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Ben S Webb

Publications and source records attributed to Ben S Webb.

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Early and late mechanisms of surround suppression in striate cortex of macaque.

The response of a neuron in striate cortex to an optimally configured visual stimulus is generally reduced when the stimulus is enlarged to encroach on a suppressive region that surrounds its classical receptive field (CRF). To characterize the mechanism that gives rise to this suppression, we measured its spatiotemporal tuning, its susceptibility to contrast adaptation, and its capacity for interocular transfer. Responses to an optimally configured grating confined to the CRF were strongly suppressed by annular surrounding gratings drifting at a wide range of temporal and spatial frequencies (including spatially uniform fields) that extended from well below to well above the range that drives most cortical neurons. Suppression from gratings capable of driving cortical CRFs was profoundly reduced by contrast adaptation and showed substantial interocular transfer. Suppression from stimuli that lay outside the spatiotemporal passband of most cortical CRFs was relatively stronger when the stimulus on the CRF was of low contrast, was generally insusceptible to contrast adaptation, and showed little interocular transfer. Our findings point to the existence of two mechanisms of surround suppression: one that is prominent when high-contrast stimuli drive the CRF, is orientation selective, has relatively sharp spatiotemporal tuning, is binocularly driven, and can be substantially desensitized by adaptation; the other is relatively more prominent when low-contrast stimuli drive the CRF, has very broad spatiotemporal tuning, is monocularly driven, and is insusceptible to adaptation. Its character suggests an origin in the input layers of primary visual cortex, or earlier.

Animals↗

Spatial distribution of suppressive signals outside the classical receptive field in lateral geniculate nucleus.

A suppressive surround modulates the responsiveness of cells in the lateral geniculate nucleus (LGN), but we know nothing of its spatial structure or the way in which it combines signals arising from different locations. It is generally assumed that suppressive signals are either uniformly distributed or balanced in opposing regions outside the receptive field. Here, we examine the spatial distribution and summation of suppressive signals outside the receptive field in extracellular recordings from 46 LGN cells in anesthetized marmosets. The receptive field of each cell was stimulated with a drifting sinusoidal grating of the preferred size and spatial and temporal frequency; we probed different positions in the suppressive surround with either a large half-annular grating or a small circular grating patch of the preferred spatial and temporal frequency. In many of the cells with a strong suppressive surround (29/46), the spatial distribution of suppression showed clear deviation from circular symmetry. In the majority of these of cells, suppressive signals were spatially asymmetrical or balanced in opposing areas outside the receptive field. A suppressive area was larger than the classical receptive field itself and spatial summation within and between these areas was nonlinear. There was no bias for suppression to arise from foveal or nasal retina where cone density is higher and no other sign of a systematic spatial organization to the suppressive surround. We conclude that nonclassical suppressive signals in LGN deviate from circular symmetry and are nonlinearly combined.

Action Potentials↗

Visual system: how is the retina wired up to the cortex?

A single retinal output neuron transmits to primary visual cortex through multiple pathways with different strengths. A new study in which activity was simultaneously recorded in pairs of retinal and cortical neurons provides evidence that these pathways converge on a single cortical neuron.

Animals↗

The nature of V1 neural responses to 2D moving patterns depends on receptive-field structure in the marmoset monkey.

A plaid pattern is formed when two sinusoidal gratings of different orientations are added together. Previous work has shown that V1 neurons selectively encode the direction and orientation of the component gratings in a moving plaid but not the direction of the plaid itself (Movshon et al. 1985). We recorded the responses of 49 direction-selective neurons to moving gratings and plaid patterns in area V1 of the anesthetized marmoset monkey (Callithrix jacchus). The responses of V1 neurons to rectangular patches of varying lengths and widths containing gratings of optimal spatial frequency were used to measure size and aspect ratio of the receptive-field subunits. We measured responses to plaid patterns moving in different directions and graded the magnitude of the response to the direction of motion of the plaid and the response to the direction of motion of the component gratings. We found significant correlations between receptive-field structure and the type and strength of its response to moving plaid patterns. The strength of pattern and component responses was significantly correlated with the interrelated properties of direction tuning width (Spearman's r = 0.82, P < 0.001), and receptive-field subunit aspect ratio (Spearman's r = -0.79, P < 0.001). Neurons with broad direction tuning and short, wide receptive-field subunits gave their greatest response when the plaid moved in their preferred direction. Conversely, neurons with narrow direction tuning and long, narrow receptive-field subunits gave their greatest responses when the plaid moved in a direction such that one of its components moved in the preferred direction.

Animals↗

The uses of colour vision: behavioural and physiological distinctiveness of colour stimuli.

Colour and greyscale (black and white) pictures look different to us, but it is not clear whether the difference in appearance is a consequence of the way our visual system uses colour signals or a by-product of our experience. In principle, colour images are qualitatively different from greyscale images because they make it possible to use different processing strategies. Colour signals provide important cues for segmenting the image into areas that represent different objects and for linking together areas that represent the same object. If this property of colour signals is exploited in visual processing we would expect colour stimuli to look different, as a class, from greyscale stimuli. We would also expect that adding colour signals to greyscale signals should change the way that those signals are processed. We have investigated these questions in behavioural and in physiological experiments. We find that male marmosets (all of which are dichromats) rapidly learn to distinguish between colour and greyscale copies of the same images. The discrimination transfers to new image pairs, to new colours and to image pairs in which the colour and greyscale images are spatially different. We find that, in a proportion of neurons recorded in the marmoset visual cortex, colour-shifts in opposite directions produce similar enhancements of the response to a luminance stimulus. We conclude that colour is, both behaviourally and physiologically, a distinctive property of images.

Animals↗

Feedback from V1 and inhibition from beyond the classical receptive field modulates the responses of neurons in the primate lateral geniculate nucleus.

It is well established that the responses of neurons in the lateral geniculate nucleus (LGN) can be modulated by feedback from visual cortex, but it is still unclear how cortico-geniculate afferents regulate the flow of visual information to the cortex in the primate. Here we report the effects, on the gain of LGN neurons, of differentially stimulating the extraclassical receptive field, with feedback from the striate cortex intact or inactivated in the marmoset monkey, Callithrix jacchus. A horizontally oriented grating of optimal size, spatial frequency, and temporal frequency was presented to the classical receptive field. The grating varied in contrast (range: 0-1) from trial to trial, and was presented alone, or surrounded by a grating of the same or orthogonal orientation, contained within either a larger annular field, or flanks oriented either horizontally or vertically. V1 was ablated to inactivate cortico-geniculate feedback. The maximum firing rate of LGN neurons was greater with V1 intact, but was reduced by visually stimulating beyond the classical receptive field. Large horizontal or vertical annular gratings were most effective in reducing the maximum firing rate of LGN neurons. Magnocellular neurons were most susceptible to this inhibition from beyond the classical receptive field. Extraclassical inhibition was less effective with V1 ablated. We conclude that inhibition from beyond the classical receptive field reduces the excitatory influence of V1 in the LGN. The net balance between cortico-geniculate excitation and inhibition from beyond the classical receptive field is one mechanism by which signals relayed from the retina to V1 are controlled.

Animals↗

Gain control from beyond the classical receptive field in primate primary visual cortex.

Gain control is a salient feature of information processing throughout the visual system. Heeger (1991, 1992) described a mechanism that could underpin gain control in primary visual cortex (V1). According to this model, a neuron's response is normalized by dividing its output by the sum of a population of neurons, which are selective for orientations covering a broad range. Gain control in this scheme is manifested as a change in the semisaturation constant (contrast gain) of a V1 neuron. Here we examine how flanking and annular gratings of the same or orthogonal orientation to that preferred by a neuron presented beyond the receptive field modulate gain in V1 neurons in anesthetized marmosets (Callithrix jacchus). To characterize how gain was modulated by surround stimuli, the Michaelis-Menten equation was fitted to response versus contrast functions obtained under each stimulus condition. The modulation of gain by surround stimuli was modelled best as a divisive reduction in response gain. Response gain varied with the orientation of surround stimuli, but was reduced most when the orientation of a large annular grating beyond the classical receptive field matched the preferred orientation of neurons. The strength of surround suppression did not vary significantly with retinal eccentricity or laminar distribution. In the marmoset, as in macaques (Angelucci et al., 2002a,b), gain control over the sort of distances reported here (up to 10 deg) may be mediated by feedback from extrastriate areas.

Animals↗