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Classic studies of lateral geniculate nucleus (LGN) and visual cortex (V1) in carnivores and primates have found that a majority of neurons in LGN exhibit a center-surround organization, while V1 neurons exhibit strong orientation selectivity and, in many species, direction selectivity. Recent work in the mouse and the monkey has discovered previously unknown classes of orientation- and direction-selective neurons in LGN. Furthermore, some recent studies in the mouse report that many LGN cells exhibit pronounced orientation biases that are of comparable strength to the subthreshold inputs to V1 neurons. These results raise the possibility that, in rodents, orientation biases of individual LGN cells make a substantial contribution to cortical orientation selectivity. Alternatively, the size and contribution of orientation- or direction-selective channels from LGN to V1 may vary across mammals. To address this question, we examined orientation and direction selectivity in LGN and V1 neurons of a highly visual diurnal rodent: the gray squirrel. In the representation of central vision, only a few LGN neurons exhibited strong orientation or direction selectivity. Across the population, LGN neurons showed weak orientation biases and were much less selective for orientation compared with V1 neurons. Although direction selectivity was weak overall, LGN layers 3abc, which contain neurons that express calbindin, exhibited elevated direction selectivity index values compared with LGN layers 1 and 2. These results suggest that, for central visual fields, the contribution of orientation- and direction-selective channels from the LGN to V1 is small in the squirrel. As in other mammals, this small contribution is elevated in the calbindin-positive layers of the LGN., (Copyright © 2015 the American Physiological Society.)

The gray squirrel (Sciurus carolinensis) is a diurnal highly visual rodent with a cone-rich retina. To determine which features of visual cortex are common to highly visual mammals and which are restricted to non-rodent species, we studied the laminar organization of response properties in primary visual area V1 of isoflurane-anesthetized squirrels using extra-cellular single-unit recording and sinusoidal grating stimuli. Of the responsive cells, 75% were tuned for orientation. Only 10% were directionally selective, almost all in layer 6, a layer receiving direct input from the dorsal lateral geniculate nucleus (LGN). Cone opponency was widespread but almost absent from layer 6. Median optimal spatial frequency tuning was 0.21 cycles/ degrees . Median optimal temporal frequency a high 5.3 Hz. Layer 4 had the highest percentage of simple cells and shortest latency (26 ms). Layers 2/3 had the lowest spontaneous activity and highest temporal frequency tuning. Layer 5 had the broadest spatial frequency tuning and most spontaneous activity. At the layer 4/5 border were sustained cells with high cone opponency. Simple cells, determined by modulation to drifting sinusoidal gratings, responded with shorter latencies, were more selective for orientation and direction, and were tuned to lower spatial frequencies. A comparison with other mammals shows that although the laminar organization of orientation selectivity is variable, the cortical input layers contain more linear cells in most mammals. Nocturnal mammals appear to have more orientation-selective neurons in V1 than diurnal mammals of similar size.

Physiological studies of the lateral geniculate nucleus (LGN) have revealed three classes of relay neurons, called X, Y, and W cells in carnivores and parvocellular (P), magnocellular (M), and koniocellular (K) in primates. The homological relationships among these cell classes and how receptive field (RF) properties of these cells compare with LGN cells in other mammals are poorly understood. To address these questions, we have characterized RF properties and laminar organization in LGN of a highly visual diurnal rodent, the gray squirrel, under isoflurane anesthesia. We identified three classes of LGN cells. One class found in layers 1 and 2 showed sustained, reliable firing, center-surround organization, and was almost exclusively linear in spatial summation. Another class, found in layer 3, showed short response latencies, transient and reliable firing, center-surround organization, and could show either linear (76%) or nonlinear (24%) spatial summation. A third, heterogeneous class found throughout the LGN but primarily in layer 3 showed highly variable responses, a variety of response latencies and could show either center-surround or noncenter-surround receptive field organization and either linear (77%) or nonlinear (23%) spatial summation. RF sizes of all cell classes showed little dependency on eccentricity, and all of these classes showed low contrast gains. When compared with LGN cells in other mammals, our data are consistent with the idea that all mammals contain three basic classes of LGN neurons, one showing reliable, sustained responses, and center-surround organization (X or P); another showing transient but reliable responses, short latencies, and center-surround organization (Y or M); and a third, highly variable and heterogeneous class of cells (W or K). Other properties such as dependency of receptive field size on eccentricity, linearity of spatial summation, and contrast gain appear to vary from species to species.