Neural responses in the primary visual cortex of the monkey during perceptual filling-in at the blind spot

doi:10.1016/S0168-0102(02)00149-9

Neuroscience Research

Volume 44, Issue 3, November 2002, Pages 231-236

https://doi.org/10.1016/S0168-0102(02)00149-9 Get rights and content

Abstract

The phenomenon of perceptual filling-in demonstrates that physical stimuli presented on the retina do not necessarily correspond to surface perception, and that our visual system has mechanisms with which to interpolate missing information in order to construct continuous surfaces. Among its various forms, filling-in at the blind spot is one of the most remarkable. To study the neural mechanisms involved in filling-in at the blind spot, we recently conducted a recording experiment aimed at determining whether the neurons in the primary visual cortex (V1) that represent the visual field corresponding to the blind spot are activated when filling-in occurs. We found that neurons located in deep layers of the V1, particularly layer 6, respond to large stimuli that cover the blind spot and induce perceptual filling-in. These neurons tended to have very large receptive fields, which extended out of the blind spot, and preferred relatively large stimuli. We believe that neurons in the V1 region representing the blind spot encode information essential for perceptual filling-in at the blind spot.

Section snippets

Retinotopic map

A remarkable feature of vision that distinguishes it from other sensory modalities is its ability to precisely transmit information about the relative locations of objects in the outer world. This ability has its basis in the topographic organization of the visual system. Neural projections that send retinal information to the visual cortex have a precise retinotopic organization that faithfully reproduce a map of the visual field on the visual cortical surface (retinotopic map). When we see an

Filling-in and surface perception

Perceptual filling-in indicates certain kinds of phenomena in which one perceives visual attributes in a region of the visual field where the information is actually missing. Many forms of this phenomenon have been identified, with filling-in at the blind spot being one of the most remarkable examples. The optic disk on the retina is an area in which the blood vessels enter and the optic nerve exits (Fig. 1). This area of the retina contains no photoreceptors; consequently, when one sees a

Neuron activities in the retinotopic representation of the blind spot in V1

We recorded the activity of single neurons in V1 of awake Japanese monkeys (macaca fuscata) performing a visual fixation task. Before the recording experiment, we determined the location of the blind spot in the visual field using a visual saccade paradigm (Komatsu and Murakami, 1994): it was on the horizontal meridian at about 15° in eccentricity, and its size was about 5° horizontally and 7° vertically. We then used a small spot (0.3–1°) to map the visual receptive fields of the neurons

A possible mechanism of perceptual filling-in at the blind spot

So far, we have no direct evidence of a causal relationship between the activity of V1 neurons we observed and perceptual filling-in at the blind spot. However, a recent fMRI study in human subjects suggests that indeed neuronal activation in V1 closely correlates with perceptual filling-in at the blind spot (Tong and Engel, 2001). If so, how are neurons in the BS representation involved? One fact that we find particularly interesting is that these neurons are mainly located in layer 6, a

Relation to other completion phenomena

There have been several studies investigating neural correlates of various kinds of perceptual filling-in and completion in the visual cortex. For instance, it has been shown that neural activity in V1 correlates with the perceptual outcome of some phenomena related to filling-in, including brightness induction (Rossi et al., 1996, Kinoshita and Komatsu, 2001) or amodal completion (Sugita, 1999). Other studies, however, have suggested the involvement of higher visual areas in such phenomena as

Acknowledgements

This work is supported by the RFTF (‘Research for the Future’ Program) from the JSPS (The Japan Society for the Promotion of Science; JSPS-RFTF96L00202) and by Grant 08279102 from the Japanese Ministry of Education.

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Cited by (35)

Extrastriate activity reflects the absence of local retinal input
2023, Consciousness and Cognition
The physiological blind spot corresponds to the optic disc where the retina contains no light-detecting photoreceptor cells. Our perception seemingly fills in this gap in input. Here we suggest that rather than an active process, such perceptual filling-in could instead be a consequence of the integration of visual inputs at higher stages of processing discounting the local absence of retinal input. Using functional brain imaging, we resolved the retinotopic representation of the physiological blind spot in early human visual cortex and measured responses while participants perceived filling-in. Responses in early visual areas simply reflected the absence of visual input. In contrast, higher extrastriate regions responded more to stimuli in the eye containing the blind spot than the fellow eye. However, this signature was independent of filling-in. We argue that these findings agree with philosophical accounts that posit that the concept of filling-in of absent retinal input is unnecessary.
Filled/non-filled pairs: An empirical challenge to the integrated information theory of consciousness
2022, Consciousness and Cognition
Perceptual filling-in for vision is the insertion of visual properties (e.g., color, contour, luminance, or motion) into one’s visual field, when those properties have no corresponding retinal input. This paper introduces and provides preliminary empirical support for filled/non-filled pairs, pairs of images that appear identical, yet differ by amount of filling-in. It is argued that such image pairs are important to the experimental testing of theories of consciousness. We review recent experimental research and conclude that filling-in involves brain activity with relatively high integrated information ( $Φ$ ) compared to veridical visual perceptions. We then present filled/non-filled pairs as an empirical challenge to the integrated information theory of consciousness, which predicts that phenomenologically identical experiences depend on brain processes with identical $Φ$ .
Central mechanisms of perceptual filling-in
2019, Current Opinion in Behavioral Sciences
Citation Excerpt :
The same adapting pattern induced multiple colored afterimages depending on the configuration of the test contours [58–61]. Some previous imaging studies indicated a role for retinotopic activity in early visual areas such as V1 in the processing of uniform surfaces [62–64] and also in the processing of patterns presented at the natural blind spot [65–67]. This interpretation has been disputed [68] by showing that surround induced responses in V1, in fact, depend on an extended edge response.
Human observers generally perceive a stable and coherent visual scene despite the fact that sensory information is ambiguous and often incomplete. Perceptual filling-in provides an interesting example of how the visual system realizes perceptual inferences from incomplete information. Vision scientists have a long history studying filling-in phenomena in the context of surface color filling-in. While significant progress has been achieved with behavioral experiments, little is known about the neural substrate of perceptual filling-in. We explored several hypotheses that have been considered to determine how the neural representation of edge-induced filling-in percepts arises in the brain. We argue that the visual system uses distinct extra-striate pathways for the processing of chromatic surfaces generated by edge-dependent filling-in that indirectly influence color pathways via a contour integration mechanism. Such a mechanism may play an important role in figure/ground segregation. Finally, we highlight the potential role of feedback projections that are ignored in many models despite the fact that they are as numerous as feedforward projections.
Characteristics of the filled-in surface at the blind spot
2012, Vision Research
Citation Excerpt :
This filling-in process is rather remarkable given the relatively large size of the blind spot, which encompasses an ellipse with long and short axes subtending about 6° in width and 8° in height (Armaly, 1969). Neurophysiological studies have demonstrated that the filled-in information is not merely conceptually noted (Dennett, 1992) but is represented by lateral propagation of neural activity (Komatsu, Kinoshita, & Murakami, 2002; Matsumoto & Komatsu, 2005; Pessoa, Thompson, & Noë, 1998). Due to the active propagation of neural activity from the regions surrounding the blind spot, cortical neurons that have receptive fields corresponding to the blind spot can respond to stimulation imaged within the blind spot region.
Our visual system can restore information missing within the portion of the retinal image corresponding to the blind spot where the optic nerve exits the eye. Previous studies of the properties of filled-in surfaces at the blind spot have found similarities and dissimilarities between filled-in and real surfaces and have therefore not provided a consistent view of the characteristics of the filled-in surface. First, we investigated whether filling-in utilizes a contour integration mechanism. Gratings with collinear lines filled in the blind spot more effectively than those both with orthogonal lines and without any line, suggesting that collinear facilitation underlies the filling-in of the blind spot. Second, the dynamics of binocular rivalry was examined by comparing the dominance duration distributions of filled-in and real surfaces. The results indicated that the strength of the filled-in surface was attenuated compared to that of the real surface during rivalry. Lastly, we tested whether travelling waves of dominance in rivalry could occur at the blind spot. The travelling waves could propagate through a hole only at the blind spot, suggesting that the filled-in surface helps perceptual waves to travel across the blind spot. These results suggest that the filled-in surface shares a common mechanism via a horizontal connection but that it has weak strength to suppress the opposite eye during binocular viewing.
Primary sensory cortices, top-down projections and conscious experience
2011, Progress in Neurobiology
Citation Excerpt :
In assessing the role of the primary visual cortex (V1) in the generation of conscious visual experience, neuroscientists have exploited the fact that experience is not a facsimile of external reality: under certain conditions, what we see is different from what physically impacts the retina. Such conditions include, for instance, visual illusions (von der Heydt et al., 1984; Grosof et al., 1993; Lee and Nguyen, 2001; Komatsu et al., 2002; Sasaki and Watanabe, 2004; Meng et al., 2005; Muckli et al., 2005; Murray et al., 2006; Sterzer et al., 2006; Watkins et al., 2006), masking paradigms (Macknik and Haglund, 1999; Haynes et al., 2005), binocular rivalry (Leopold and Logothetis, 1996; Fries et al., 1997; Sheinberg and Logothetis, 1997; Polonsky et al., 2000; Tong and Engel, 2001; Gail et al., 2004; Lee et al., 2005, 2007; Meng et al., 2005), generalized flash suppression (Wilke et al., 2006; Maier et al., 2008), near-threshold stimuli (which, although present, are not always perceived; Pins and ffytche, 2003; Ress and Heeger, 2003) and situations in which we “see with the mind's eye” (Le Bihan et al., 1993; Kosslyn et al., 1995, 1999; Klein et al., 2000; Harrison and Tong, 2009; Serences et al., 2009). The crucial question, in each case, is whether neural activity in V1 reflects more closely the visual information present in the retina or, instead, the visual mental images of the subject.
Beginning with a prominent article by Crick and Koch in 1995 (Nature 375, 121–123), cognitive neuroscience has witnessed an intensive debate about whether or not neural activity in primary visual cortex correlates with conscious visual experience. While some studies – especially those employing functional magnetic resonance imaging – imply that this is the case, others – particularly those recording from single neurons – suggest that it is not. In the light of this ongoing controversy, it is surprising that the analogous question in other sensory modalities has received far less attention. The first part of the present article reviews studies relevant to the role of primary auditory and primary somatosensory cortices in conscious auditory and tactile experience. As will become evident, the results of these studies, at least at first sight, appear no less contradictory than those obtained in the visual modality – in fact, they evidence discrepancies that resemble those found in the visual system to an impressive degree. The second part of the article attempts to reconcile the seemingly contradictory data by suggesting that only activity induced in the primary sensory cortices through cortico-cortical top-down signals can become consciously accessible, whereas activity induced by bottom-up signals from the thalamus cannot. This conclusion is in line with the earlier proposals of several prominent neuroscientists that portrayed conscious perception as the result of an active interpretative process by the brain, rather than a passive reflection of the environment.
A new taxonomy for perceptual filling-in
2011, Brain Research Reviews
Citation Excerpt :
Moreover, spatial alignment thresholds in healthy humans are lower across the blind spot than across intact retina (Crossland and Bex, 2009), consistent with involvement of a low-level mechanism in perceptual filling-in at the blind spot. Single cell recordings from anaesthetized monkeys show that when filling-in takes place at the blind spot, neural responses are generated at the retinotopic representation of the blind spot in primary visual cortex (Fiorani et al., 1992; Matsumoto and Komatsu, 2005; Komatsu et al., 2002). Some V1 neurons activated during perceptual filling-in at the blind spot have large receptive fields, extending out of the blind spot (Komatsu et al., 2002), suggesting the passive importing of information from the surrounding visual field.
Perceptual filling-in occurs when structures of the visual system interpolate information across regions of visual space where that information is physically absent. It is a ubiquitous and heterogeneous phenomenon, which takes place in different forms almost every time we view the world around us, such as when objects are occluded by other objects or when they fall behind the blind spot. Yet, to date, there is no clear framework for relating these various forms of perceptual filling-in. Similarly, whether these and other forms of filling-in share common mechanisms is not yet known. Here we present a new taxonomy to categorize the different forms of perceptual filling-in. We then examine experimental evidence for the processes involved in each type of perceptual filling-in. Finally, we use established theories of general surface perception to show how contextualizing filling-in using this framework broadens our understanding of the possible shared mechanisms underlying perceptual filling-in. In particular, we consider the importance of the presence of boundaries in determining the phenomenal experience of perceptual filling-in.

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¹: Present address: The Rockefeller University, 1230 York Avenue, New York, NY 10021, USA.

²: Present address: Human and Information Science Laboratory, NTT Communication Science Laboratories, NTT Corporation, 3-1 Morinosato Wakamiya, Atsugi, Kanagawa 243-0198, Japan.

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Update articleNeural responses in the primary visual cortex of the monkey during perceptual filling-in at the blind spot

Abstract

Section snippets

Retinotopic map

Filling-in and surface perception

Neuron activities in the retinotopic representation of the blind spot in V1

A possible mechanism of perceptual filling-in at the blind spot

Relation to other completion phenomena

Acknowledgements

Vision Res.

Vision Res.

Cognitive Brain Res.

Receptive-field properties of deafferentiated visual cortical neurons after topographic map reorganization in adult cats

J. Neurosci.

Visual Perception

Responses of cells in monkey visual cortex during perceptual filling-in of an artificial scotoma

Nature

Dynamic surrounds of receptive fields in primate striate cortex: a physiological basis for perceptual completion?

Proc. Natl. Acad. Sci. USA

Laminar differences in receptive field properties of cells in cat primary visual cortex

J. Physiol. (Lond.)

The projections of cells in different layers of the cat's visual cortex

J. Comp. Neurol.

Receptive field dynamics in adult primary visual cortex