VISUAL RESOLUTION AND SENSITIVITY OF SINGLE CELLS IN THE PRIMARY VISUAL-CORTEX (V1) OF A NOCTURNAL PRIMATE (BUSH BABY) - CORRELATIONS WITH CORTICAL LAYERS AND CYTOCHROME-OXIDASE PATTERNS

1. This study describes the response properties of V1 cortical cells in a nocturnal primate and examines the receptive field organization of these cells in relationship to anatomically defined layers and cytochrome oxidase (CO) rich blobs and CO poor interblob compartments. Visual resolution and contrast sensitivity are consistent with other physiological and behavioral measures in this species. Comparisons are made with response properties of the same zones in macaque monkey, as well as of area 17 of a distantly related species (cat) that also occupies a nocturnal niche. 2. The responses of single cells to drifting sinusoidal gratings were recorded in V1 (striate cortex) of anesthetized, paralyzed bush babies (Galago crassicaudatus). Cells tended to be grouped with respect to ocular dominance, orientation preference, and direction selectivity. There was a high proportion of monocularly driven cells as in macaque monkey. Only 6% of the cells were nonoriented. These were poorly tuned complex cells and bore no resemblance to nonoriented lateral geniculate nucleus (LGN)-like cells reported in layer IV of macaque monkeys. Unidirectional cells were most frequently encountered in cortical layers that receive input from the magnocellular layers of the LGN. 3. Cells were classified as simple (31%) or complex (69%) according to standard criteria. Simple cells were significantly more narrowly tuned than complex cells for both orientation and spatial frequency. Complex cells had significantly higher average optimal spatial frequencies and spatial frequency cutoffs than simple cells. Contrast sensitivity of simple and complex cells averaged 38 and 34. respectively. Spatial resolution and sensitivity of these cells matches behavioral measures in bush baby. The spatial and temporal resolution of bush baby cells are similar to those of cats, which is likely related to the nocturnal niche of both species. 4. Cells in supragranular (I-III) and infragranular (V, VI) layers differed significantly in their response characteristics. The cells in the supragranular layers had significantly higher contrast sensitivity than did the cells in the infragranular layers. Cells in the supragranular layers likewise had higher temporal frequency cutoffs, significantly lower optimal spatial frequencies, lower spatial frequency cutoffs, and tighter orientation tuning than did cells in the infragranular layers. 5. Properties of cells in individual layers and CO blob and interblob compartments also showed differentiation. Layer III had the narrowest orientation and spatial frequency tuning with the tightest tuning in layer IIIC (IVB).1 Additionally, layer III had the lowest optimal spatial frequency and cutoff with IIIA and IIIB being lower than IIIC (IVB). Layer III also had the highest contrast sensitivity and highest cutoff temporal frequency of all layers. 6. Cells in the CO blobs and interblobs in layer III also exhibited differences. As in macaque monkeys CO blobs had more monocular cells. Unlike macaque monkeys, cells in the CO blobs in bush baby had significantly higher spatial frequency cutoffs and tended to have lower contrast sensitivities than cells in the interblobs. These species differences can be accounted for by differences in the indirect projections of magnocellular (M) and parvocellular (P) LGN pathways to interblobs. 7. The two divisions of layer IV (IVC) also showed major differences in response characteristics. Layer IValpha (IVCalpha), which receives input from the M LGN pathway, had significantly more directionally selective cells and tended to have higher contrast sensitivity ( 50.6 vs. 27.5) than P recipient IVbeta (IVCbeta). The projection of IValpha (IVCalpha) through IIIC (IVB) to the middle temporal visual area (MT) in both bush baby and macaque monkey would suggest that this pathway is specialized for motion processing. 8. Characteristtcs of layer V were generally complementary to those of its main cortical target, layer III. Layer V cells had the highest average optimal spatial frequency, spatial frequency cutoff and percentage of binocular cells of all layers. Cells in layer V also had the broadest spatial frequency and orientation tuning widths, and the lowest optimal temporal frequency, temporal frequency cutoff, and contrast sensitivity. Finally, layer V cells were less direction selective than cells in other layers. Layer VI cells were the least binocular of all layers and like IValpha (IVCalpha) and IIIC (IVB) had a high proportion of directionally selective cells. 9. We conclude that cells in the input and output layers and CO blob and interblob compartments of bush baby V1 show distinct properties. The existence of such distinctions in both bush baby and macaque monkey suggests that modular specialization may be a basic feature of primate cortex. However, most distinctions do not appear to relate in any simple way to either the properties of single parallel incoming LGN pathways or to individual projections between cortical layers. It appears instead that distinct properties of cortical cells may be constructed from inputs by local cortical circuitry to produce new outputs appropriate for the next steps of analysis.