GABA-mediated inhibition correlates with orientation selectivity in primary visual cortex of cat

doi:10.1016/j.neuroscience.2008.06.032

Neuroscience

Volume 155, Issue 3, 26 August 2008, Pages 914-922

https://doi.org/10.1016/j.neuroscience.2008.06.032 Get rights and content

Abstract

Orientation selectivity is an important emergent property of neurons in the primary visual cortex, and inhibition is thought to play an important role in establishing this selectivity. But the relationship between strength of inhibition and orientation selectivity is unclear. To investigate this relationship, we electrophoretically applied the inhibitory transmitter GABA and the GABA_A antagonist bicuculline on the same individual area 17 neurons in anesthetized cats. Neurons were classified as weakly orientation-selective, moderately orientation-selective, or strongly orientation-selective, according to the values of an orientation bias index. Orientation bias, half-width of the tuning curve at half-height and an orientation-specificity index (orthogonal to optimal ratio) were compared with or without GABA and bicuculline administration. GABA improved orientation selectivity with the greatest effects on weakly orientation-selective cells, smaller effects on moderately orientation-selective cells, and minimal effects on strongly orientation-selective cells; bicuculline diminished orientation selectivity the most on moderately and strongly orientation-selective cells, with minimal effects on weakly orientation-selective cells. We also found that orientation selectivity correlated with the level of neurons' spontaneous activity. These results suggest that the degree of orientation selectivity of an area 17 neuron correlates with its endogenous inhibition strength, and that GABAergic inhibition can bi-directionally regulate orientation selectivity. This correlation indicates that GABA-mediated inhibition plays an important role in establishing sharp orientation selectivity of individual neurons.

Section snippets

Preparation and recording

Experiments were performed on anesthetized and paralyzed adult cats (2.1–2.8 kg). All procedures were approved by the Institutional Animal Care and Use Committee of University of Science and Technology of China and conformed to the guidelines of the National Institutes of Health Guide for the Care and Use of Laboratory Animals. All efforts were made to minimize animal suffering and to reduce the number of animals used. The methods of preparation and single-cell recording are the same as

Results

For 86 neurons in the primary visual cortex, the recording conditions were stable and lasted long enough (at least 2 h) so that we could complete a full set of tests with GABA and bicuculline iontophoresis; the following analysis includes only those neurons for which all tests were completed. Consistent with previous reports (Nelson 1991, Ringach et al 2002a), in our present study no systematic differences were observed in the effects of GABA and bicuculline on cells classified as simple or

Discussion

In this study we employed microiontophoretic application of GABA and bicuculline to bi-directionally modulate the input inhibition strength in area 17 neurons, and compared the effects on their orientation selectivity and spontaneous responses. The main finding is that GABA-mediated inhibition was greater in Strongly-OS cells than in Weakly-OS cells. GABA was more effective in Weakly-OS cells than in Strongly-OS cells, and conversely, the GABA antagonist bicuculline was more effective in

Acknowledgments

The authors wish to thank Prof. Curtis Baker (McGill University, Montreal, Canada) for polishing the manuscript. This work was supported by the Natural Science Foundation of China (to Y.Z.).

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Citation Excerpt :
The directionality of our correlation is consistent with previous work; participants with higher GABA levels are better able to discriminate spatial and temporally different stimuli in both somatosensory and visual domains. Along similar lines, GABA plays an important role in orientation tuning, with the application of the GABA antagonist bicuculline reducing orientation selectivity (Sillito, 1975; Sillito et al., 1980; Tsumoto et al., 1979; Wolf et al., 1986) and the application of GABA increasing orientation tuning (Li et al., 2008). This is also consistent with our correlation between occipital GABA and visual orientation thresholds where participants with more occipital GABA were better at visual discrimination.
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View full text

Sensory systemGABA-mediated inhibition correlates with orientation selectivity in primary visual cortex of cat

Abstract

Section snippets

Preparation and recording

Results

Discussion

Acknowledgments

Brain Res

Vision Res

Neuron

Neuroscience

Vision Res

Neurobiol Aging

Brain Res

Inactivation of the infragranular striate cortex broadens orientation tuning of supragranular visual neurons in the cat

Exp Brain Res

The influence of input from the lower cortical layers on the orientation tuning of upper layer V1 cells in a primate

Vis Neurosci

GABAB-receptor-mediated inhibition reduces the orientation selectivity of the sustained response of striate cortical neurons in cats

Vis Neurosci

‘Simplification’ of responses of complex cells in cat striate cortex: suppressive surrounds and ‘feedback’ inactivation

J Physiol

Theory of orientation tuning in visual cortex

Proc Natl Acad Sci U S A

Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex

Vis Neurosci

The Psychophysics Toolbox

Spat Vis

Membrane potential and firing rate in cat primary visual cortex

J Neurosci

Summation and division by neurons in primate visual cortex

Science

Linearity and normalization in simple cells of the macaque primary visual cortex

J Neurosci

An intracellular analysis of visual cortical neurones to moving stimuli: response in a co-operative neuronal network

Exp Brain Res

GABA-induced inactivation of functionally characterized sites in cat striate cortex: effects on orientation tuning and direction selectivity

Vis Neurosci

Organization of suppression in receptive fields of neurons in cat visual cortex

J Neurophysiol

GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex

Exp Brain Res

Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex

J Neurosci

Orientation selectivity of thalamic input to simple cells of cat visual cortex

Nature

An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat

J Physiol

Neural mechanisms of orientation selectivity in the visual cortex

Annu Rev Neurosci

Receptive field properties of single neurons in rat primary visual cortex

J Neurophysiol

Role of suppression in shaping orientation and direction selectivity of complex neurons in cat striate cortex

J Neurophysiol

Normalization of cell responses in cat striate cortex

Vis Neurosci

Receptive fields, binocular interaction and functional architecture in the cat's visual cortex

J Physiol

Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex

J Neurosci

GABA and its agonists improved visual cortical function in senescent monkeys

Science

Sensory system
GABA-mediated inhibition correlates with orientation selectivity in primary visual cortex of cat