Laminar organization of receptive-field properties in lateral geniculate nucleus of bush baby (Galago crassicaudatus)

Academic Article

Abstract

  • In the galago lateral geniculate nucleus (LGN), nature has conveniently segregated large, medium, and small cells into three pairs of layers. The pairs each contain one layer innervated by each eye. The pairs are organized such that layers 1 and 2 are magnocellular layers, 3 and 6, are parvocellular layers, and 4 and 5 contain very small cells (koniocellular layers). In order to determine if these cell size differences have physiological correlates, we examined the response properties of 119 neurons localized histologically to individual LGN layers in 12 greater galagos (Galago crassicaudatus). Neurones were tested for latency of responses to stimulation of the optic chiasm (OX latency), latency to antidromic stimulation of striate cortex (VC latency), concentric organization, receptive-field size, sustained or transient responses to standing contrast, responsiveness to rapidly moving targets, differences in receptive-field organization as measured with spatial-temporal (S-T) maps, and linearity of spatial summation in response to counterphased bipartite and sine-wave grating stimuli. Cells in the magnocellular layers had short OX latencies (mean, 1.7 ms) and short VC latencies (mean, 1.4 ms). They responded briskly to visual stimuli and had concentrically organized (on-center with off-surround, or the reverse) receptive fields with small to medium (0.3-3.25°) center diameters that increased slightly in diameter with increasing eccentricity. Most magnocellular layer neurons (87%) responded transiently (<15 s) to stationary stimuli and 55% responded to rapidly moving stimuli appropriate to excite the surround. All had a large to moderate phasic burst of spikes at the beginning of their response to light spots (phasic-tonic index (PTI) > 55). A few responded with excitatory doubling to either bipartite stimuli (7%) or counterphased sine-wave gratings. However, most either had a null region or inhibitory doubling. Neurones in the parvocellular layers had moderate OX latencies (mean, 2.8 ms) and moderate VC latencies (mean, 3.0 ms). They responded briskly to visual stimuli and had concentrically organized receptive fields with small to medium (0.2-3.6°) center diameters that increased in diameter with increasing eccentricity. Neurons in the parvocellular and magnocellular layers did not have significantly different receptive-field diameters. Many parvocellular layer neurons (62%) gave sustained responses to standing contrast and very few (14%) responded to rapidly moving stimuli appropriate to stimulate the surround. Nearly all had only a small (or no) phasic burst of spikes at the beginning of their response to light spots (PTI<55). all either had a null region or inhibitory doubling to bipartite stimuli or counterphased sine-wave gratings. Neurones in the koniocellular layers were very heterogeneous in their response properties. The OX and VC latencies were generally long (mean OX, 4.7 ms; mean VC, 3.9 ms), but both were more variable than the latencies of cells in either the magnocellular or parvocellular layers. Some of the koniocellular layer neurons (48%) responded briskly to visual stimuli; however, some (17%) were distinctly sluggish in their responses. Thirty-five percent were either unresponsive or weakly responsive to visual stimuli. Of the cells that were visually responsive, 47% had a concentric, center-surround organization, 40% had on-, off-, or on-off centers with suppressive surrounds, and 17% had no surround. One direction-selective neuron was encountered, along with several that sharply decreased their high maintained activity in response to small dark stimuli. The receptive-field center diameters were also quite variable (0.5-8°) but on average were larger than found in the other layer pairs. The overall profile of responses to standing contrast, response to rapidly moving targets, amount of initial phasic burst, and responses to bipartite and grating stimuli were also quite variable. Thus the koniocellular layers were generally distinguished from the other layer pairs by the presence of longer latencies, larger receptive-field center diameters, and heterogeneous receptive-field properties. Our data support the conclusion that the cell-size segregation in LGN layers is strongly correlated with differences in receptive-field properties in the prosimian primate, galago. Analysis of a variety of receptive-field properties in the galago LGN suggests that the magnocellular layers contain many Y-like cells, most of which do not exhibit excitatory doubling when tested with counterphased gratings. The parvocellular layers contain many X-like cells. The koniocellular layers contain a physiologically mixed population, some of which are W-like cells. W-like cells with linear and nonlinear spatial summation were encountered in the koniocellular layers.
  • Authors

    Published In

    Digital Object Identifier (doi)

    Author List

  • Norton TT; Casagrande VA
  • Start Page

  • 715
  • End Page

  • 741
  • Volume

  • 47
  • Issue

  • 4