Brainstem modulation of visual response properties of single cells in the dorsal lateral geniculate nucleus of cat

Abstract

The dorsal lateral geniculate nucleus (dLGN) transmits visual signals from the retina to the cortex. In the dLGN the antagonism between the centre and the surround of the receptive fields is increased through intrageniculate inhibitory mechanisms. Furthermore, the transmission of signals through the dLGN is modulated in a state-dependent manner by input from various brainstem nuclei including an area in the parabrachial region (PBR) containing cholinergic cells involved in the regulation of arousal and sleep. Here, we studied the effects of increased PBR input on the spatial receptive field properties of cells in the dLGN. We made simultaneous single-unit recordings of the input to the cells from the retina (S-potentials) and the output of the cells to the cortex (action potentials) to determine spatial receptive field modifications generated in the dLGN. State-dependent modulation of the spatial receptive field properties was studied by electrical stimulation of the PBR. The results showed that PBR stimulation had only a minor effect on the modifications of the spatial receptive field properties generated in the dLGN. The PBR-evoked effects could be described mainly as increased response gain. This suggested that the spatial modifications of the receptive field occurred at an earlier stage of processing in the dLGN than the PBR-controlled gain regulation, such that the PBR input modulates the gain of the spatially modified signals. We propose that the spatial receptive field modifications occur at the input to relay cells through the synaptic triades between retinal afferents, inhibitory interneurone dendrites, and relay cell dendrites and that the gain regulation is related to postsynaptic cholinergic effects on the relay cells.

Figure 1. Recordings and PSTH illustrating visual response

A, original recording trace showing differences between S-potentials (SP) and action potentials (AP). The lower trace shows the action potential and the preceding S-potential on a larger time scale. Notice the initial shoulder on the action potential indicating that the action potential takes off from an S-potential. Scale bar in upper trace, 25 ms, in lower trace 5 ms. B, a PSTH showing the response to the sequence of the 14 stimulus conditions for one spot size. This histogram was compiled from 20 repetitions; bin width 5 ms. The six horizontal lines under the histogram mark the periods (500 ms) when the visual stimulus was on (light spot for on-centre cells, dark spot for off-centre cells). The lowermost horizontal line marks the period during which the train-stimulation of PBR was applied.

Figure 2. Effect of PBR stimulation on spatial summation and receptive field organization

Response versus spot width curves before (○) and during (•) PBR stimulation. The response was measured as mean firing rate during the first spot presentation in the control condition (2nd condition in the PSTH, cf. Fig. 1B) and the first spot presentation during PBR stimulation (6th condition in the PSTH). A, on-centre X cell. B, off-centre X cell. C, off-centre Y cell. Each data point was based on 10 stimulus repetitions in A, 10 in B, and 23 in C. The contrast was 0.33 in A, −0.67 in B, and −0.21 in C.

Figure 3. Degree of PBR-evoked enhancement of the dLGN cell response

A, X cells. B, Y cells. C, all cells.

Figure 4. Scatter plots showing the centre-surround antagonism during PBR stimulation versus antagonism in the control condition

A, X cells. B, Y cells. C, all cells.

Figure 5. Effects of PBR stimulation on receptive field dimensions

Scatter plots of the diameter of the RF-centre for A, X cells and B, Y cells, RF-surround for C, X cells and D, Y cells during PBR stimulation versus the control condition.

Figure 6. Linear relationship between response during PBR stimulation and response in the control condition

Plots for 6 X cells (A-F) and 3 Y cells (G-I). ○s, response to stimuli smaller than or equal to the receptive field centre for the dLGN cell. •s, response to stimuli larger than the receptive field centre. Straight lines are linear regression lines fitted by method of least squares. Coefficient of correlation (r), and the slope of the regression line are indicated in each plot.

Figure 7. Response to the various spot sizes during PBR stimulation showed high correlation with the response in the control condition

Frequency distribution of the coefficient of correlation for A, X cells; B, Y cells and C, all cells. Bin width 0.01.

Figure 8. Changes in spatial receptive field properties at the retinogeniculate relay are only weakly influenced by PBR stimulation

A, response versus spot width curves for an on-centre X cell. ▪s, retinal input measured by average rate of S-potentials during the 500 ms time window with spot on. Data points were based on 12 repetitions. The contrast was 0.33. ○s, response of the dLGN cell in the control condition measured by average firing rate of action potentials. •s, response of the dLGN cell during PBR stimulation. The effect of a pure gain increase is illustrated by the continuous and dotted curves which are the control response to the various spot diameters scaled by a constant to the response during PBR stimulation (continuous line, c = 1.4)or to the retinal input (dashed line, c = 1.8). B, difference between retinal input and dLGN cell response for each spot diameter. ▵s, retinal input minus response in control condition. ▴s, retinal input minus response during PBR stimulation. C, transfer ratio calculated for each spot diameter. ⋄s, transfer ratio versus spot width in the control condition. ♦s, transfer ratio versus spot width during PBR stimulation.

Figure 9. Effect of PBR stimulation on the output versus input relationship at the retinogeniculate relay

Replot of data in Fig. 8A. Circles and dashed line, response in the control condition of the dLGN cell to each spot diameter plotted against the retinal input for the same spot diameter. Triangles and continuous line, the response of the dLGN cell during PBR stimulation. Open symbols, response to stimuli smaller than or equal to the receptive field centre for the dLGN cell. Filled symbols, response to stimuli larger than the receptive field centre.

Figure 10. Effect of PBR stimulation on the transfer ratio at the retinogeniculate relay

Replot of data in Fig. 8. Circles and dashed line, transfer ratio in the control condition for each spot diameter plotted against the retinal input for the same spot diameter. Triangles and continuous line, transfer ratio during PBR stimulation. Open symbols, transfer ratios for stimuli smaller than or equal to the receptive field centre for the dLGN cell. Filled symbols, transfer ratios for stimuli larger than the receptive field centre.