retrogradely filled with HRP was plotted. In this way we determined the laminar origins of the cortical projections to the nine separate cortical visual areas which were injected. There are three major observations. First, areas 17 and 18 are the only two visual areas in which layers II and III are the primary site of cortically projecting cells; in the other 13 areas the deeper layers of cortex provide a large percentage of such neurons. Second, within any one cortical area, cortically projecting neurons may be distributed among different layers; the specific layer depends upon the cortical target of those neurons. Third, any one cortical area receives projections from several different cortical layers, the specific layers being dependent upon the area from which the projection originates. An individual cortical area, therefore, contributes to several different cortical visual circuits, with each of these circuits defined by the laminar connections of its neurons.     

Localization of last-order premotor interneurons in the lumbar spinal cord of rats

There is strong evidence that neural circuits underlying certain rhythmic motor behaviors are located in the spinal cord. Such local central pattern generators are thought to coordinate the activity of motoneurons through specific sets of last-order premotor interneurons that establish monosynaptic contacts with motoneurons. After injections of biotinylated dextran amine into the lateral and medial motor columns as well as the ventrolateral white matter at the level of the upper and lower segments of the lumbar spinal cord, we intended to identify and localize retrogradely labelled spinal interneurons that can likely be regarded as last-order premotor interneurons in rats. Regardless of the location of the injection site, labelled interneurons were revealed in laminae V–VIII along a three- or four-segment-long section of the spinal gray matter. Although most of the stained cells were confined to laminae V–VIII in all cases, the distribution of neurons within the confines of this area varied according to the site of injection. After injections into the lateral motor column at the level of the L4–L5 segments, the labelled neurons were located almost exclusively in laminae V–VII ipsilateral to the injection site, and the perikarya were distributed throughout the entire mediolateral extent of this area. Interneurons projecting to the lateral motor column at the level of the L1–L2 segments were also located in laminae V–VII, but most of them were concentrated in the middle one-third or in the lateral half of this area. Following injections into the medial motor column at the level of the L1–L2 segments, the majority of labelled neurons were confined to the medial aspect of laminae V–VII and lamina VIII, and the proportion of neurons that were found contralateral to the injection site was strikingly higher than in the other experimental groups. The results suggest that the organization of last-order premotor interneurons projecting to motoneurons, which are located at different areas of the lateral and medial motor columns and innervate different muscle groups, may present distinct features in the rat spinal cord. J. Comp. Neurol. 389:377–389, 1997. © 1997 Wiley-Liss, Inc.     

Effects of early monocular eyelid suture upon development of relay cell classes in the cat's lateral geniculate nucleus

Horseradish peroxidase (HRP) was injected into visual cortex of four normal cats and five cats raised with monocular lid suture, and retrograde labelling was assessed in cells of the lateral geniculate nucleus. In all but one of the sutured cats (noted below) focal injections were carefully limited to area 17 or 18 and analysis of labelling focused on laminae A and A1. The effects of deprivation were indistinguishable whether lamina A or A1 was deprived, and in all cases, the nondeprived laminae had labelling essentially identical to that seen in normal cats. After area 17 injections (bilateral in one normal cat and unilateral in 3 deprived cats), roughly 77% of the cells in nondeprived laminae were labelled and they were mostly small to medium in size. Deprived laminae, when compared to nondeprived laminae, had two abnormalities: (1) cells, both labelled and unlabelled, were smaller; and (2) roughly 11% fewer cells (i.e., 66%) were labelled, and this represents a small but statistically significant difference for each cat. After area 18 injections (bilateral in one normal cat plus unilateral in 3 other normal and 3 deprived cats), roughly 15% of the cells in nondeprived laminae were labelled, and they tended to be large in size. Deprived laminae, when compared to nondeprived laminae, had three abnormalities: (1) only 5–6% of the cells were labelled, and these tended to be quite faintly labelled; (2) the volume occupied by labelled cells was small; and (3) both labelled and unlabelled cells were reduced in size. Finally, large bilateral injections were made throughout occipitotemporal cortex in one lid sutured cat in an effort to label completely the terminal zones of cells in the medial interlaminar nucleus (MIN), a division of the lateral geniculate nucleus; this cat also had a prior intraocular injection of tritiated proline to provide through subsequent autoradiography a delineation of deprived and nondeprived portions of MIN. Roughly 78% of the cells in nondeprived portions of MIN were labelled in this cat. In the deprived portions, only about 51% of the cells were labelled, and these tended to be faintly labelled. Also, labelled cells were smaller, and unlabelled cells were larger in deprived than they were in nondeprived portions. Since prior studies have shown that, within the A laminae, X-cells project exclusively to area 17 whereas the Y-cell population projects to areas 17 and 18, these data are taken as further support of the conclusion that geniculate Y-cells are more seriously affected by the early deprivation than are geniculate X-cell. That is, these data are consistent with the suggestion that a similar population of Y-cells in deprived laminae (roughly 10% of the overall cell total) fail to transport HRP from area 17 or area 18 injections. This can be extended to the MIN, which seems to be comprised nearly exclusively of Y-cells. However, these conclusions must be considered tentative, since interpretation of HRP data can be difficult as evidenced by discrepancies in the literature.     

Origin of ascending intratrigeminal pathways in the cat

The retrograde horseradish peroxidase technique was used to locate neurons projecting to rostral trigeminal areas via ascending intranuclear pathways. After rostral trigeminal injections, labeled neurons were found in the subnucleus interpolaris and in all laminae of the medullary dorsal horn. Most neurons were labeled ipsilaterally in laminae III and IV, but some small neurons were labeled in lamina II in the medullary dorsal horn. The distribution of labeled cells suggested that these projections are topographically arranged. Labeled neurons were found in lamina I and lamina V, bilaterally; this was especially true if the parabrachial complex was included in the injection.     

Morphology and distribution of retinal ganglion cells projecting to different layers of the dorsal lateral geniculate nucleus in normal and Siamese cats

Electrophoretic injections of horseradish peroxidase were made into physiologically characterized sites within the different layers of the dorsal lateral geniculate nuclei (LGNd) of normal and Siamese cats. The histochemical procedures used stained the cell bodies, dendrites, and axons of retrogradely labeled ganglion cells. In both normal and Siamese cats, only alpha and beta ganglion cells are labeled by injections restricted to the A laminae. In normal cats, the alpha/beta ratios (number of labeled alpha cells/number of labeled alpha + beta cells) resulting from injections into lamina A increase from about 0.045 at 0.5 mm from the area centralis to about 0.12 in the far periphery. The alpha/beta ratios observed outside of the area centralis in normal cats following injections into different parts of lamina A1 were lower at each eccentricity than those resulting from injections into corresponding parts of lamina A. Also, the cell bodies and dendritic fields of alpha and beta cells projecting to lamina A1 are somewhat larger than those projecting to corresponding parts of lamina A. Outside of the area centralis, the relative numbers of alpha and beta cells projecting to Siamese lamina A are normal. However, alpha cells comprise an abnormally small proportion of ganglion cells projecting to the normal segments of Siamese lamina A1 and an abnormally large proportion of cells projecting to the abnormal segments of lamina A1. In Siamese cats, alpha and beta cells projecting to lamina A1 are distributed continuously throughout virtually all of the ipsilateral and contralateral temporal retinas. Since large parts of the ipsilateral and contralateral hemifields are not represented in Siamese lamina A1, it seems that some of the retinal afferents to this lamina are being suppressed. Injections into the C laminae of the LGNd show that the same morphological classes of ganglion cells project to these laminae in normal and Siamese cats. The classes projecting to the contralateral as C laminae (laminae C and C2) include alpha, beta, gamma, and epsilon as well as two other groups of cells referred to g1 and g2 cells, gamma, epsilon, g1, and g2 cells project to the ipsilateral C lamina (lamina C1). In siamese, but not in normal cats, examples of all of these types are found far into the contralateral temporal retina following injections involving lamina C1. This indicates that all classes projecting to the ipsilateral C lamina misproject in Siamese cats.     

The origin of efferent pathways from the primary visual cortex,area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase

The retrograde transport of horseradish peroxidase has been used to identify efferent cells in area 17 of the macaque. Cells projecting to the lateral geniculate nucleus are small to medium sized pyramidal neurons with somata in lamina 6 and the adjacent white matter. The projection to the parvocellular division arises preferentially from the upper half of lamina 6, while that to the magnocellular division arises preferentially from the lower part of the lamina. The projection to both superior colliculus and inferior pulvinar arises from all sizes of pyramidal neurons lying in lamina 5B (Lund and Boothe, '75); at least the largest pyramidal neurons of lamina 5B send collateral axon branches to both destinations. Injections with extensive spread of horseradish peroxidase show that many cells of lamina 4B and the large pyramidal neurons of upper lamina 6 also project extrinsically but their terminal sites have not been identified. Other studies have indicated that cells of laminae 2 and 3 project to areas 18 and 19. Therefore every lamina of the visual cortex, with the exception of those receiving a direct thalamic input, contains cells projecting extrinsically. Further, each lamina projects to a different destination and from Golgi studies can be shown to contain cells with specific patterns of dendritic branching which relate to the distribution of thalamic afferents and to the patterns of intracortical connections. These findings emphasise the significance of the horizontal organisation of the cortex with relation to the flow of information through it and contrast with the current concept of columnar organisation shown in physiological studies.     

Transient projections from the lateral geniculate to the posteromedial lateral suprasylvian visual cortex in kittens

The postnatal maturation of the projection from the lateral geniculate nucleus to the posteromedial lateral suprasylvian visual cortex (PMLS) was studied with injections of fluorescent dyes into the PMLS at various postnatal ages. Labeled neurons projecting to the PMLS were present in all laminae of the ipsilateral lateral geniculate on the day of birth. However, there was a conspicuous change in the distribution of labeled geniculo-PMLS neurons by 11 days of age: now very few labeled neurons were present in lamina A, indicating a loss of geniculo-PMLS connections. The loss of connections began at the peripheral margins of lamina A and proceeded through other laminae toward laminae C1-3. By adulthood, labeled geniculo-PMLS neurons were largely confined to laminae C1-3; they were never observed in lamina A or A1 and were rarely observed in lamina C. To determine whether the lateral geniculate neurons survived after their projections to PMLS were lost, injections of fast blue were made at 1 or 2 days postnatally and the animals were allowed long postinjection survival times. Labeled neurons were found in all lateral geniculate laminae, thereby indicating that for many neurons the loss of connections could be attributed to a loss of their axon collaterals rather than to the death of the neurons themselves. After injections of fast blue into the PMLS and diamidino yellow dihydrochloride into area 17 shortly after birth, many double-labeled neurons were present in all laminae, indicating that they have collaterals to both targets. Thus, the survival of many of the geniculo-PMLS neurons contributing to the transient geniculo-PMLS projection seems to be due to sustaining collateral projections to area 17 or other cortical targets.     

Characterization of transient cortical projections from auditory, somatosensory, and motor cortices to visual areas 17, 18, and 19 in the kitten

We have examined the anatomical features of ipsilateral transient cortical projections to areas 17, 18, and 19 in the kitten with the use of axonal tracers Fast Blue and WGA-HRP. Injections of tracers in any of the three primary visual areas led to retrograde labeling in frontal, parietal, and temporal cortices. Retrogradely labeled cells were not randomly distributed, but instead occurred preferentially at certain loci. The pattern of retrograde labeling was not influenced by the area injected. The main locus of transiently projecting neurons was an isolated region in the ectosylvian gyrus, probably corresponding to auditory area A1. Other groups of transiently projecting neurons had more variable locations in the frontoparietal cortex. The laminar distribution of neurons sending a transient projection to the visual cortex is characteristic and different from that of parent neurons of other cortical pathways at the same age. In the frontoparietal cortex, transiently projecting neurons were located mainly in layer 1 and the upper part of layers 2 and 3. In the ectosylvian gyrus, nearly all the neurons are located in layers 2 and 3. In addition, a few transiently projecting neurons are found in layer 6 and in the white matter. Transiently projecting neurons have a pyramidal morphology except for the occasional spindle-shaped cell of layer 1 and multipolar cells observed in the white matter. Anterograde studies were used to investigate the location of transient fibers in the visual cortex. Injections of WGA-HRP at the site of origin of transient projections gave rise to few retrogradely labeled cells in areas 17, 18, and 19, demonstrating that transient projections to these areas are not reciprocal. Although labeled axons were found over a wide area of the posterior cortex, they were more numerous over certain regions, including areas 17, 18, and 19, and absent from other more lateral cortical regions. Transient projecting fibers were present in all cortical layers at birth. Plotting the location of transient fibers in numerous sections and at all ages showed that these fibers are not more plentiful in the white matter than they are in the gray matter. We found no evidence that the white/gray matter border constituted a physical barrier to the growth of transient axons. Comparison of the organization of this transient pathway to that of other transient connections is discussed with respect to the development of the cortex.     

The patterns of projection of cortical areas 17, 18, and 19 onto the laminae of the dorsal lateral geniculate nucleus in the cat.

The projection of cortical areas 17, 18, and 19 onto the laminar part of the dorsal lateral geniculate nucleus was investigated with degeneration methods and with the autoradiographic axon tracing method. In agreement with previous accounts, degenerating cortical axons stained by the Nauta method were restricted to laminae A, A1, C and to the interlaminar zones. In contrast, adjacent sections stained with the Fink-Heimer method showed fine dust like degeneration throughout all of the laminae of the nucleus. Comparisons of Fink-Heimer degeneration resulting from lesions of area 17 with that resulting from lesions of areas 18 and 19 further suggested that the area ) projection is heavier and more uniform than the projections from areas 18 and 19. Autoradiographic tracing of axons after intracortical injections of 3H-proline provided detailed demonstrations of the cortical projection patterns that confirmed the Fink-Heimer results. Following restricted injections of areas 17 or 18 the termination zones in the dorsal lateral geniculate nucleus consisted of columns of labeled tissue oriented perpendicular to the laminae of the nucleus. Area 17 was found to project heavily and uniformly throughout all of the laminae of the nucleus. The projection from area 18 also extended throughout all of the laminae of the nucleus, but was sparser and less uniformly distributed than that from area 17. Projections from area 18 distributed more heavily to the interlaminar zones and to lamina C than to laminae A, A1 C1, C2 or C3. A projection from area 19 to laminae C1, C2 and C3 was also demonstrated autoradiographically.     

Organization of association projections from area 17 to areas 18 and 19 and to suprasylvian areas in the cat's visual cortex.

Cells in area 17 that are labelled by single, discrete injections of retrogradely transported tracers into extrastriate visual areas are discontinuously distributed in dense patches. In this study we made multiple, closely spaced injections of fluorescent dyes into extrastriate areas, to generate large deposits that would reveal whether the distributions of corticocortical cell bodies in area 17 are truly patchy or appear clustered only after small injections. By injecting a different tracer into each extrastriate area, or group of areas, we examined the spatial relationships between the populations of association cells. All deposits of tracers in areas 18, 19, or suprasylvian cortex, irrespective of size, label cells in a series of clusters in topographically related parts of area 17. We conclude that the complete populations of cells in area 17 that project to areas 18, 19, and the lateral suprasylvian cortex are all genuinely distributed in a patchy fashion. There appears to be a complex relationship between the sets of association cells projecting to different extrastriate regions: they do not completely overlap, only partially, and share some cortical zones but not others. In these experiments, only tiny percentages (2-5%) of labelled cells in the overlapping regions were filled with both tracers, suggesting that very few association cells in area 17 project to more than one of the extrastriate areas we studied. By comparing the dimensions of each injection site and of the labelled region in area 17, we estimated the extent of the convergence from area 17 to areas 18, 19, and posteromedial suprasylvian areas in retinotopic terms. The functional convergence was very similar in these pathways.     

Corticofugal projections from the visual cortices to the thalamus, pretectum and superior colliculus in the cat

Small lesions were placed in visual cortical areas 17, 18, 19, 20, 21, 7, and Clare-Bishop in the cat, and the sites of terminal degeneration seen with Fink-Heimer technique were plotted in thalamus, pretectum and superior colliculus. No degeneration was found in these sites after area 20 lesions; lesions in the other cortical areas gave different patterns of degeneration. Two major patterns were present, one from lesions in 17–18, one from lesions in 21, 7 and C-B, with degeneration from 19 forming a transition between the two groups. Areas 17, 18 and 19 project to the dorsolateral geniculate nuclear complex (LGN_d); areas 21, C-B and 7 do not. Area 17 projects to the laminar part, area 18 to both laminar and interlaminar (NIM) parts, and 19 only to NIM. The corticogeniculate projections from all three areas are topically organized anteroposteriorly, and at least that from area 17 is topically organized mediolaterally. Areas 17 and 18 project topically to a columnar locus of the medial pulvinar (=lateral posterior) nucleus which ventrally includes that area known as the posterior nucleus. Area 19 has a double columnar projection to this part of the thalamus, one in the medial and one in the lateral pulvinar area. The medial column lies medial to that from 17–18, and appears to overlap the termination of the ascending projection from the superior colliculus. Cortical areas 21, C-B and 7 also have a double projection to the pulvinar. These findings indicate that the corticorecipient neurons in both medial and lateral sectors of the pulvinar are organized so that dorsal neurons are activated by stimuli in upper visual fields (lower retina) and ventral neurons by stimuli in lower fields (upper retina). Areas 17 and 18 project to the external layer of the ventrolateral geniculate (LGN_v) nucleus, 19 to both external and internal layers, and 21, C-B and 7 to internal layer only. The pretectal projection from 17–18 is limited to its caudal pole chiefly in the posterior pretectal nucleus (NPP), and also in the nucleus of the optic tract (NOT). Area 19 fibers terminate in NPP, NOT and also in the reticular part of the anterior pretectal nucleus (NPA_r). Those from 21 and C-B end primarily in NPA_r, and from area 7 in both reticular and compact parts of NPA. These corticopretectal systems all appear to be organized topically. Areas 17, 18 and 19 have a double termination in the superior colliculus, a focal pattern in the superficial layers (chiefly lamina II), and a diffuse pattern in deeper layers (laminae IV, V, VI). The superficial pattern only provides the retinotopical matching with the optic afferents. All other cortical areas project diffusely to the deep layers. After lesions in 21 and C-B, the superficial foci are larger and centered in lamina III; after area 7 lesions this focal degeneration is centered in laminae III and IV and spread over much of the width of the colliculus. Degeneration to pontine nuclei and inferior olive was not examined.     

The projection of the lateral geniculate nucleus to area 18

The present study is concerned with the projection of the lateral geniculate nucleus onto cortical area 18. Horseradish peroxidase (HRP) was injected into area 18 of 15 cats. Drawings were made to determine the location of the injection site and the distribution of labeled neurons in the lateral geniculate nuclei of each cat. The local retinotopic maps constructed prior to the injections and the reconstructions of the lateral geniculate nucleus were used to determine the location and the extent of each of the HRP injections. In 15 of the 25 hemispheres studied, the ratio of the number of HRP-labeled neurons in lamina A relative to the number of labeled neurons in lamina A1 was calculated. This ratio varied from 1.06 to 0.28, indicating that at least some regions of area 18 are dominated by inputs from lamina A1. However, if the HRP-labeled neurons in lamina C are included in the counts for lamina A, then the ratio A + C/A1 has a mean of 1.11, suggesting that area 18 receives a balanced input, with inputs from the contralateral eye being relayed through laminae A and C, and inputs from the ipsilateral eye being relayed through lamina A1. When the distribution of HRP-labeled neurons in lamina A was plotted onto a dorsal view of the lateral geniculate nucleus, the labeled neurons formed an ellipse with the long axis of the ellipse oriented parallel to the isoelevation lines. The representation of azimuth is compressed in area 18 relative to the lateral geniculate nucleus. In six hemispheres the injections were restricted to a few layers of the area 18. Following small injections into layer IV of area 18, the HRP-labeled neurons occupied an extensive region of the lateral geniculate nucleus, indicating a considerable amount of convergence of the inputs to area 18. In hemispheres where the injections were restricted to layers I and II, labeled neurons were only seen in the medial interlaminar nucleus and the C laminae.     

Cortical projections to the superior colliculus in the macaque monkey: A retrograde study using horseradish peroxidase

The topical and laminar distribution of corticotectal cells, as well as their size and morphology, were studied in the macaque monkey with the horseradish peroxidase (HRP) technique. After HRP injections restricted primarily to the superficial layers of the colliculus, labelled cells were found in visual cortex (areas 17, 18, and 19) and both in the frontal eye field (area 8) and the adjacent part of premotor cortex (area 6). The clustering of labelled cells in visual cortex indicated that each of the anatomically and functionally distinct visual areas has its own set of collicular projections. When intermediate and deeper layers of the colliculus were injected, labelled cells were found also in posterior parietal cortex (area 7) where they were concentrated mainly on the posterior bank of the intraparietal fissure, in inferotemporal cortex (areas 20 and 21), in auditory cortex (area 22), in the somatosensory representation SII (anterior bank of sylvian fissure, area 2), in upper insular cortex (area 14), in motor cortex (area 4), in premotor cortex (area 6), and in prefrontal cortex (area 9). In the motor and premotor cortex, labelled cells formed a continuous band which appeared to stretch across finger-hand-arm-shoulder-neck representation. Similarly, the cluster of labelled cells in area 2 may correspond to the finger-hand representation of SII. The cortical regions not containing labelled cells were the somatosensory representation SI (areas 3, 1 and 2) and the infraorbital cortex. Labelled cells were restricted to layer V of all cortical areas except in the primary visual cortex, where labelled cells were found in both layer V and layer VI. The size spectrum of corticotectal cells ranged from 14.8 μm (average diameter) in area 17 to 27.8 μm in area 6, comprising cells as small as 8 μm and as large as 45 μm. Labelled cells in posterior parietal (area 7), in auditory (area 22), and in motor cortex (area 4) were small and distributed over only a narrow range of sizes. Those in premotor cortex (area 6) were often large and had a wide range in size distribution. The differences in size and morphology of corticotectal neurons suggest that they do not form a uniform class of neurons.     

The postnatal development of the association projection from visual cortical area 17 to area 18 in the cat

The postnatal development of the association projection from area 17 to area 18 was studied in normal and binocularly deprived kittens between 1 and 28 days of age, using retrograde transport of horseradish peroxidase conjugated with wheat germ agglutinin. The positions of injection sites in the visual cortex, defined in relation to the borders of visual areas 17, 18, and 19 located in Nissl- and cytochrome oxidase-stained sections, were confirmed by observing the patterns of labeling of cells in the lateral geniculate nucleus. The association projection is present and is arranged at least roughly topographically from birth onward; at all ages it arises from cells in both the superficial layers (II, III, and the upper part of IV) and the deep layers (V and VI). In older kittens (20 days or more), however, the origin of the pathway is principally from the upper layers, as in adult cats, whereas in younger animals the projection arises roughly equally from cells in superficial and deep laminae. Initially, the association neurons in area 17 are distributed uniformly along each lamina. Periodic clustering of labeled cells in the upper layers can just be discerned at 10 days, and this patchiness has reached its adult clarity by 20 days, at which stage the projection from the lower layers is greatly diminished. Binocular deprivation until the age of 28 days did not prevent these developmental changes in the projection. Various controls established that the patterns of labeling seen in this study were not due to direct spread of tracer into area 17, to uptake of tracers by fibers-of-passage, or to transcellular transport via the thalamus.