The rat is a popular animal model for vision research, yet there is little quantitative information about the physiological properties of the cells that provide its brain with visual input, the retinal ganglion cells. It is not clear whether rats even possess the full complement of ganglion cell types found in other mammals. Since such information is important for evaluating rodent models of visual disease and elucidating the function of homologous and heterologous cells in different animals, we recorded from rat ganglion cells in vivo and systematically measured their spatial receptive field (RF) properties using spot, annulus, and grating patterns. Most of the recorded cells bore likeness to cat X and Y cells, exhibiting brisk responses, center-surround RFs, and linear or nonlinear spatial summation. The others resembled various types of mammalian W cell, including local-edge-detector cells, suppressed-by-contrast cells, and an unusual type with an ON–OFF surround. They generally exhibited sluggish responses, larger RFs, and lower responsiveness. The peak responsivity of brisk-nonlinear (Y-type) cells was around twice that of brisk-linear (X-type) cells and several fold that of sluggish cells. The RF size of brisk-linear and brisk-nonlinear cells was indistinguishable, with average center and surround diameters of 5.6 ± 1.3 and 26.4 ± 11.3 deg, respectively. In contrast, the center diameter of recorded sluggish cells averaged 12.8 ± 7.9 deg. The homogeneous RF size of rat brisk cells is unlike that of cat X and Y cells, and its implication regarding the putative roles of these two ganglion cell types in visual signaling is discussed.

We recorded the responses of neurons from the cat’s lateral geniculate nucleus to drifting sine-wave grating stimuli both before and during electrical stimulation of the parabrachial region of the midbrain. The parabrachial region provides a mostly cholinergic input to the lateral geniculate nucleus, and our goal was to study its effect on responses of geniculate cells to visual stimulation. Geniculate neurons respond to visual stimuli in one of two modes. At relatively hyperpolarized membrane potentials, low threshold (LT) Ca2+ spikes are activated, leading to high-frequency burst discharges (burst mode). At more depolarized levels, the low threshold Ca2+ spike is inactivated, permitting a more tonic response (relay or tonic mode). During our intracellular recordings of geniculate cells, we found that, at initially hyperpolarized membrane potentials, LT spiking in response to visual stimulation was pronounced, but that parabrachial activation abolished this LT spiking and associated burst discharges. Coupled with the elimination of LT spiking, parabrachial activation also led to a progressive increase in tonic responsiveness. Parabrachial activation thus effectively switched the responses to visual stimulation of geniculate neurons from the burst to relay mode. Accompanying this switch was a gradual depolarization of resting membrane potential by about 5–10 mV and a reduction in the hyperpolarization that normally occurs in response to the inhibitory phase of the visual stimulus. Presumably, the membrane depolarization was sufficient to inactivate the LT spikes. We were able to extend and confirm our intracellular observations on the effects of parabrachial activation to a sample of cells recorded extracellularly. This was made possible by adopting empirically determined criteria to distinguish LT bursts from tonic responses solely on the basis of the temporal pattern of action potentials. During parabrachial activation, every cell responded only in the relay mode, an effect that corresponds to our intracellular observations. We quantified the effects of parabrachial activation on various response measures. The fundamental Fourier response amplitude (Fl) was calculated separately for the total response, the tonic response component, and the LT burst component. Parabrachial activation resulted in an increased Fl amplitude for the total response. This increase was due to an increase in the tonic response component. For a subset of cells showing epochs of LT bursting, parabrachial activation concurrently reduced LT bursting and increased the amplitude of the tonic response. Parabrachial activation, by eliminating LT bursting, also caused cells to respond with more linearity. By keeping geniculate cells in the relay mode, the parabrachial region serves to maintain a more linear retinogeniculate transfer of information to cortex, and this may be important for detailed analysis of visual targets. However, when a geniculate neuron becomes hyperpolarized, as may occur during states of visual inattention, it would not respond well to visual stimuli without the sort of nonlinear amplification provided by the LT spike. Thus, the LT spike may permit hyperpolarized cells to relay to cortex the presence of a potentially salient or dangerous stimulus, but this is done at the expense of linearity. This may serve as a sort of “wake-up call” that redirects attention to a particular stimulus and eventually enhances activity of appropriate parabrachial inputs to switch the critical geniculate neurons into the relay mode.

The superior colliculus (SC) projects to all layers of the cat's lateral geniculate nucleus (LGN) and thus is in a position to influence information transmission through the LGN. We investigated the function of the tecto-geniculate pathway by studying the responses of cat LGN neurons before, during, and after inactivating the SC with microinjections of lidocaine. The LGN cells were stimulated with drifting sine-wave gratings that varied in spatial frequency and contrast. Among 71 LGN neurons that were studied, 53 showed a statistically significant change in response during SC inactivation. Control experiments with mock injections indicated that some changes could be attributed to slow waxing and waning of responsiveness over time. However, this could not account for all of the effects of SC inactivation that were observed. Forty cells showed changes that were attributed to the removal of tecto-geniculate influences. About equal numbers of cells showed increases (22 cells) and decreases (18 cells) in some aspect of their response to visual stimuli during SC inactivation. The proportion of cells that showed tecto-geniculate influences was somewhat higher in the C layers (68% of the cells) than in the A layers (44% of the cells). In addition, among cells that showed a significant change in maximal response to visual stimulation, the change was larger for cells in the C layers (64% average change) than in the A layers (26% average change) and it was larger for W cells (61% average change) than for X and Y cells (29% average change). Nearly all of the X cells that showed changes had an increase in response, and nearly all of the Y cells had a decrease in response. In addition, across all cell classes, 80% of the cells with receptive fields < 15 deg from the area centralis had an increase in response, and 80% of the cells with receptive fields > 15 deg from the area centralis had a decrease in response. None of the LGN cells had significant changes in spatial resolution, and only three cells had changes in optimal spatial frequency. Ten cells had a change in contrast threshold, 25 cells had a change in contrast gain, and 29 cells had a change in the maximal response to a high-contrast stimulus. Thus, our results suggest that the tecto-geniculate pathway has little or no effect on spatial processing by LGN neurons. Rather, the major influence is on maximal response levels and the relationship between response and stimulus contrast. Several hypotheses about the role of the tecto-geniculate pathway in visual behavior are considered.