Retrograde transport studies have shown that widespread areas of the cerebral cortex project upon the superior colliculus. In order to explore the organization of these extensive projections, the anterograde autoradiographic method has been used to reveal the distribution and pattern of corticotectal projections arising from 25 cortical areas. In the majority of experiments, electrophysiological recording methods were used to characterize the visual representation and cortical area prior to injection of the tracer. Our findings reveal that seventeen of the 25 cortical areas project upon some portion of the superficial layers (stratum zonale, stratum griseum superficiale, and stratum opticum, SO). These cortical regions include areas 17, 18, 19, 20a, 20b, 21a, 21b, posterior suprasylvian area (PS), ventral lateral suprasylvian area (VLS), posteromedial lateral suprasylvian area (PMLS), anteromedial lateral suprasylvian area (AMLS), anterolateral lateral suprasylvian area (ALLS), posterolateral lateral suprasylvian area (PLLS), dorsolateral lateral suprasyvian area (DLS), periauditory cortex, cingulate cortex, and the visual portion of the anterior ectosylvian sulcus. While some of these corticotectal projections target all superficial laminae and sublaminae, others are more discretely organized in their laminar-sublaminar distribution. Only the corticotectal projections arising from areas 17 and 18 are exclusively related to the superficial layers. The remaining 15 pathways innervate both the superficial and intermediate and/or deep layers. The large intermediate gray layer (stratum griseum intermedium; SGI) receives projections from almost every cortical area; only areas 17 and 18 do not project ventral to SO. All corticotectal projections to SGI vary in their sublaminar distribution and in their specific pattern of termination. The majority of these projections are periodic, or patchy, and there are elaborate (double tier, bridges, or streamers) modes of distribution. We have attempted to place these findings into a conceptual framework that emphasizes that the SGI consists of sensory and motor domains, both of which contain a mosaic of connectionally distinct afferent compartments (Illing and Graybiel, '85, Neuroscience 14:455-482; Harting and Van Lieshout, '91, J. Comp. Neurol. 305:543-558). Corticotectal projections to the layers ventral to SGI, (stratum album intermediale, stratum griseum profundum, and stratum album profundum) arise from thirteen cortical areas. While an organizational plan of these deeper projections is not readily apparent, the distribution of several corticotectal inputs reveals some connectional parcellation.
The distribution of cortical projections from areas 17, 18 and 19 to the lateral thalamus, pretectum, and superior colliculus was investigated with the autoradiographic tracing method. Cortical areas 17, 18 and 19 were demonstrated to project retinotypically and in register upon the dorsal lateral geniculate nucleus, medial interlaminar nucleus, lateral zone of the lateral posterior complex, nucleus of the optic tract and superior colliculus. Area 19 was shown to project retinotopically upon the pulvinar nucleus. Clear retinotopic organization was not demonstrable in the projections of areas 17, 18 and 19 to the reticular complex of the thalamus and ventral lateral geniculate nucleus, or in the projection of area 19 to the anterior pretectal nucleus. The cortical projections were employed to define the retinotopic organization of the nucleus of the optic tract, pulvinar nucleus, and later zone of the lateral posterior complex. The cortical projections show the vertical meridian to be represented caudally, with the lower visual field represented laterally, and the upper visual field medially, within the nucleus of the optic tract. The projections of area 19 to the pulvinar nucleus demonstrate the lower visual field to be represented rostrally and the upper field caudally in this mucleus; the vertical meridian to be represented at the lateral border and the visual field periphery to be represented at the medial border of the pulvinar nucleus. Cortical projections to the lateral zone of the lateral posterior complex demonstrate the lower visual field to be represented rostrally and the upper visual field caudally; the vertical meridian to be represented at the medial limit and the visual field periphery at the lateral border of the termination zones. On the basis of the experimental findings a new terminology is introduced for the feline lateral posterior complex. Divisions are proposed which correspond to zones with demonstrably distinct afferent input. The pulvinar nucleus is defined by the distribution of projections from area 19. Three flanking divisions are defined within the lateral posterior complex; a lateral division recipient of projections from area 17, 18 and 19, and interjacent division recipient of projections of the superficial layers of the superior colliculus, and a medial division flanking the tectorecipient zone medially.
The organization of extrastriate visual areas of the cat's posterior suprasylvian sulcus and gyrus was studied with electrophysiological mapping methods. Analysis of retinotopic organization confirmed the presence of dorsal lateral and ventral lateral suprasylvian (DLS, VLS) visual areas (Palmer et al., '78, J. Comp. Neurol. 177:237-256) and demonstrated new features of organization. Areas DLS and VLS occupy the upper two-thirds of the posterior suprasylvian sulcus, with DLS wholly confined to the upper bank and VLS straddling the sulcal fundus. Both areas contain a partial representation of the lower quadrant of the visual field. A narrow strip of visually responsive cortex (periauditory belt) was identified adjoining DLS on the posterior ectosylvian gyrus; its organization and extent were not explored in detail. The organization of the posterior suprasylvian areas (PS) (Updyke, '82, Soc. Neurosci. Abst. 8:810) was explored in detail. Area PS lies inferior to areas VLS and 21b in the lower third of the posterior suprasylvian sulcus and gyrus, extending onto the fusiform gyrus. PS contains a partial representation of the lower quadrant of the visual field. It shares a representation of horizontal meridian with area 21b and a representation of central gaze with area VLS. Analysis of the PS/20 border region indicates that the representation of the lower quadrant periphery is common to the borders of PS, 20a, and 20b rather than lying internal to areas 20a and 20b as suggested by Tusa and Palmer ('80, J. Comp. Neurol. 193:147-164).
Electrophysiological mapping methods were employed to systematically study the retinotopic organization within the cat's lateral posterior complex (LP). Visual responses were recorded in all the major subdivisions of the LP as well as in several adjoining cell groups. Specifically, separate representations of the visual field were identified for pulvinar, zones LP1-c, LP1-r, LPi, and LPm. Partial representations of the visual field were also evident in the geniculate wing, subdivisions of the lateral posterior shell, the inferior division of the posterior nuclear group, the suprageniculate nucleus, and the central lateral nucleus. Sufficient mapping observations were made to define the internal organization of major visual representations. Additionally, there was a very close correspondence between the mapping observations when they were compared with the cytoarchitectural criteria for recognizing functional cell groups (Updyke: J. Comp. Neurol. 219:143-181, '83).
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.
The distribution of corticothalamic projections from lateral suprasylvian areas AMLS, PMLS, ALLS, and PLLS was investigated with the autoradiographic method. Areas AMLS and PMLS were both found to project retinotopically upon the medial interlaminar nucleus and the lateral and pulvinar zones of the lateral posterior complex, as well as to the ventral lateral geniculate nucleus, intralaminar nuclei, and thalamic reticular complex. Retinotopic projections to the dorsal lateral geniculate nucleus were demonstrated from PMLS but not AMLS, and projections to zona incerta were demonstrated from AMLS but not PMLS. Areas PLLS and ALLS were both found to project retinotopically upon the interjacent zone of the lateral posterior complex, as well as to the intermediate and suprageniculate divisions of the posterior nuclear group, the magnocellular division of the medial geniculate complex, the thalamic reticular complex, and central lateral nucleus. Area ALLS was also found to project onto the dorsal division of the medial geniculate complex and lateral division of the posterior nuclear group. Differences between the four cortical areas in the pattern and density of their thalamic projections supports the parcellation of these areas as proposed by Palmer et al. ('78). The projection patterns of areas PMLS, AMLS, PLLS, and ALLS were found to respect the boundaries of the zones of the lateral posterior complex, which had been identified and defined previously (Updyke, '77), and the results thus support the hypothesis that these zones are the functional units of organization of visual traffic between the cat's extrastriate visual areas.
Electrophysiological mapping criteria were employed to identify visual areas 20a, 20b, 21a, 21b, PMLS, AMLS, ALLS, PLLS, DLS, VLS, and PS in the cat, and to guide placement of tracer deposits. Anterograde tracer methods were used to study the corticostriatal projections of these extrastriate visual areas. The experiments demonstrate that all 11 extrastriate areas send projections to two distinct regions within the striatum, an extensive longitudinal zone within the caudate nucleus, and a more compact region within the posterolateral putamen. Cortical visual projections to the putamen terminate in relatively compact sheets or slabs, and appear to overlap extensively, while those to the caudate nucleus are irregularly patchy and more widely dispersed. Retrograde tracer deposits into the visual recipient zone of the caudate nucleus reveal substantial convergence of other cortical inputs to this same domain. Aspects of visuotopic organization are preserved in the visual projections to both the putamen and the caudate nucleus, but unequivocal retinotopic organization could not be inferred from the available material. Ten of the eleven extrastriate visual area also project topographically onto the visual zone of the claustrum. Area PS does not appear to contribute to the corticoclaustral projections. Five of the extrastriate visual areas (ALLS, PLLS, DLS, VLS, PS) also send sparse projections to the amygdaloid complex.
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