Vivien A. Casagrande

A third parallel visual pathway to primate area V1

Recent studies of the primate visual system have focused on the proposal that the perception of form and motion are processed by two parallel pathways that originate from separate populations of cells in the retina. Earlier proposals for parallel processing of visual signals identified a third pathway that could be traced from the retina to the visual cortex. This third pathway was assumed to be unimportant. A growing body of evidence suggests that this pathway to cortex is distinct anatomically, physiologically and neurochemically, and is well represented in primates. These findings raise new and interesting questions not only about the role of this pathway, but also about the intracortical integration of afferent parallel signals.

The Afferent, Intrinsic, and Efferent Connections of Primary Visual Cortex in Primates

Because of its distinctive architecture, connections, and functions, primary visual cortex, area 17 or V1 of primates, can be easily identified in most mammals (Kaas, 1987). V1 (also referred to as striate cortex) is particularly distinctive in primates, and, as a result, it was the first cortical area identified histologically (see Gennari, 1782, in Fulton, 1937). V1 of most, if not all, primates has a number of conspicuous features that distinguish this structure from its homologue in other mammals. Unlike carnivores, such as cats and ferrets, almost all of the visual input relayed from the lateral geniculate nucleus (LGN) of primates terminates in V1 (Benevento and Standage, 1982; Bullier and Kennedy, 1983; see Henry, 1991, for review), and lesions of V1 produce a severe deficit known as cortical blindness (e.g., Cowey and Stoerig, 1989). In addition, visual cortex of all primates is activated by physiologically and morphologically distinguishable streams, or channels, of inputs that are relayed from the retina to V1 in a manner unique to primates (Kaas and Huerta, 1988; Casagrande and Norton, 1991). Furthermore, the intrinsic connections of V1 in primates exhibit both vertical (laminar) and areal (modular) distinctions that appear designed to create new output channels from input channels via features of internal circuitry. Finally, the output streams project to visual areas that seem to be organized in a manner unique to primates. In particular, the major cortical target of V1, the second visual area, V2, is composed of three morphologically distinct modules that are differentially activated from V1, and at least one other major target of V1, the middle temporal visual area or MT, appears to be a unique specialization of primates (Kaas and Preuss, 1993). These common features of visual cortex in primates are of particular interest because these specializations relate to vision in humans as well as other primates. In this review, we focus on common features that have been described for V1 across a variety of primate species, and therefore are most likely to be present in most or all primates. In addition, we describe differences in V1 organization across primate groups, since these differences may relate to functional specializations and adaptations in the greatly varied primate order. Features that vary across taxa, when related to behavioral niches, may provide clues as to the significance of variations. Finally, this review briefly compares V1 in primates with V1 in some nonprimates to emphasize the distinctiveness of V1 in primates.

A comparison of koniocellular, magnocellular and parvocellular receptive field properties in the lateral geniculate nucleus of the owl monkey (Aotus trivirgatus)

1 By analogy to previous work on lateral geniculate nucleus (LGN) magnocellular (M) and parvocellular (P) cells our goal was to construct a physiological profile of koniocellular (K) cells that might be linked to particular visual perceptual attributes. 2 Extracellular recordings were used to study LGN cells, or their axons, in silenced primary visual cortex (V1), in nine anaesthetized owl monkeys injected with a neuromuscular blocker. Receptive field centre‐surround organization was examined using flashing spots. Spatial and temporal tuning and contrast responses were examined using drifting sine‐wave gratings; counterphase sine‐wave gratings were used to examine linearity of spatial summation. 3 Receptive fields of 133 LGN cells and 10 LGN afferent axons were analysed at eccentricities ranging from 2.8 to 31.3 deg. Thirty‐four per cent of K cells and only 9 % of P and 6 % of M cells responded poorly to drifting gratings. K, P and M cells showed increases in centre size with eccentricity, but K cells showed more scatter. All cells, except one M cell, showed linearity in spatial summation. 4 At matched eccentricities, K cells exhibited lower spatial and intermediate temporal resolution compared with P and M cells. K contrast thresholds and gains were more similar to those of M than P cells. M cells showed lower spatial and higher temporal resolution and contrast gains than P cells. 5 K cells in different K LGN layers differed in spatial, temporal and contrast characteristics, with K3 cells having higher spatial resolution and lower temporal resolution than K1/K2 cells. 6 Taken together with previous results these findings suggest that the K cells consist of several classes, some of which could contribute to conventional aspects of spatial and temporal resolution.

W-like response properties of interlaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus)

Recent anatomical studies have suggested that the cells located in the interlaminar zones (ILZs) of the primate dorsal lateral geniculate nucleus (LGN) relay visual information from the retina to the striate cortex in a manner similar to that of W-cells in the LGN of cat. In the present study, we examined this idea directly by recording the response properties of single cells localized to the ILZs in the prosimian primate, Galago crassicaudatus. The properties of the cells in the ILZs were found to be physiologically distinct from the X-like and Y-like properties of the parvocellular and magnocellular LGN layers. Moreover, the small cells located in the interlaminar zones were physiologically similar to the W-like cells found in the specialized small-celled koniocellular layers in these primates. As is the case with the koniocellular layer cells, the ILZ cells exhibited a broad range of properties which, as a group, were distinguished by the following characteristics: the ILZ cells had long latencies to stimulation of the optic chiasm (mean, 3.95 ms) and to antidromic stimulation from striate cortex (mean, 3.31 ms) and had relatively large receptive-field centers (mean, 1.79 degrees). They also had low maintained discharge rates (5.5 spikes/s), relatively long response latencies to light (mean onset, 82 ms; peak, 112 ms) and low peak firing rates (59 spikes/s). Few (25%) had standard receptive-field organization (ON-center, OFF-surround, or vice versa). Only 29% responded well to sine-wave gratings and all were influenced by non-visual (auditory and tactile) stimuli.(ABSTRACT TRUNCATED AT 250 WORDS)

Center/surround relationships of magnocellular, parvocellular, and koniocellular relay cells in primate lateral geniculate nucleus

As in other primates, the lateral geniculate nucleus (LGN) of the prosimian primate, bush baby (Galago crassicaudatus), contains three morphologically and physiologically distinct cell classes [magnocellular (M), parvocellular (P), and koniocellular (K)] (Norton & Casagrande, 1982; Casagrande & Norton, 1991). The present study examined quantitatively the center/surround relationships of cells in all three classes. Estimates of receptive-field center size (Rc) and sensitivity (Kc) and of surround size (Rs) and sensitivity (Ks) were obtained from 47 LGN relay cells by fitting a difference of Gaussians function to contrast-sensitivity data. For M and P cells, center size (Rc) increases with eccentricity but is about two times larger for M than for P cells at a given eccentricity. Surround size (Rs) increases with eccentricity for P but not for M or K cells. The center sensitivity (Kc) is inversely related to center size (Rc) and surround sensitivity (Ks) is inversely related to surround size (Rs) for cells in all classes, a result consistent with the sensitivity regulation that is produced by light adaptation. High spatial-frequency cutoff (acuity) is inversely related to center size (Rc). However, the peak contrast sensitivity is relatively independent of Rc. The ratio of the integrated strength (volume) of the surround to the volume of the center remains relatively constant (median, 0.87) across all three cell classes. This ratio is an excellent predictor of a cells rolloff in contrast sensitivity at low spatial frequencies: cells with a low surround/center ratio have less low-frequency rolloff. Although M, P, and K cells generally display similar center/surround relationships, differences in center size and the other parameters between the classes distinguish most M, P, and K cells. These findings demonstrate that both similarities and differences in the visual-response properties of primate LGN cells in these three parallel afferent pathways can be explained by basic center/surround relationships.

Gating and control of primary visual cortex by pulvinar

The primary visual cortex (V1) receives its driving input from the eyes via the lateral geniculate nucleus (LGN) of the thalamus. The lateral pulvinar nucleus of the thalamus also projects to V1, but this input is not well understood. We manipulated lateral pulvinar neural activity in prosimian primates and assessed the effect on supra-granular layers of V1 that project to higher visual cortex. Reversibly inactivating lateral pulvinar prevented supra-granular V1 neurons from responding to visual stimulation. Reversible, focal excitation of lateral pulvinar receptive fields increased the visual responses in coincident V1 receptive fields fourfold and shifted partially overlapping V1 receptive fields toward the center of excitation. V1 responses to regions surrounding the excited lateral pulvinar receptive fields were suppressed. LGN responses were unaffected by these lateral pulvinar manipulations. Excitation of lateral pulvinar after LGN lesion activated supra-granular layer V1 neurons. Thus, lateral pulvinar is able to powerfully control and gate information outflow from V1.

Endothelial nitric oxide synthetase (eNOS) in astrocytes: another source of nitric oxide in neocortex.

The distribution of the endothelial form of nitric oxide synthetase (eNOS) was examined in the visual cortex of three species of primate and in the rat using immunocytochemistry. Labeled cells were found in both the gray and white matter. These cells were stellate in appearance and labeled cell processes were seen contacting blood vessels or the pia, suggesting that, by morphological criteria, the cells were astrocytes. All eNOS positive cells were double labeled with an antibody against S100β. Although all cells were double labeled in the white matter, in the gray matter, some S100β positive cells did not contain detectable levels of eNOS. eNOS positive astrocytic processes appeared to form prominent and distinctive structures next to neurons, especially in cortical layer IIIC. We postulate that these eNOS‐positive structures form astrocytic perisynaptic sheaths on neuronal somas in the cortex. If this is true, then nitric oxide can influence neuronal transmission directly at axosomatic synapses in the cortex. In addition, the presence of eNOS in astrocytes and in their processes that contact blood vessels suggests that the link between local cortical activity and changes in cerebral blood flow could be mediated by astrocytic release of nitric oxide. GLIA 26:280–290, 1999.

The size and topographic arrangement of retinal ganglion cells in the galago

Abstract The distribution and sizes of ganglion cells in the retinae of two species of the nocturnal prosimian primate galago were investigated. The distribution of ganglion cells in both species is not uniform, ranging from 12,000 cells/mm 2 in the area centralis to 300 cells/mm 2 in the periphery. Isodensity contours also reveal specialized areas of high ganglion cell density forming a cruciform pattern around the area centralis with horizontal and vertical extensions oriented approximately along the zero meridians. Analysis of cell areas demonstrates that the central area contains exclusively small to medium-sized cells (25–90 μ 2 ) with large cells (>100 μ 2 ) first appearing approximately 1 mm from the area centralis.

Are primate lateral geniculate nucleus (LGN) cells really sensitive to orientation or direction

There is considerable controversy over the existence of orientation and direction sensitivity in lateral geniculate nucleus (LGN) neurons. Claims for the existence of these properties often were based upon data from cells tested well beyond their peak spatial frequencies. The goals of the present study were to examine the degree of orientation and direction sensitivity of LGN cells when tested at their peak spatial and temporal frequencies and to compare the tuning properties of these subcortical neurons with those of visual cortex. For this investigation, we used conventional extracellular recording to study orientation and direction sensitivities of owl monkey LGN cells by stimulating cells with drifting sinusoidal gratings at peak temporal frequencies, peak or higher spatial frequencies, and moderate contrast. A total of 110 LGN cells (32 koniocellular cells, 34 magnocellular cells, and 44 parvocellular cells) with eccentricities ranging from 2.6 deg to 27.5 deg were examined. Using the peak spatial and temporal frequencies for each cell, 41.8% of the LGN cells were found to be sensitive to orientation and 19.1% were direction sensitive. The degree of bias for orientation and direction did not vary with eccentricity or with cell class. Orientation sensitivity did, however, increase, and in some cases orientation preferences changed, at higher spatial frequencies. Increasing spatial frequency had no consistent effect on direction sensitivity. Compared to cortical cell orientation tuning, the prevalence and strength of LGN cell orientation and direction sensitivity are weak. Nevertheless, the high percentage of LGN cells sensitive to orientation even at peak spatial and temporal frequencies reinforces the view that subcortical biases could, in combination with activity-dependent cortical mechanisms and/or cortical inhibitory mechanisms, account for the much narrower orientation and direction tuning seen in visual cortex.

The distribution and morphology of LGN K pathway axons within the layers and CO blobs of owl monkey V1

The lateral geniculate nucleus (LGN) of primates contains three classes of relay cells, the magnocellular (M), parvocellular (P), and koniocellular (K) cells. At present, very little is known about either the structure or function of the K relay cells in New or Old World monkeys (simian primates). In monkeys, K cells are located between the main LGN layers and adjacent to the optic tract. For convenience, these intercalated cell layers are numbered K1-K4 starting closest to the optic tract with K1. The objective of this study was to examine the details of K axon morphology in the primary visual cortex (V1) of owl monkeys and to determine if different K layers give rise to distinct axon types. For this purpose, injections of WGA-HRP or PHA-L were made into specific K LGN layers and the distribution and morphology of the resulting labeled axons were analyzed. Injections of fluorescent tracers also were made within the superficial layers of V1 to further document connections via analysis of the patterns of retrogradely labeled cells in the LGN. Our main finding is that K axons in owl monkeys terminate as delicate focused arbors within single cytochrome oxidase (CO) blob columns in cortical layer III and within cortical layer I. Overall, the morphology of the K axons in these monkeys is quite similar to what we described previously for K geniculocortical axons in the distantly related bush baby (prosimian primate), suggesting that the basic features of this pathway are common to all primates. Our results also provide evidence that the axon arbors from different K layers are morphologically distinct; axons from LGN layer K1 project mainly to cortical layer I, while axons from LGN layer K3 chiefly terminate in cortical layer III. Taken together, these results imply that the basic features of axons within the K pathway are conserved across primates, and that the K axons from different K layers are likely to differ in function based upon their different morphologies.