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Anatomical and electrophysiological studies have provided us with detailed information regarding the extent and topography of the primary (V1) and secondary (V2) visual areas in primates. The consensus about the V1 and V2 maps, however, is in sharp contrast with controversies regarding the organization of the cortical areas lying immediately rostral to V2. In this review, we address the contentious issue of the extent of the third visual area (V3). Specifically, we will argue for the existence of both ventral (V3v) and dorsal (V3d) segments of V3, which are located, respectively, adjacent to the anterior border of ventral and dorsal V2. V3v and V3d would together constitute a single functional area with a complete representation of both upper and lower visual hemifields. Another contentious issue is the organization of the parietal-occipital (PO) area, which also borders the rostral edge of the medial portion of dorsal V2. Different from V1, V2, and V3, which exhibit a topography based on the defined lines of isoeccentricity and isopolar representation, area PO only has a systematic representation of polar angles, with an emphasis on the peripheral visual field (isoeccentricity lines are not well defined). Based on the connectivity patterns of area PO with distinct cytochrome oxidase modules in V2, we propose a subdivision of the dorsal stream of visual information processing into lateral and medial domains. In this model, area PO constitutes the first processing instance of the dorsal-medial stream, coding for the full-field flow of visual cues during navigation. Finally, we compare our findings with those in other species of Old and New World monkeys and argue that larger animals, such as macaque and capuchin monkeys, have similar organizations of the areas rostral to V2, which is different from that in smaller New World monkeys.
We investigated the contribution of the projections from area MT to the receptive field properties of cells in visual area V2 in anesthetized and paralyzed Cebus apella monkeys. We recorded extracellular single-unit activity using tungsten microelectrodes in three monkeys before and after pressure injection of a 0.25-mol/l GABA solution. The visual stimulus consisted of a single bar moving in one of eight directions. In total, 72 V2 neurons were studied in 18 sessions of GABA injection into area MT. A group of 22 neurons was investigated over a shorter period of time ranging from 15 to 60 min, during which the activity did not return to baseline levels. The remaining 50 neurons were studied over a period of at least 2 h, and no statistical difference was observed in the neuronal response before and long after GABA inactivation. The effects on these 50 neurons consisted of an early (1–20 min) significant general decrease in excitability with changes in either orientation or direction selectivity. The differential decrease in excitability resulted in an intermediate improvement (20–40 min) of the signal-to-noise ratio for the stimulus-driven activity. The inactivation depended on the quantity of GABA injected into area MT and persisted for a period of 2 h. The GABA inactivation in area MT produced inhibition of most cells (72%) and a significant change of direction tuning in the majority (56%) of V2 neurons. Both increases and also decreases in the direction tuning of V2 neurons were observed. These feedback projections are capable of modulating not only the levels of spontaneous and driven activity of V2 neurons but also the V2 receptive field properties, such as direction selectivity.
Previous immunohistochemical studies combined with retrograde tracing in macaque monkeys have demonstrated that corticocortical projections can be differentiated by their content of neurofilament protein. The present study analyzed the distribution of nonphosphorylated neurofilament protein in callosally projecting neurons located at the V1/V2 border. All of the retrogradely labeled neurons were located in layer III at the V1/V2 border and at an immediately adjacent zone of area V2. A quantitative analysis showed that the vast majority (almost 95%) of these interhemispheric projection neurons contain neurofilament protein immunoreactivity. This observation differs from data obtained in other sets of callosal connections, including homotypical interhemispheric projections in the prefrontal, temporal, and parietal association cortices, that were found to contain uniformly low proportions of neurofilament protein-immunoreactive neurons. Comparably, highly variable proportions of neurofilament protein-containing neurons have been reported in intrahemispheric corticocortical pathways, including feedforward and feedback visual connections. These results indicate that neurofilament protein is a prominent neurochemical feature that identifies a particular population of interhemispheric projection neurons at the V1/V2 border, and suggest that this biochemical attribute may be critical for the function of this subset of callosal neurons.
Cortical projections to the middle temporal (MT) visual area were studied by injecting the retrogradely transported fluorescent tracer Fast Blue into MT in adult New World monkeys (Cebus apella). Injection sites were selected based on electrophysiological recordings, and covered eccentricities from 2–70 deg, in both the upper and lower visual fields. The position and laminar distribution of labeled cell bodies were correlated with myeloarchitectonic boundaries and displayed in flat reconstructions of the neocortex. Topographically organized projections were found to arise mainly from the primary, second, third, and fourth visual areas (V1, V2, V3, and V4). Coarsely topographic patterns were observed in transitional V4 (V4t), in the parieto-occipital and parieto-occipital medial areas (PO and POm), and in the temporal ventral posterior area (TVP). In addition, widespread or nontopographic label was found in visual areas of the superior temporal sulcus (medial superior temporal, MST, and fundus of superior temporal, FST), annectent gyrus (dorsointermediate area, DI; and dorsomedial area, DM), intraparietal sulcus (lateral intraparietal, LIP; posterior intraparietal, PIP; and ventral intraparietal, VIP), and in the frontal eye field (FEF). Label in PO, POm, and PIP was found only after injections in the representation of the peripheral visual field (>10 deg), and label in V4 and FST was more extensive after injections in the central representation. The projections from V1 and V2 originated predominantly from neurons in supragranular layers, whereas those from V3, V4t, DM, DI, POm, and FEF consisted of intermixed patches with either supragranular or infragranular predominance. All of the other projections were predominantly infragranular. Invasion of area MST by the injection site led to the labeling of further pathways, including substantial projections from the dorsal prelunate area (DP) and from an ensemble of areas located along the medial wall of the hemisphere. In addition, weaker projections were observed from the parieto-occipital dorsal area (POd), area 7a, area prostriata, the posterior bank of the arcuate sulcus, and areas in the anterior part of the lateral sulcus. Despite the different nomenclatures and areal boundaries recognized by different models of simian cortical organization, the pattern of projections to area MT is remarkably similar among primates. Our results provide evidence for the existence of many homologous areas in the extrastriate visual cortex of New and Old World monkeys.
Based on cytoarchitectonic criteria, the primate pulvinar
nucleus has been subdivided into medial (PM), lateral (PL),
and inferior (PI) regions. However, these subdivisions
show no correlation with those established by electrophysiological,
immunocytochemical, or neuroanatomical tracer studies.
In this work, we studied the connections of the pulvinar
nucleus of Cebus monkey with visual areas V1,
V2, V4, MT, and PO by means of retrograde fluorescent tracers
injected into these areas. Based on the projection zones
to cortical visual areas, the visual portion of the pulvinar
of Cebus monkey was subdivided into three subregions:
P1, P2, and P3, similar to those described in the macaque
(Ungerleider et al., 1984). In Cebus, P1 includes
the centrolateral portion of traditionally defined PI and
adjacent portion of PL. P2 is located in the dorsal portion
of PL and P3 includes the medial portion of PI and extends
dorsally into adjacent PL and PM. In addition, we studied
the histology of the pulvinar using multiple criteria,
such as cytoarchitecture and myeloarchitecture; histochemistry
for cytochrome oxidase, NADPH-diaphorase, and acetylcholinesterase;
and immunocytochemistry for two calcium-binding proteins,
calbindin and parvalbumin, and for a neurofilament recognized
by the SMI-32 antibody. Some of these stains, mainly calbindin,
showed additional subdivisions of the Cebus pulvinar,
beyond the traditional PI, PL, and PM. Based on this immunohistochemical
staining, the border of PI is moved dorsally above the
brachium of the superior colliculus and PI can be subdivided
in five regions (PIP, PIM, PIC,
PIL, and PILS). Regions P1, P2, and
P3 defined based on efferent connections with cortical
visual areas are not architectonically/neurochemically
homogeneous. Rather they appear to consist of further chemoarchitectonic
subdivisions. These distinct histochemical regions might
be related to different functional modules of visual processing
within one connectional area.
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