Spatial Resolution for Feature Binding Is Impaired in Peripheral and Amblyopic Vision

Abstract

Neri, Peter and Dennis M. Levi. Spatial resolution for feature binding is impaired in peripheral and amblyopic vision. J Neurophysiol 96: 142-153, 2006. First published January 18, 2006 doi:10.1152/jn.01261.2005. We measured spatial resolution for discriminating targets that differed from nearby distractors in either color or orientation or their conjunction. In the fovea of normal human observers, whenever both attributes are big enough to be individually visible, their conjunction is also visible. In the periphery, the two attributes may be visible, but their conjunction may be invisible. We found a similar impairment in resolving conjunctions for the fovea of deprived eyes of humans with abnormal visual development (amblyopia). These results are quantitatively explained by a model of primary visual cortex (V1) in which orientation and color maps are imperfectly co-registered topographically. Our results in persons with amblyopia indicate that the ability of the fovea to compensate for this poor co-registration is consolidated by visual experience during postnatal development. I N T R O D U C T I O NWe perceive individual objects as possessing multiple attributes: a red ball falls behind a brown fence. This perceptual representation combines four different attributes (color, shape, motion, and depth) and provides an example of feature binding (Treisman 1998).Feature binding can fail (Treisman 1996). When this occurs, normal observers experience illusory conjunctions of physically disjunct features (Treisman and Schmidt 1982;Wolfe and Cave 1999). The failure is chronic in patients with subcortical (Ward et al. 2002) but particularly cortical (Cohan and Rafal 1991) damage like visual neglect (Eglin et al. 1989;Estermann et al. 2000) and Balint's syndrome Robertson et al. 1997), and there is some evidence for impaired binding in schizophrenia (Alain et al. 2002). Our goal was to identify and measure aspects of the visual stimulus that lead to selective failure of feature binding in both normal and pathological vision.We focused on the ability to resolve small visual items. We chose this measure for two reasons. First, the assessment of resolution has a well-established history in visual psychophysics and can be easily related to the physiological concept of neuronal receptive fields (RFs) . Second, it pertains directly to a major issue and currently active debate in contemporary neuroscience: how the representation of space (and its resolution) "glues" together separate representations of object properties (Treisman 1998;Yu et al. 2005). We opted for a design that allowed us to factor out potential effects of crowding (Parkes et al. 2001), working memory (Luck and Vogel 1997), and coarse attentional deployment (Treisman 1998;Yu et al. 2005). We achieved this by normalizing the spatial resolution for binding features (orientation and color) by the resolution for discriminating features individually (orientation or color), in almost identical stimuli.We found that the resolution for binding features is much coarse...

Positional averaging explains crowding with letter-like stimuli

“…In other words, the deleterious effects of crowding on position encoding can be accounted for by simple recourse to the inherent positional uncertainty in the peripheral visual field (18)(19)(20). This aspect of our model is similar to a recent model of feature binding (37), where the high positional noise in the periphery causes target features to be erroneously associated with adjacent elements within coarse feature maps. Additionally, because there are also intrinsic levels of uncertainty in other domains affected by crowding (3-6), such as orientation (38) and direction (39), our model raises the intriguing possibility that crowding could involve the averaging of features across all affected modalities, as opposed to the addition of noise suggested by the historic focus on error rates in crowding tasks.…”

Saccade-confounded image statistics explain visual crowding

“…Our quantitative results illustrate an important aspect of the anomalous contextual interactions underlying crowding that has not been fully explored empirically: diminished binding of target features 35 due to proximal weakening of connectivity combined with inappropriate and spurious binding of distracter features due to distal strengthening of connectivity in the lateral interaction zone. This dual nature of the binding deficiency explains our previous finding with classification images that crowding reduces the use of valid features while at the same increasing the number of invalid features used by the visual system 5 .…”

Precise discrimination of object position in the human pulvinar

“…Allocating spatial attention has been hypothesized as a possible function of the pulvinar (Bender and Youakim 2001; Petersen, et al 1987), and with the spatial resolution reported here of 0.05E or better (where E is the eccentricity from fixation), highly precise spatial attention could be supported by the right hemisphere pulvinar. Neri and Levi (2006) report the resolution of feature binding at about 0.11E for a dense stimulus array and about 0.06E for a sparse array, so the precision of spatial coding in the pulvinar is also fine enough to account for these data. If the pulvinar is involved in feature binding, the coarser resolution for feature binding could be due to downstream noise, or to wiring scatter as proposed by Neri & Levi (2006).…”

“…Neri and Levi (2006) report the resolution of feature binding at about 0.11E for a dense stimulus array and about 0.06E for a sparse array, so the precision of spatial coding in the pulvinar is also fine enough to account for these data. If the pulvinar is involved in feature binding, the coarser resolution for feature binding could be due to downstream noise, or to wiring scatter as proposed by Neri & Levi (2006). The lateralization that we report is consistent with several previous findings, including the implication of the pulvinar in spatial neglect (Karnath, et al 2002) and the prospect that spatial attention is dominated by the right hemisphere (Mapstone, et al 2003; Mesulam 1999).…”