Mechanisms underlying direction selectivity of neurons in the primary visual cortex of the macaque

Abstract

1. We studied the effects of blocking intracortical inhibition by microiontophoretic administration of bicuculline methiodide (BMI), a selective antagonist for gamma-aminobutyric acid-A receptors, on direction sensitivity of 103 neurons in the primary visual cortex (VI) of anesthetized and paralyzed monkeys. 2. The direction selectivity index (DSI) of each cell was calculated for the control response and response during the BMI administration at the optimal stimulus orientation to assess the directionality of an individual cell. 3. The averaged direction tuning of visual responses of cells was sharp in layers IVa and IVb, moderate in both interblob and blob regions of layer II/III and layers V and VI, and poor in layers IVc alpha and IVc beta. 4. Iontophoretic administration of BMI uncovered or facilitated responses to stimuli moving in the nonpreferred direction, and reduced DSIs of cells to a varying extent in all the layers except layer VI. Responses to stimuli moving in the preferred direction were also facilitated so that a slight bias of response toward the originally preferred direction remained during BMI administration in most cells. 5. Most of the cells in layers II/III (both blobs and interblobs) and IVb that receive inputs from layers IVc alpha and IVc beta showed a clear reduction of direction selectivity during BMI administration. This result suggests that intracortical inhibition plays an important role in the elaboration of direction selectivity at the second stage of information processing in VI. 6. The direction selectivity of cells in layer VI was most resistant to the effects of BMI, suggesting that it is dependent on excitatory inputs that are already direction selective, even though the sample size of this layer was small. 7. In direction-selective cells outside layer VI, responses to a stimulus moving in the preferred direction were enhanced in a way that was linearly related with those in the nonpreferred direction as the BMI dose was increased. This suggests that various amounts of inhibition interact linearly with directionally biased excitatory inputs to raise the firing threshold to various levels so as to produce various degrees of directionality. 8. These results suggest that, in most of the directionally sensitive cells except for those in layer VI, there are excitatory inputs which are bidirectional but slightly biased to one direction, and that the intracortical inhibition raises a threshold level of responses to excitatory inputs so that the response become direction selective.

Dendritic Computation of Direction Selectivity and Gain Control in Visual Interneurons

“…2a,b). Such a strong decrease of direction selectivity caused by the GABA receptor blocker has been reported previously for extracellular measurements of spiking L P TC s such as the H1-cell (Schmid and Bülthoff, 1988) as well as for other systems, e.g., rabbit retinal ganglion cells (Wyatt and Daw, 1976) or cells of the striate cortex (Sillito, 1977;Sato et al, 1995). The effects of P TX on the motion-induced change of R I N as measured by injection of small hyperpolarizing current pulses were as follows.…”

Contribution of Cholinergic and GABAergic Mechanisms to Direction Tuning, Discriminability, Response Reliability, and Neuronal Rate Correlations in Macaque Middle Temporal Area

“…GABAergic mechanisms contribute to directional tuning in V1 (Sillito, 1977;Sato et al, 1995;Crook et al, 1998;Murthy and Humphrey, 1999;Roerig and Kao, 1999). It was argued that neurons in macaque area MT inherit their direction selectivity from neurons in areas V1, V2, and V3 , because cells that project to MT are already directionally selective.…”

Physiological and Anatomical Organization of Multiwhisker Response Interactions in the Barrel Cortex of Rats

“…The direction-selective response is thought to play a crucial role in detecting the direction of movements of nearby objects and the animal itself. It has been reported that the direction-selective response in the visual cortex is based on a linear summation of directionally biased excitatory and inhibitory inputs (Sato et al, 1995). In the barrel cortex, single whisker response is also reported to exhibit direction preference (Simons 1983(Simons , 1985.…”