Mechanisms of direction selectivity in cat primary visual cortex as revealed by visual adaptation

Abstract

In contrast to neurons of the lateral geniculate nucleus (LGN), neurons in the primary visual cortex (V1) are selective for the direction of visual motion. Cortical direction selectivity could emerge from the spatiotemporal configuration of inputs from thalamic cells, from intracortical inhibitory interactions, or from a combination of thalamic and intracortical interactions. To distinguish between these possibilities, we studied the effect of adaptation (prolonged visual stimulation) on the direction selectivity of intracellularly recorded cortical neurons. It is known that adaptation selectively reduces the responses of cortical neurons, while largely sparing the afferent LGN input. Adaptation can therefore be used as a tool to dissect the relative contribution of afferent and intracortical interactions to the generation of direction selectivity. In both simple and complex cells, adaptation caused a hyperpolarization of the resting membrane potential (-2.5 mV, simple cells, -0.95 mV complex cells). In simple cells, adaptation in either direction only slightly reduced the visually evoked depolarization; this reduction was similar for preferred and null directions. In complex cells, adaptation strongly reduced visual responses in a direction-dependent manner: the reduction was largest when the stimulus direction matched that of the adapting motion. As a result, adaptation caused changes in the direction selectivity of complex cells: direction selectivity was reduced after preferred direction adaptation and increased after null direction adaptation. Because adaptation in the null direction enhanced direction selectivity rather than reduced it, it seems unlikely that inhibition from the null direction is the primary mechanism for creating direction selectivity.

Fig. 1.

Measurements of the effects of visual adaptation. For both simple and complex cells, the response was defined by the peak response, which is equal to the sum of the membrane potential modulation (F1 component) and mean response (DC component). The measurement was made in 2 ways: relative to the resting potential (V_rest) in the control condition (R_abs), or the response relative to the resting potential in the adapted condition (R_rel). In the control, unadapted condition (left), R_abs and R_rel are equivalent. In the adapted state (right) R_abs and R_rel are potentially distinct if there are changes in the V_rest caused by adaptation.

Fig. 2.

Effects of prolonged stimulation on a simple cell. Average responses to drifting gratings in the preferred (light traces) and opposite (dark traces) directions after no visual adaptation (A), prolonged visual stimulation in the preferred direction (B), or prolonged visual stimulation in the opposite (null) direction (C). The resting membrane potential for each adaptation condition is indicated by the black dashed lines. Upward pointing arrows indicate the beginning of visual stimulation. D and E: contrast-response curves for the six stimulus conditions: preferred and null direction stimuli after adaptation to a blank stimulus, to the preferred direction, or to the null direction. Responses are measured as the peak depolarization (F1+DC) relative to the adapted resting potential (R_rel). F and G: same as D and E for the peak depolarization measured relative to the unadapted resting potential (R_ab).

Fig. 3.

Effects of prolonged stimulation on a complex cell. Format follows Fig. 2 with the exception of cycle-averaged responses.

Fig. 4.

Changes in resting potential and depolarization amplitude across the population. A and B: the relationship between depolarization evoked by the adapting stimulus and the change in resting membrane potential observed during adaptation. A: simple cells, B: complex cells. ○, response to the preferred direction; ●, response to the null direction. C and D: changes in R_rel, the peak visually evoked depolarization measured relative to the adapted V_rest. C: simple cells, D: complex cells. E and F: the changes R_abs, the depolarization measured relative to the unadapted V_rest, E: simple cells, F: complex cells.

Fig. 5.

Adaptation-induced changes in the direction index. For each panel, the postadaptation direction index (DI) is plotted relative to the control (unadapted) DI. Indices were calculated from R_rel. Each symbol indicates the preand postadaptation DI for a single cell. A: for simple cells, neither preferred direction adaptation (○) nor opposite (null) direction adaptation (●) caused significant changes in the direction indices. B: for complex cells, preferred direction adaptation decreased the DI whereas opposite direction adaptation increases DI. C: the hybrid direction index (HDI) for simple (●) and complex (○) cells shows little change in direction selectivity after adaptation of the cortical network.

Fig. 6.

A schematic model that describes the changes in direction selectivity caused by prolonged visual stimulation in complex cells. A: a diagram of the input to the complex cell coming from simple cells tuned to preferred direction (top 4 inputs) and simple cells tuned to the null direction (bottom 2 inputs). B: after preferred direction adaptation, those simple cells tuned to the preferred direction (top 4 inputs, gray) have reduced responses relative to those inputs tuned to the opposite direction the responses of which are less affected by the adapting stimulus. The target complex cell's direction selectivity is therefore reduced. C: in the case of null direction adaptation, the simple cells tuned to the opposite direction have reduced responses, causing the direction selectivity of the complex cell to increase.