X- and Y-cells in the dorsal lateral geniculate nucleus of the owl monkey (Aotus trivirgatus)

The owl monkey, as do other mammals, has Xand Y-cells in its lateral geniculate nucleus. X-cells are found in the parvocellular laminae; Y-cells, in the magnocellular laminae. Studies of the cat retino-geniculo-cortical system have recently defined at least two parallel and functionally distinct pathways involving Xand Y-cells, respectively (1-3). Preliminary data have extended this arrangement to the tree shrew (4), but to our knowledge no clear evidence for Xand Y-cells has yet been presented for primates (5). We now extend this general scheme to the owl monkey (Aotus trivirgatus) with the identification of Xand Y-cells in its lateral geniculate nucleus. Figure 1 shows the layering scheme in this nucleus (6). Not only did we find that the vast majority of neurons in the lateral geniculate nucleus was clearly composed of either Xor Ycells, but we also found only X-cells in the parvocellular laminae and only Ycells in the magnocellular laminae (see Fig. 1). We studied electrophysiological properties from 59 single geniculate neurons in four monkeys and used techniques essentially identical to previously reported methods (2, 4). Monkeys were anesthetized (initially with halothane, then maintained with N20/02, 70/30), paralyzed and artificially ventilated, and end-tidal C02 was monitored and kept near 3 to 4 percent. The pupils were dilated with topical atropine, and contact lenses were chosen by retinoscopy to focus the eyes on a 114-cm-distant tangent screen. Stimulating electrodes were placed in the optic chiasm and at various sites throughout the striate cortex. Action potentials from single geniculate neurons were extracellularly monitored with varnished tungsten microelectrodes (10 to 20 megohms at 500 hertz). We used black or white targets against the gray tangent screen to plot and study neuronal receptive fields. Colored stimuli were not used in these experiments. For many cells, post-stimulus histograms relating firing rate to various stimulus parameters [see (7) and Fig. 2] were generated by use of an optical system controlled by a computer. Cells were classified as Xor Ycells by previously described methods based on axonal conduction velocity and receptive field criteria (2, 4). We studied each cell for the following properties (2, 4): (i) action potential latencies for orthodromic optic chiasm 30 APRIL 1976 stimulation and, where possible, antidromic cortical stimulation; (ii) the dominant eye for receptive field activation; (iii) the size of the field center; (iv) the duration for which the neuron responded above spontaneous levels while a stimulus of appropriate contrast (that is, white for ON center and black for OFF center) was held in the field center; and (v) whether or not the cell was excited by rapidly moving (> 100? per second) large targets of appropriate contrast to excite the cell through its antagonistic surround (that is, black for ON center and white for OFF center). After the recording sessions, the monkeys' brains were histologically prepared in order to reconstruct electrode penetrations and cell locations (see Fig. 1). Nearly all of the cells were classified as either X-cells (42 of 59; 71 percent) or Y-cells (15 of 59; 25 percent). Only two of 59 cells (3 percent) were unclassified. We also sampled three Y-fibers apparently in the optic radiation plus two Xand seven Y-fibers in the optic tract (8). As in the cat and tree shrew (1, 2, 4), X-cells compared to Y-cells in the owl monkey isplayed more tonic or sustained responses to appropriate standing contrast (Fig. 2A), poor activation by fast visual stimuli (Fig. 2B), and no activation by fast targets of appropriate contrast to excite the cell through the surround. The difference between Xand Y-cells based on the tonic-phasic distinction was particularly dramatic in the owl monkey. All but two X-cells sustained their response to an appropriate, centered target for as long as it was presented (30 to 50 seconds) whereas no Y-cell responded for more than 1 or 2 seconds to such a stimulus, and most Y-cell responses were considerably briefer (see Fig. 2A). Field center sizes and latencies to electrical stimulation for these geniculate neurons were also similar to analogous data for Xand Y-cells from the cat and tree shrew (1, 2, 4). For 42 X-cells, the field sizes averaged 0.3? + 0.1? (mean and standard deviation for this and the following values); for 15 Y-cells this was 0.9? 0.3? Latencies to orthodromic optic chiasm stimulation for 28 X-cells averaged 2.3 ? 0.3 msec; for 12 Y-cells this was 1.4 ? 0.2 msec. Latencies to antidromic cortical stimulation for 14 X-cells averaged 2.3 ? 0.5 msec; for eight Ycells this was 1.5 ? 0.2 msec. In addition to finding clearly distinguishable geniculate Xand Y-cells in the owl monkey, we also found these cell types to be anatomically segregated in the nucleus. Figure 1 is a typical example of one of our electrode track reconstructions. Six X-cells were located in the parvocellular laminae, an unclassified neuron was found in the interlaminar zone, and three Y-cells were recorded in the magnocellular laminae. In every electrode penetration through the nucleus we noticed the following pattern: first (in the parvocellular laminae) we found neurons with unambiguous X-cell characteristics; then (in the interlaminar zone) we found very few cells (apparently only two in the entire series) which could be isolated above background "hash," and these were unclassified cells; then (in the magnocellular laminae) we found neurons with clear Y-cell features; and finally, we occasionally isolated an optic tract fiber. Fig. 1. Reconstruction of electrode penetration through the lateral geniculate nucleus, which is shown in parasagittal section. Closed symbols represent the location of neu-/ P rons driven by the ipsilateral/ / /* p eye; open symbols, those P driven by the contralateral eye; and the lesion is marked by an arrow. Circles repre/ sent X-cells; squares, Y-cells; and the star, an unclassified / / / // cell. Note that X-cells were / // in the parvocellular laminae, mm Y-cells were in the magnocellular laminae, and the unOT classified cell was in the cellpoor interlaminar zone (6). Abbreviations: OT, optic tract; PG, perigeniculate; IP, inferior pulvinar; PE, external parvocellular lamina; PI, internal parvocellular lamina; MI, internal magnocellular lamina; ME, external magnocellular lamina; S, lamina S.