Relationship between Excitation and Inhibition Underlying Size Tuning and Contextual Response Modulation in the Cat Primary Visual Cortex (original) (raw)

A study of inhibitory antagonism in cat visual cortex

Brain Research, 1975

Since there seems to be good evidence that GABA may act as an inhibitory neurotransmitter in the mammalian cortex, we tested the effects of an antagonist of GABA, namely the alkaloid bicuculline, on the response properties of visual cortex neurons, using a computer-controlled stimulus presentation system to assess quantitatively the changes in receptive field organization after the drug. Complex cells were most affected, increasing both evoked and spontaneous activity and losing some of their specificities for stimulus parameters such as orientation and direction. Hypercomplex cells lost their inhibitory flanks, responding equally well to long and short bars after the drug. Simple cells were the least affected, usually becoming somewhat depressed after the drug. Preliminary tests with another inhibitory amino acid antagonist, strychnine, showed that it excited simple cells, indicating that possibly more than one inhibitory transmitter is at work in the cortex. The results are discussed with relation to the synaptic anatomy of the cortex, and it is concluded that a class of stellate cells, using GABA, is a likely candidate for the transmitter of some intracortical inhibition.

Length and width tuning of neurons in the cat's primary visual cortex

Journal of neurophysiology, 1994

1. The classically defined receptive field of a visual neuron is the area of visual space over which the cell responds to visual stimuli. It is well established, however, that the discharge produced by an optimal stimulus can be modulated by the presence of additional stimuli that by themselves do not produce any response. This study examines inhibitory influences that originate from areas located outside of the classical (i.e., excitatory) receptive field. Previous work has shown that for some cells the response to a properly oriented bar of light becomes attenuated when the bar extends beyond the receptive field, a phenomenon known as end-inhibition (or length tuning). Analogously, it has been shown that increasing the number of cycles of a drifting grating stimulus may also inhibit the firing of some cells, an effect known as side-inhibition (or width tuning). Very little information is available, however, about the relationship between end- and side-inhibition. We have examined ...

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

Journal of neurophysiology, 1992

1. The response to an optimally oriented stimulus of both simple and complex cells in the cat's striate visual cortex (area 17) can be suppressed by the superposition of an orthogonally oriented drifting grating. This effect is referred to as cross-orientation suppression. We have examined the spatial organization and tuning characteristics of this suppressive effect with the use of extracellular recording techniques. 2. For a total of 75 neurons, we have measured the size of each cell's excitatory receptive field by use of rectangular patches of drifting sinusoidal gratings presented at the optimal orientation and spatial frequency. The length and width of these grating patches are varied independently. Receptive-field length and width are determined from the dimensions of the smallest grating patch required to elicit a maximal response. 3. The extent of the area from which cross-orientation suppression originates has been measured in an analogous manner. Each neuron is exc...

Effects of stimulus spatial frequency, size, and luminance contrast on orientation tuning of neurons in the dorsal lateral geniculate nucleus of cat

Neuroscience Research, 2013

It is generally thought that orientation selectivity first appears in the primary visual cortex (V1), whereas neurons in the lateral geniculate nucleus (LGN), an input source for V1, are thought to be insensitive to stimulus orientation. Here we show that increasing both the spatial frequency and size of the grating stimuli beyond their respective optimal values strongly enhance the orientation tuning of LGN neurons. The resulting orientation tuning was clearly contrast-invariant. Furthermore, blocking intrathalamic inhibition by iontophoretically administering ␥-aminobutyric acid (GABA) A receptor antagonists, such as bicuculline and GABAzine, slightly but significantly weakened the contrast invariance. Our results suggest that orientation tuning in the LGN is caused by an elliptical classical receptive field and orientation-tuned surround suppression, and that its contrast invariance is ensured by local GABA A inhibition. This contrastinvariant orientation tuning in LGN neurons may contribute to the contrast-invariant orientation tuning seen in V1 neurons.

Contribution of GABAergic Inhibition to Receptive Field Structures of Monkey Inferior Temporal Neurons

Cerebral Cortex, 2002

Receptive field (RF) structures of neurons in area TE of the monkey inferior temporal cortex were investigated under blockade of inhibition mediated by γ-aminobutyric acid (GABA). Bicuculline methiodide, a GABA A receptor antagonist, was microiontophoretically administered to TE neurons. Blockade of inhibition enhanced responses to a particular range of visual stimuli not only at the RF center, but also at the periphery of or outside RFs where the stimuli originally evoked little or no response, enlarging the RFs. The strongest responses under normal and disinhibited conditions occurred at the RF center in most neurons. The largest increase in responses, reflecting the strongest inhibitory input, usually occurred at the RF center, but in some neurons it occurred in the periphery. A neuron had a silent region within its RF where some stimuli effective at adjacent locations could not elicit responses even under blockade of inhibition. We suggest that (i) afferent information to individual TE neurons originates from a wide retinotopic region beyond their normal RF; (ii) the afferent convergence is not necessarily complete throughout a RF; and (iii) GABAergic inhibition contributes to the generation of RF structures of TE neurons.

Spatiotemporal characteristics of surround suppression in primary visual cortex and lateral geniculate nucleus of the cat

Journal of Neurophysiology, 2014

In the primary visual cortex (V1), a neuronal response to stimulation of the classical receptive field (CRF) is predominantly suppressed by a stimulus presented outside the CRF (extraclassical receptive field, ECRF), a phenomenon referred to as ECRF suppression. To elucidate the neuronal mechanisms and origin of ECRF suppression in V1 of anesthetized cats, we examined the temporal properties of the spatial extent and orientation specificity of ECRF suppression in V1 and the lateral geniculate nucleus (LGN), using stationary-flashed sinusoidal grating. In V1, we found three components of ECRF suppression: 1) local and fast, 2) global and fast, and 3) global and late. The local and fast component, which resulted from within 2° of the boundary of the CRF, started no more than 10 ms after the onset of the CRF response and exhibited low specificity for the orientation of the ECRF stimulus. These spatiotemporal properties corresponded to those of geniculate ECRF suppression, suggesting th...

The influence of GABAergic inhibitory processes on the receptive field structure of X and Y cells in cat dorsal lateral geniculate nucleus (dLGN)

Brain Research, 1983

Key words: X and Y cells --dorsolateral geniculate nucleus --centre surround antagonism --GABA --inhibitory processes Visually elicited inhibitory processes, underlying the receptive field structure of cells in layers A and A 1 of the cat dorsal lateral geniculate nucleus (dLGN), have been examined by a combination of visual neurophysiological and iontophoretic techniques. Discrete visual stimulation of both centre and surround mechanisms, produced a powerful suppression of the elevated background discharge levels induced by iontophoretic application of an excitatory amino acid. These observations are consistent with the activation of a postsynaptic inhibitory input, a view supported by the fact that the suppressive effects were blocked by iontophoretic application of bicuculline, an antagonist of GABA, a putative inhibitory transmitter in the dLGN. These inhibitory effects were always elicited by the opposite phase of a flashed stimulus to that eliciting responses associated with the receptive field region. That is 'on' inhibitory effects were elicited from 'off' excitatory regions and 'off' inhibitory effects from 'on' excitatory regions.

Inhibitory contributions to spatiotemporal receptive-field structure and direction selectivity in simple cells of cat area 17

Journal of neurophysiology, 1999

Intracortical inhibition contributes to direction selectivity in primary visual cortex, but how it acts has been unclear. We investigated this problem in simple cells of cat area 17 by taking advantage of the link between spatiotemporal (S-T) receptive-field structure and direction selectivity. Most cells in layer 4 have S-T-oriented receptive fields in which gradients of response timing across the field confer a preferred direction of motion. Linear summation of responses across the receptive field, followed by a static nonlinear amplification, has been shown previously to account for directional tuning in layer 4. We tested the hypotheses that inhibition acts by altering S-T structure or the static nonlinearity or both. Drifting and counterphasing sine wave gratings were used to measure direction selectivity and S-T structure, respectively, in 17 layer 4 simple cells before and during iontophoresis of bicuculline methiodide (BMI), a GABAA antagonist. S-T orientation was quantified...

Quantitative measurements of receptive field changes during antagonism of GABAergic transmission in primary somatosensory cortex of cats

Experimental Brain Research, 1989

In cortical area 3b of cats, responses of 76 single neurons to punctate indentations were recorded before and during iontophoretic administration of bicuculline methiodide (BMI), a GABAergic antagonist, at levels that did not affect spontaneous activity. Constant amplitude indentations were applied to selected sites along distalproximal and radial-ulnar axes that intersected the most sensitive area in the receptive field. Profiles of response magnitudes were used to measure receptive field dimensions before and during antagonism of GABAergic inhibition. Blockade of GABAergic transmission caused receptive field dimensions of 48 rapidly-adapting neurons to increase an average 141%, or nearly 2.5 times their original size. Analysis of the spatial distribution of inhibition indicated that in-field inhibition was larger than surround inhibition. During BMI administration, response latency was significantly longer for response elicited from the expanded territory than for responses elicited from within the original receptive field, suggesting that receptive field expansion might be mediated by multisynaptic intracortical connections. The magnitude of receptive field expansion was independent of receptive field size or peripheral location. In a substantial number of neurons, however, BMI produced asymmetric expansions that extended only in the proximal direction. For 9 slowly-adapting neurons, BMI produced measureable increases in receptive field dimensions, but these changes were significantly smaller than the changes in rapidly-adapting neurons.