Nonlagged relay cells and interneurons in the cat lateral geniculate nucleus: Receptive-field properties and retinal inputs

Abstract Simultaneous recording in the cat's retina and lateral geniculate nucleus (LGN) was used to find excitatory inputs to LGN cells. These recordings, correlated with measurements of LGN cell receptive-field properties, suggested new functional subdivisions of LGN cells. Distinctions between lagged and nonlagged cells were described before (Mastronarde, 1987a,b; Mastronarde et al., 1991), classification of nonlagged cells is examined here. The Xs-type relay cells described before (Mastronarde, 1987a,b) each had detectable excitatory input from only one retinal X cell. Cells that received significant input from more than one retinal X cell were of three kinds: relay cells with pure X input (XM); relay cells with mixed X and Y input (X/Y); and cells that could not be antidromically activated from visual cortex (XI). In the series of relay cells, XS-XM-X/Y-Y, cells had progressively larger receptive-field centers, lower spatial resolution, and faster and more Y-like responses to various stimuli. XI cells resembled XM and X/Y cells in some respects but tended to have higher maintained firing rates, more sustained responses, and weaker surround suppression of the center response. The distinctness of XS, XM, X/Y, XI, and Y from each other was examined with a modification of discriminant analysis that allowed cells to lack measurements for some parameters. Any given pair of categories could be distinguished reliably with only three parameters, although less so for X/Y-Y. In particular, XI cells were distinguishable from relay cells by properties other than the results of cortical stimulation, thus supporting the identity of XI cells as a separate class of X interneurons. Two discontinuities in the behavior of retinal input suggest that XM cells are a separate class from XS and X/Y cells: (1) LGN X cells received either no detectable input from any of the retinal X cells adjacent to their main input, or an easily detectable amount from several such cells; and (2) cells received either no Y input or a certain minimum amount. No such discontinuity in input underlies the distinction between X/Y and Y cells. LGN Y cells were also heterogeneous. Those with substantial input from more than one retinal Y cell had larger receptive fields and a greater preference for fast-moving stimuli than did Y cells dominated by a single input. Three Y cells could not be antidromically activated. They tended to differ from Y relay cells and resemble X interneurons in several ways. These shared properties, and the general reliability of cortical stimulation for nonlagged cells, indicate that the cells were Y interneurons. The strength of excitatory input extrapolated to zero at a separation between LGN and ganglion cell receptive fields equivalent to the radius of a retinal X axonal arbor for X input to XM, XI, and X/Y cells, or to the radius of a Y arbor for Y input to X/Y and Y cells. Thus, a retinal axon appears to be selective in providing input primarily to cells with somata within its arbor, rather than to all cells with overlapping dendrites. Coverage, the number of receptive-field centers overlapping a single point, was estimated for each kind of LGN cell described here. Each had a coverage of at least 6, comparable to that of retinal Y cells; most kinds had coverages of 15–35. These estimates support the idea that these subdivisions of LGN cells are functionally significant. XM and X/Y cells fill in the functional gap that is present between retinal X and Y cells and make the distribution of spatial properties more continuous, while multiple-input Y cells broaden the range of spatial properties. One role of LGN circuitry might thus be to provide a substrate for the correspondingly broad and continuous range of spatial-frequency tuning in the visual cortex.