Connectional and architectonic evidence for dorsal and ventral V3, and dorsomedial area in marmoset monkeys.

The existence of a third visual area, V3, along the outer margin of V2 was originally proposed for primates on the basis of projections from V1. The evidence for V3 was never totally convincing because investigators failed to demonstrate V1 projections to ventral V3, and projections to dorsal V3 could be attributed to the dorsomedial visual area (DM). We have reexamined the issue by placing large injections into both dorsal and ventral portions of V1 and subsequently processing flattened cortex for myelin and cytochrome oxidase so that borders of V1 and V2 could be determined accurately. The injections were in small-brained marmosets, where ventral V1 was most accessible and cortex could be flattened easily. The results indicate that dorsal V1 (representing the lower visual quadrant) projects to a narrow "dorsal V3" located between DM and dorsal V2, whereas ventral V1 (representing the upper visual quadrant) projects to a narrow "ventral V3." Architectonic borders for these dorsal and ventral strips were clearly apparent. In addition, all parts of V1 project to DM, whereas ventral V1 connections indicate that the dorsolateral area (DL) extends more ventral than has been established previously. We also placed injections within dorsal V2, dorsal and ventral DM, and dorsal, central, and ventral middle temporal (MT) area. Results from these injections were consistent with the proposed retinotopic organizations of V3, DM, and DL. We provide compelling evidence for the existence of areas V3, DM, and DL in marmosets and suggest that these areas are likely to be found in all primates.

Cortical connections of striate and extrastriate visual areas in tree shrews.

The ipsilateral and contralateral cortical connections of visual cortex of tree shrews (Tupaia belangeri) were investigated by placing restricted injections of fluorochrome tracers, wheat germ agglutinin-horseradish peroxidase, or biotinylated dextran amine into area 17 (V1), area 18 (V2), or the adjoining temporal dorsal area (TD). As previously reported, V1 was characterized by a widespread, patchy pattern of intrinsic connections; ipsilateral connections with V2, TD, and to a lesser extent, other areas of the temporal cortex; and contralateral connections with V1, V2, and TD. A surface-view of the myelin pattern in V1 revealed a patchwork of light and dark module-like regions. The ipsilateral connections with V2 and TD were roughly topographic, whereas heterotopic locations in V1 were callosally connected. Injections in V2 labeled as much as one third of V2 in a patchy pattern, and portions of ipsilateral V1 and TD in roughly topographic patterns. In addition, connections with several other visual areas in the temporal lobe were revealed. Contralaterally, most of the label was in V2, with some in V1 and TD. Injections in TD demonstrated connections within the region, and with adjoining portions of the temporal cortex, V2, and V1. There were sparse connections with an oval of densely myelinated cortex, which we have termed the temporal inferior area (TI). Callosal connections were concentrated in TD, but also included V2. The results provide further evidence for modular organizations within V1 and V2, and reveal for the first time the complete patterns of cortical connections of V2 and TD. The results are consistent with the proposal that at least three visual areas, the temporal anterior area, TA, the temporal dorsal area, TD, and the temporal posterior area, TP, exist along the rostrolateral border of V2 in tree shrews; suggest visual involvement of at least three other areas, the temporal inferior area, TI, the temporal anterior lateral area, and the temporal posterior inferior area located more ventrally in the temporal cortex; and fortify the conclusion that TD is the likely homologue of the middle temporal visual area of primates. Because tree shrews are considered close relatives of primates, the evidence for several visual areas along the border of V2 is more compatible with theories that propose a series of visual areas along V2 in primates, rather than a single visual area, V3.

Cortical organization in shrews: evidence from five species.

Cortical organization was examined in five shrew species. In three species, Blarina brevicauda, Cryptotis parva, and Sorex palustris, microelectrode recordings were made in cortex to determine the organization of sensory areas. Cortical recordings were then related to flattened sections of cortex processed for cytochrome oxidase or myelin to reveal architectural borders. An additional two species (Sorex cinereus and Sorex longirostris) with visible cortical subdivisions based on histology alone were analyzed without electrophysiological mapping. A single basic plan of cortical organization was found in shrews, consisting of a few clearly defined sensory areas located caudally in cortex. Two somatosensory areas contained complete representations of the contralateral body, corresponding to primary somatosensory cortex (S1) and secondary somatosensory cortex (S2). A small primary visual cortex (V1) was located closely adjacent to S1, whereas auditory cortex (A1) was located in extreme caudolateral cortex, partially encircled by S2. Areas did not overlap and had sharp, histochemically apparent and electrophysiologically defined borders. The adjacency of these areas suggests a complete absence of intervening higher level or association areas. Based on a previous study of corticospinal connections, a presumptive primary motor cortex (M1) was identified directly rostral to S1. Apparently, in shrews, the solution to having extremely little neocortex is to have only a few small cortical subdivisions. However, the small areas remain discrete, well organized, and functional. This cortical organization in shrews is likely a derived condition, because a wide range of extant mammals have a greater number of cortical subdivisions.

Visual cortex organization in primates: theories of V3 and adjoining visual areas.

After years of experimentation and substantial progress, there is still only limited agreement on how visual cortex in primates is organized, and what features of this organization are variable or stable across lines of primate phylogeny. Only three visual areas, V1, V2, and MT, are widely recognized as common to all primates, although there are certainly more. Here we consider various concepts of how the cortex along the outer border of V2 is organized. An early proposal was that this region is occupied by a V3 that is as wide and as long as V2, and represents the visual hemifield as a mirror image of V2. We refer to this notion as the classical V3 or V3-C. Another proposal is that only the dorsal half of V3-C exists, the half representing the lower visual quadrant, and thus the representation is incomplete (V3-I) by half. A version of this proposal is that V3-I is discontinuous, extremely thin in places, and highly variable across individuals, much as a vestigial or degenerate structure might be (V3-IF-incomplete and fragmented). A fourth proposal is that there is no V3. Many results suggest that a series of visual areas border V2, none of which has the characteristics of V3. Alternatively, the possibility exists that primate taxa differ with regard to visual areas bordering V2. Currently, much of the supporting evidence for a classical V3 comes from fMRI studies in humans, much of the evidence for a series of bordering areas comes from New World Monkeys and prosimian galagos, and much of the evidence for a V3-I or V3-IF comes from macaque monkeys. Possibly all these interpretations of visual cortex organization are valid, but each for only one of the major groups of primate evolution. Here, we suggest that none of these interpretations is correct, and propose instead that a modified V3 (V3-M) exists in a similar form in all primates. This V3-M is smaller and thinner than V3-C, discontinuous in the middle, but with comparable dorsal and ventral halves representing the lower and upper visual hemifields, respectively. Because the evidence for V3-M is limited, and it stems in part from our ongoing but incomplete comparative studies of V1 connections in primates, this suggestion requires further experimental evaluation and it remains tentative.

Sharper orientation tuning of the extraclassical suppressive-surround due to a neuron's location in the V1 orientation map emerges late in time.

Neuronal responses in primary visual cortex (V1) can be suppressed by a stimulus presented to the extraclassical surround, and such interactions are thought to be critical for figure ground segregation and form perception. While surround suppression likely originates from both feedforward afferents and multiple cortical circuits, it is unclear what role each circuit plays in the surround's orientation tuning. To investigate this we recorded from single units in V1 of anesthetized cat and analyzed the orientation tuning of the suppressive-surround over time. In addition, based on orientation maps derived through optical imaging prior to recording, neurons were classified as being located in domains or pinwheels. For both types of neurons, shortly after response onset (10 ms) the suppressive-surround is broadly tuned to orientation, but this is followed by a steep improvement in tuning over the next ∼30 ms. While the tuning of the pinwheel cells plateaus at this point, tuning is enhanced further for domain cells, especially those located superficially in the cortex, reaching a peak at 80 ms from response onset. This relatively slow evolution of the orientation tuning of the suppressive surround suggests that fast-arriving feedforward circuits (10 ms) likely only provide broadly tuned suppression, but that feedback from higher visual areas which is likely to arrive over the next 30 ms and can cover both the receptive field center and the extraclassical surround contributes to the initial steep rise in tuning for both cell types. Moreover, we speculate that the even later enhancement in tuning for domain neurons could mean the involvement of inputs from relatively long-range lateral connections, which not only propagate slowly but also link like-oriented domains corresponding to the receptive field of only the extraclassical surround.