Ben S. Webb

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.

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.

Perceptual learning reduces crowding in amblyopia and in the normal periphery

Amblyopia is a developmental visual disorder of cortical origin, characterized by crowding and poor acuity in central vision of the affected eye. Crowding refers to the adverse effects of surrounding items on object identification, common only in normal peripheral but not central vision. We trained a group of adult human amblyopes on a crowded letter identification task to assess whether the crowding problem can be ameliorated. Letter size was fixed well above the acuity limit, and letter spacing was varied to obtain spacing thresholds for central target identification. Normally sighted observers practiced the same task in their lower peripheral visual field. Independent measures of acuity were taken in flanked and unflanked conditions before and after training to measure crowding ratios at three fixed letter separations. Practice improved the letter spacing thresholds of both groups on the training task, and crowding ratios were reduced after posttest. The reductions in crowding in amblyopes were associated with improvements in standard measures of visual acuity. Thus, perceptual learning reduced the deleterious effects of crowding in amblyopia and in the normal periphery. The results support the effectiveness of plasticity-based approaches for improving vision in adult amblyopes and suggest experience-dependent effects on the cortical substrates of crowding.

Can perceptual learning be used to treat amblyopia beyond the critical period of visual development

Citation information: Astle AT, Webb BS & McGraw PV. Can perceptual learning be used to treat amblyopia beyond the critical period of visual development? Ophthalmic Physiol Opt 2011, 31, 564–573. doi: 10.1111/j.1475‐1313.2011.00873.x

Cortical pooling algorithms for judging global motion direction

Physiological studies suggest that decision networks read from the neural representation in the middle temporal area to determine the perceived direction of visual motion, whereas psychophysical studies tend to characterize motion perception in terms of the statistical properties of stimuli. To reconcile these different approaches, we examined whether estimating the central tendency of the physical direction of global motion was a better indicator of perceived direction than algorithms (e.g., maximum likelihood) that read from directionally tuned mechanisms near the end of the motion pathway. The task of human observers was to discriminate the global direction of random dot kinematograms composed of asymmetrical distributions of local directions with distinct measures of central tendency. None of the statistical measures of image direction central tendency provided consistently accurate predictions of perceived global motion direction. However, regardless of the local composition of motion directions, a maximum-likelihood decoder produced global motion estimates commensurate with the psychophysical data. Our results suggest that mechanism-based, read-out algorithms offer a more accurate and robust guide to human motion perception than any stimulus-based, statistical estimate of central tendency.

Recovery of stereo acuity in adults with amblyopia.

Disruption of visual input to one eye during early development leads to marked functional impairments of vision, commonly referred to as amblyopia. A major consequence of amblyopia is the inability to encode binocular disparity information leading to impaired depth perception or stereo acuity. If amblyopia is treated early in life (before 4 years of age), then recovery of normal stereoscopic function is possible. Treatment is rarely undertaken later in life (adulthood) because declining levels of neural plasticity are thought to limit the effectiveness of standard treatments. Here, the authors show that a learning-based therapy, designed to exploit experience-dependent plastic mechanisms, can be used to recover stereoscopic visual function in adults with amblyopia. These cases challenge the long-held dogma that the critical period for visual development and the window for treating amblyopia are one and the same.

A Weber-like law for perceptual learning.

What determines how much an organism can learn? One possibility is that the neural factors that limit sensory performance prior to learning, place an upper limit on the amount of learning that can take place. We tested this idea by comparing learning on a sensory task where performance is limited by cortical mechanisms, at two retinal eccentricities. Prior to learning, visual performance at the two eccentricities was either unmatched or equated in two different ways (through spatial scaling or visual crowding). The magnitude of learning was equivalent when initial levels of performance were matched regardless of how performance was equated. The magnitude of learning was a constant proportion of initial performance. This Weber-like law for perceptual learning demonstrates that it should be possible to predict the degree of perceptual improvement and the final level of performance that can be achieved via sensory training, regardless of what cortical constraint limits performance.

Spatial frequency discrimination learning in normal and developmentally impaired human vision

Research highlights ► Amblyopic observers show greater learning compared to normal observers. ► Learning transfers asymmetrically from high to low spatial frequencies. ► Spatial frequency discrimination learning transfers to contrast sensitivity. ► Principles established may help develop more effective treatment protocols.

The Pattern of Learned Visual Improvements in Adult Amblyopia

PURPOSE Although amblyopia is diagnosed in terms of a monocular letter acuity loss, individuals typically present with deficits on a wide range of spatial tasks. Many of these deficits can be collapsed along two basic visual dimensions (visual acuity and contrast sensitivity) that together account for most of the variability in performance of the amblyopic visual system. In this study, this space was exploited, to target the main deficits and fully characterize the pattern of learned visual improvements in adult amblyopic subjects. METHODS Twenty-six amblyopic subjects (mean age, 39 ±12 years) were trained on one of four tasks, categorized as either visual acuity (letter or grating acuity) or contrast sensitivity (letter or grating contrast) tasks. Performance was measured on all tasks before and after training, to quantify learning along each dimension and generalization to the other dimension. Performance in 35 visually normal subjects (mean, age 24 ± 5 years) was used to establish normal variation in visual performance along each dimension, against which the learned improvements in amblyopic subjects was compared. RESULTS Training on the contrast sensitivity tasks produced substantial within-task learning and generalization to measures of visual acuity. The learned improvements in performance after training on the letter acuity task were also substantial, but did not generalize to contrast sensitivity. CONCLUSIONS Mapping the pattern of learning onto the known deficit space for amblyopia enabled the identification of tasks and stimulus configurations that optimized learning, guiding further development of learning-based interventions in this clinical group.

can Human amblyopia be Treated in adulthood

Amblyopia is a common visual disorder that results in a spatial acuity deficit in the affected eye. Orthodox treatment is to occlude the unaffected eye for lengthy periods, largely determined by the severity of the visual deficit at diagnosis. Although this treatment is not without its problems (poor compliance, potential to reduce binocular function, etc) it is effective in many children with moderate to severe amblyopia. Diagnosis and initiation of treatment early in life are thought to be critical to the success of this form of therapy. Occlusion is rarely undertaken in older children (more than 10 years old) as the visual benefits are considered to be marginal. Therefore, in subjects where occlusion is not effective or those missed by mass screening programs, there is no alternative therapy available later in life. More recently, burgeoning evidence has begun to reveal previously unrecognized levels of residual neural plasticity in the adult brain and scientists have developed new genetic, pharmacological, and behavioral interventions to activate these latent mechanisms in order to harness their potential for visual recovery. Prominent amongst these is the concept of perceptual learning—the fact that repeatedly practicing a challenging visual task leads to substantial and enduring improvements in visual performance over time. In the normal visual system the improvements are highly specific to the attributes of the trained stimulus. However, in the amblyopic visual system, learned improvements have been shown to generalize to novel tasks. In this paper we ask whether amblyopic deficits can be reduced in adulthood and explore the pattern of transfer of learned improvements. We also show that developing training protocols that target the deficit in stereo acuity allows the recovery of normal stereo function even in adulthood. This information will help guide further development of learning-based interventions in this clinical group.