Orientation Tuning of Input Conductance, Excitation, and Inhibition in Cat Primary Visual Cortex

Abstract

The input conductance of cells in the cat primary visual cortex (V1) has been shown recently to grow substantially during visual stimulation. Because increasing conductance can have a divisive effect on the synaptic input, theoretical proposals have ascribed to it specific functions. According to the veto model, conductance increases would serve to sharpen orientation tuning by increasing most at off-optimal orientations. According to the normalization model, conductance increases would control the cell's gain, by being independent of stimulus orientation and by growing with stimulus contrast. We set out to test these proposals and to determine the visual properties and possible synaptic origin of the conductance increases. We recorded the membrane potential of cat V1 cells while injecting steady currents and presenting drifting grating patterns of varying contrast and orientation. Input conductance grew with stimulus contrast by 20-300%, generally more in simple cells (40-300%) than in complex cells (20-120%), and in simple cells was strongly modulated in time. Conductance was invariably maximal for stimuli of the preferred orientation. Thus conductance changes contribute to a gain control mechanism, but the strength of this gain control does not depend uniquely on contrast. By assuming that the conductance changes are entirely synaptic, we further derived the excitatory and inhibitory synaptic conductances underlying the visual responses. In simple cells, these conductances were often arranged in push-pull: excitation increased when inhibition decreased and vice versa. Excitation and inhibition had similar preferred orientations and did not appear to differ in tuning width, suggesting that the intracortical synaptic inputs to simple cells of cat V1 originate from cells with similar orientation tuning. This finding is at odds with models where orientation tuning in simple cells is achieved by inhibition at off-optimal orientations or sharpened by inhibition that is more broadly tuned than excitation.

Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina

“…Our results indicate that direction selectivity for both on-and off-responses is generated to some extent by a push-pull mechanism, where complementary changes in excitation and inhibition drive the cell to a greater or lesser degree with only small changes in overall membrane conductance (Watanabe and Murakami, 1984;Anderson et al, 2000). However, although this study characterized the synaptic inputs to the DSGCs in unprecedented detail, our results raise many questions.…”

“…To separate the conductance records into excitatory and inhibitory components, we assumed that the DSGCs were isopotential (Anderson et al, 2000;Borg-Graham, 2001). However, a simple test confirmed the expectation that this is an approximation.…”

Synaptic Responses to Whisker Deflections in Rat Barrel Cortex as a Function of Cortical Layer and Stimulus Intensity

“…5, bottom plots). This technique has been successfully applied before in comparable in vivo experiments (Moore and Nelson, 1998;Anderson et al, 2000Anderson et al, , 2001Monier et al, 2003), and Monier et al (2003) obtained the same values when measuring the input conductance in current-clamp mode and in voltage-clamp mode, thereby prompting them to consider both methods equally valid. During the Gr cell synaptic response, Rin dropped sharply by 50% to a peak minimum of 15.0 M⍀ (Rin at rest, 29.6 M⍀) and peak latency of 20.7 msec and then returned slowly to baseline.…”

Local networks in visual cortex and their influence on neuronal responses and dynamics

“…This work led to the hypothesis that more than one mechanism may produce orientation tuning in V1 neurons [69]. Other studies have failed to find substantial evidence for orthogonal tuning of inhibition [1,23,46]. Recently, in a comprehensive study, Monier et al [44] have convincingly demonstrated that indeed the orientation tuning of inhibitory synaptic inputs shows substantial variability across the population.…”

“…It is also possible that the balance of excitation and inhibition plays an important role in regulating the tuning of spiking outputs of neurons near pinwheel centers. There is substantial evidence for shunting inhibition in V1 neurons [1,10,30,44], though the tuning of such inhibition is not entirely clear [1,44]. Shunting inhibition can effectively clamp the membrane potential, which has the effect of reducing the influence of excitatory synaptic inputs, and also reducing the variability of membrane potential [44].…”