A neuronal model of attentional spotlight: parietal guiding the temporal

doi:10.1016/S0165-0173(99)00005-3

Brain Research Reviews

Volume 30, Issue 1, July 1999, Pages 66-76

https://doi.org/10.1016/S0165-0173(99)00005-3 Get rights and content

Abstract

Recent studies have reported an attentional feedback that highlights neural responses as early along the visual pathway as the primary visual cortex. Such filtering would help in reducing informational overload and in performing serial visual search by directing attention to individual locations in the visual field. The magnocellular (M) and parvocellular (P) subdivisions are two of the major parallel pathways in primate vision that originate in the retina and carry distinctly different types of information. The M pathway, characterized by its high sensitivity to movement and to low contrast stimuli, forms the predominant visual input into the dorsal, parietal stream in the neocortex. The P inputs, characterized by their colour selectivity and higher spatial resolution, are channeled mainly into the ventral, temporal stream. It is proposed that the attentional spotlight originates in the dorsal stream and helps in serially searching the field for conjunction of the relevant target features in the temporal stream, effectively performing a gating function on all visual inputs. This model predicts that a defect limited to the magnocellular or the dorsal pathway can lead to widespread deficits in cognitive abilities, including those functions that are largely based on parvocellular information. For example, the model provides a neural mechanism linking a peripheral defect in the magnocellular pathway to the reading disabilities in dyslexia. Even though there has been strong evidence for a magnocellular deficit in dyslexia, the paradox has been that the cognitive disability seems to be related to P pathway function. The scheme proposed here shows how M input may be vital for controlling sequential attention during reading.

Introduction

Over the last 40 years, we have made considerable progress in our knowledge of the visual pathways, in particular through electrophysiological investigations regarding the trigger features of cells at various levels of the visual system and also from psychophysical studies in humans and other primates. However, the natural world differs substantially from the visual stimuli used in these studies in many ways. One important respect in which it differs is that stimuli in real life rarely occur in isolation and the visual system is often confronted with a multitude of stimuli of different shapes, sizes, colours, depths and speeds of movement. Nevertheless, we are able to focus attention on one object and process just the relevant information, sometimes even doing this covertly while foveating elsewhere. We are also able to employ visual search over a large scene and find, for example, a known face in a crowd fairly rapidly. While doing all this, we can also quite effortlessly bind different features of an object together, so that we can attribute correctly say, the yellow colour to the banana and the red to the apple. One puzzling aspect of this capability is a large body of evidence (see later) which suggests that different stimulus attributes like colour, form and motion may be processed in different areas of the brain. Given this, how is the binding of features made possible? A neuronal model that provides a framework for visual attention should be able to address these questions satisfactorily.

This paper will briefly review some of the psychophysical and neurophysiological studies that are relevant to this problem and propose a neuronal scheme that can explain these data and make testable predictions.

Section snippets

A model of attention that incorporates a novel view of convergence of parallel pathways in vision

In proposing a neurophysiological basis for attention, this paper builds upon concepts that have been derived largely from psychophysical experiments over the last 20 years. These ideas and the relevant literature on parallel pathways in vision will be reviewed first.

Psychophysical consequences

This neural account of selective attention explains a number of psychophysical observations that have been difficult to reconcile fully with Treisman's original Feature Integration Theory and seem to fit better with its modified version, namely the guided search model [100]. Treisman's early examples [83]of conjunctions that required serial search were features that would be largely processed by the parvocellular pathways and the ventral stream. They in fact showed the typical dependence on

Relation to other models

The scheme outlined here stresses the importance of spatial selection in visual attention as have some others 19, 83, 86. It seems to contradict the alternative idea that attentional selection could be the result of competition between objects for dominance over neural resources rather than due to an early spatial filter 27, 28, 29. This latter model has gained considerable currency in recent years with the finding of within-modality competition in attentional tasks and single unit studies

Conclusions

In the present scheme, the following factors determine the time taken for visual search.

(1) Which of the features defining the target can be processed by the magnocellular dominated dorsal stream. To the extent that one or more defining features can be processed by the dorsal stream, the search would be parallel and therefore faster.

(2) The sizes and spatial separation of the targets that need to be processed by the ventral stream. When objects are crowded together in the visual world, the

Acknowledgements

I wish to thank M.B. Calford, M. Cook, B. Dreher and G.H. Henry for helpful criticism and J. Cappello for technical assistance. The work is supported by a grant from the National Health and Medical Research Council of Australia.

References (104)

R.S Anderson et al.
Psychophysical evidence for a selective loss of M ganglion cells in glaucoma
Vision Res.
(1997)
E Ashbridge et al.
Temporal aspects of visual search studied by transcranial magnetic stimulation
Neuropsychologia
(1997)
E Borsting et al.
The presence of a magnocellular defect depends on the type of dyslexia
Vision Res.
(1996)
P.L Cornelissen et al.
Magnocellular visual function and children's single word reading
Vision Res.
(1998)
J Duncan et al.
Competitive brain activity in visual attention
Curr. Opin. Neurobiol.
(1997)
M.J Farah et al.
Parietal lobe mechanisms of spatial attention: modality-specific or supramodal?
Neuropsychologia
(1989)
J.C Greatrex et al.
The magnocellular deficit hypothesis in dyslexia: a review of reported evidence
Ophthalmic Physiol. Opt.
(1995)
R.W Guillery et al.
Paying attention to the thalamic reticular nucleus
Trends Neurosci.
(1998)
H.C Nothdurft
The role of features in preattentive vision: comparison of orientation, motion and color cues
Vision Res.
(1993)
A.J Richardson
Dyslexia, handedness and psychosis-proneness
Int. J. Psychophysiol.
(1994)

P.H Schiller

On the specificity of neurons and visual areas

Behav. Brain Res.

(1996)

T Shallice et al.

The possible role of selective attention in acquired dyslexia

Neuropsychologia

(1977)

B.C Skottun

Some remarks on the magnocellular deficit theory of dyslexia

Vision Res.

(1997)

J.F Stein

Developmental dyslexia, neural timing and hemispheric lateralisation

Int. J. Psychophysiol.

(1994)

J Stein et al.

To see but not to read; the magnocellular theory of dyslexia

Trends Neurosci.

(1997)

A Treisman

The binding problem

Curr. Opin. Neurobiol.

(1996)

A.M Treisman et al.

A feature integration theory of attention

Cognit. Psychol.

(1980)

D.J Withington-Wray et al.

A four-day period of bimodality auditory and visual experience is sufficient to permit normal emergence of the map of auditory space in the guinea pig superior colliculus

Neurosci. Lett.

(1990)

R.A Andersen

Multimodal integration for the representation of space in the posterior parietal cortex

Philos. Trans. R. Soc. London, Ser. B, Biol. Sci.

(1997)

R.A Andersen et al.

Multimodal representation of space in the posterior parietal cortex and its use in planning movements

Annu. Rev. Neurosci.

(1997)

D Badcock et al.

The effects of contrast, stimulus duration and spatial frequency on visible persistence in normal and specifically disabled readers

J. Exp. Psychol., Hum. Percept. Perform.

(1981)

G.G Blasdel et al.

Physiological organization of layer 4 in macaque striate cortex

J. Neurosci.

(1984)

D Boussaoud et al.

Visual topography of area TEO in the macaque

J. Comp. Neurol.

(1991)

D.L Braff

Information processing and attention dysfunctions in schizophrenia

Schizophr. Bull.

(1993)

J.R Brannan et al.

Allocation of visual attention in good and poor readers

Percept. Psychophysiol.

(1987)

B.G Breitmeyer

Unmasking visual masking: a look at the `why' behind the veil of the `how'

Psychol. Rev.

(1980)

D.C Burr et al.

Selective suppression of the magnocellular visual pathway during saccadic eye movements

Nature

(1994)

E.M Calloway

Local circuits in primary visual cortex of the macaque monkey

Annu. Rev. Neurosci.

(1998)

V Carr et al.

Schizophrenia: an information processing model

Aust. N. Z. J. Psychol.

(1986)

L Chelazzi et al.

A neural basis for visual search in inferior temporal cortex

Nature

(1993)

C.L Colby et al.

Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area

J. Neurophysiol.

(1996)

G.R Cole et al.

Visual interactions with luminance and chromatic stimuli

J. Opt. Soc. Am. A

(1990)

M Corbetta et al.

Superior parietal cortex activation during spatial attention shifts and visual feature conjunction

Science

(1995)

M Corbetta et al.

Human cortical mechanisms of visual attention during orienting and search

Philos. Trans. R. Soc. London, Ser. B

(1998)

B.A Cornblatt et al.

Impaired attention, genetics and the pathophysiology of schizophrenia

Schizophr. Bull.

(1994)

F Crick

Function of the thalamic reticular complex: the searchlight hypothesis

Proc. Natl. Acad. Sci. U.S.A.

(1984)

J.B Demb et al.

Functional magnetic resonance imaging of early visual pathways in dyslexia

J. Neurosci.

(1998)

R. Desimone, L.G. Ungerleider, Neural mechanisms of visual processing in monkeys, in: F. Boller, J. Grafman (Eds.),...

W.K Dong et al.

Somatosensory, multisensory, and task-related neurons in cortical area 7b (PF) of unanaesthetized monkeys

J. Neurophysiol.

(1994)

C.L Downing

Expectancy and visual–spatial attention effects on vision

J. Exp. Psychol., Hum. Percept. Perform.

(1988)

J Duncan

Coordination of what and where in visual attention

Perception

(1993)

J Duncan

Converging levels of analysis in the cognitive neuroscience of visual attention

Philos. Trans. R. Soc. London, Ser. B

(1998)

G.F Eden et al.

Abnormal processing of visual motion in dyslexia revealed by functional brain imaging

Nature

(1996)

V.P Ferrera et al.

Mixed parvocellular and magnocellular geniculate signals in visual area V4

Nature

(1992)

V.P Ferrera et al.

Responses in macaque visual area V4 following inactivation of the parvocellular and magnocellular LGN pathways

J. Neurosci.

(1994)

S.R Friedman-Hills et al.

Parietal contributions to visual feature binding: Evidence from a patient with bilateral lesions

Nature

(1995)

A.M Galaburda et al.

Evidence for aberrant auditory anatomy in developmental dyslexia

Proc. Natl. Acad. Sci. U.S.A.

(1994)

H.L Hawkins et al.

Visual attention modulates signal detectability

J. Exp. Psychol., Hum. Percept. Perform.

(1990)

J.M Henderson

Spatial precues affect target discrimination in the absence of visual noise

J. Exp. Psychol., Hum. Percept. Perform.

(1996)

T.S Horowitz et al.

Visual search has no memory

Nature

(1998)

Cited by (256)

Disentangling influences of dyslexia, development, and reading experience on effective brain connectivity in children
2023, NeuroImage
Altered brain connectivity between regions of the reading network has been associated with reading difficulties. However, it remains unclear whether connectivity differences between children with dyslexia (DYS) and those with typical reading skills (TR) are specific to reading impairments or to reading experience. In this functional MRI study, 132 children (M = 10.06 y, SD = 1.46) performed a phonological lexical decision task. We aimed to disentangle (1) disorder-specific from (2) experience-related differences in effective connectivity and to (3) characterize the development of DYS and TR. We applied dynamic causal modeling to age-matched (n_dys = 25, n_TR = 35) and reading-level-matched (n_dys = 25, n_TR = 22) groups. Developmental effects were assessed in beginning and advanced readers (TR: n_beg = 48, n_adv = 35, DYS: n_beg = 24, n_adv = 25). We show that altered feedback connectivity between the inferior parietal lobule and the visual word form area (VWFA) during print processing can be specifically attributed to reading impairments, because these alterations were found in DYS compared to both the age-matched and reading-level-matched TR. In contrast, feedforward connectivity from the VWFA to parietal and frontal regions characterized experience in TR and increased with age and reading skill. These directed connectivity findings pinpoint disorder-specific and experience-dependent alterations in the brain's reading network.
Perceptual pathways to hallucinogenesis
2022, Schizophrenia Research
Citation Excerpt :
The visual detection task deficits described above are consistent with a model of selective deficits in magnocellular over parvocellular visual processing pathways (Butler et al., 2001, 2005). Magnocellular pathways carry low-resolution visual feature information quickly and primarily drive attention capture and salience in downstream higher-level cortical areas, whereas parvocellular streams are thought to be slower and comprise more high-resolution featural information such as fine-grained stimulus configurations that enables operations including object identification in higher-level visual processing cortical areas (Norman, 2002; Steinman et al., 1997; Vidyasagar, 1999; Merigan and Maunsell, 2003). In a seminal series of studies, steady-state visual evoked potentials were measured from patients with schizophrenia in response to stimuli varying in luminance contrast, chromatic contrast, and spatial frequency (Butler and Javitt, 2005).
Recent advances in computational psychiatry have provided unique insights into the neural and cognitive underpinnings of psychotic symptoms. In particular, a host of new data has demonstrated the utility of computational frameworks for understanding how hallucinations might arise from alterations in typical perceptual processing. Of particular promise are models based in Bayesian inference that link hallucinatory perceptual experiences to latent states that may drive them. In this piece, we move beyond these findings to ask: how and why do these latent states arise, and how might we take advantage of heterogeneity in that process to develop precision approaches to the treatment of hallucinations? We leverage specific models of Bayesian inference to discuss components that might lead to the development of hallucinations. Using the unifying power of our model, we attempt to place disparate findings in the study of psychotic symptoms within a common framework. Finally, we suggest directions for future elaboration of these models in the service of a more refined psychiatric nosology based on predictable, testable, and ultimately treatable information processing derangements.
Dynamic coupling of oscillatory neural activity and its roles in visual attention
2022, Trends in Neurosciences
Oscillatory neural activity is believed to have a central role in information processing in the mammalian brain. While early studies often focussed on the function of individual frequency bands, there is emerging appreciation for the role of simultaneous activity in many distinct frequency bands and the interactions between them in high-level cognitive functions. Here, we focus on the role of cross-frequency coupling (CFC) in visual attention. First, we propose a framework that reconciles previous contrasting findings, showing how CFC could have a functional role on both intra- and interareal scales. Second, we outline how CFC between distinct frequency bands could label different submodalities of sensory information. Overall, our scheme provides a novel perspective of how interfrequency interaction contributes to efficient and dynamic processing of information across the brain.
Multisensory deficits in dyslexia may result from a locus coeruleus attentional network dysfunction
2021, Neuropsychologia
A fundamental educational requirement of beginning reading is to learn, access, and rapidly process associations between novel visuospatial symbols and their phonological representations in speech. Children with difficulties in such cross-modal integration are often divided into dyslexia subtypes, based on whether their primary problem is with the written or spoken component of decoding. The present review suggests that starting in infancy, perceptions of audiovisual speech are integrated by mutual oscillatory phase-resetting between sensory cortices, and throughout development visual and auditory experiences are coupled into unified perceptions. Entirely separate subtypes are incompatible with this view. Visual or auditory deficits will invariably affect processing to some degree in both domains. It is suggested that poor auditory/visual integration may be diagnostic for both forms of dyslexia, stemming from an encoding weakness in the early cross-sensory binding of audiovisual speech. The review presents a model of dyslexia as a dysfunction of the large-scale ventral and dorsal attention networks controlling such binding. Excessive glutamatergic neuronal excitability of the attention networks by the Locus coeruleus-norepinephrine system may interfere with multisensory integration, with deleterious effects on the acquisition of reading by degrading graphene/phoneme conversion.
Attentional limits in visual search with and without dorsal parietal dysfunction: space-based window or object-based span?
2021, Neuropsychologia
Citation Excerpt :
The tenets of the visuo-attentional (VA) theory of impaired reading performance argue that a subset of dyslexic children are unable to process as many letters as normal reading children and therefore cannot develop any reading expertise. This VA impairment has been associated with SPL dysfunction (Lobier et al, 2012a, 2012b, 2014; Peyrin et al, 2011, 2012; Reilhac et al., 2013) and is viewed in the literature as a consequence of either a reduced VA span (Lobier and Valdois, 2015; Valdois et al., 2019) or a reduced “spotlight” (Khan et al., 2016; Vidyasagar, 1999; Vidyasagar and Pammer, 2010). LP, AZK and AV designed the study, analyzed the data and wrote the manuscript.
Attentional resource and distribution are specifically impaired in simultanagnosia, and also in the visuo-attentional form of developmental dyslexia. Both clinical conditions are conceived as a limitation of simultaneous visual processing after superior parietal lobule (SPL) dysfunction (review in Valdois et al., 2019). However, a reduced space-based attentional window (i.e. a limited visual eccentricity at which the target object can be identified, Khan et al. 2016) has been demonstrated in simultanagnosia versus a reduced object-based span (i.e. a limited number of objects processed at each fixation, Bosse et al., 2007) in developmental dyslexia. In healthy individuals, the cost in reaction times per item in serial search tasks suggests that a group of objects is processed simultaneously at a time, but this group is also undefined and depends on the visual complexity of the task.
Healthy individuals and a patient with simultanagnosia performed serial search tasks involving either symbols (made of separable features) or objects made of non-separable features, and with distractors that were either all identical or all dissimilar. We used a moving window paradigm to determine whether the task was performed with a “working space” versus a “working span” limitation in control group and in patient with bilateral SPL damage.
We found that healthy individuals performed search in a color task comprising non-separable feature objects and dissimilar distractors with a limited space-based attentional window; this attentional window, as well as the mean saccade amplitude used to displace it across the visual display, were independent of set size, thus inconsistent with an object-based attentional span. In the symbol task comprising a feature-absent search in which all feature-present distractors were dissimilar, we observed that mean saccade amplitude decreased with set size and that search performance could not be mimicked by a moving window of a single diameter; instead participants seemed to process a fixed number of symbols at a time (object-based span).
Following bilateral SPL lesions, patient IG demonstrated a similar space-based search process in the color search task with a normal attentional window. In contrast, her cost-per-item in the symbol task increased dramatically, demonstrating a clear deficit of simultaneous object perception. These results confirmed the specific contribution of the SPL to the visual processing of multiple objects made of separable features (like letters), and more dramatically when they are all different, which explains the specific difficulty for a reading beginner in case of SPL dysfunction.
Visual search efficiency and functional visual cortical size in children with and without dyslexia
2021, Neuropsychologia
Dyslexia is characterised by poor reading ability. Its aetiology is probably multifactorial, with abnormal visual processing playing an important role. Among adults with normal reading ability, there is a larger representation of central visual field in the primary visual cortex (V1) in those with more efficient visuospatial attention. In this study, we tested the hypothesis that poor reading ability in school-aged children (17 children with dyslexia, 14 control children with normal reading ability) is associated with deficits in visuospatial attention using a visual search task. We corroborated the psychophysical findings with neuroimaging, by measuring the functional size of V1 in response to a central 12° visual stimulus. Consistent with other literature, visual search was impaired and less efficient in the dyslexic children, particularly with more distractor elements in the search array (p = 0.04). We also found atypical interhemispheric asymmetry in functional V1 size in the dyslexia group (p = 0.02). Reading impaired children showed poorer visual search efficiency (p = 0.01), needing more time per unit distractor (higher ms/item). Reading ability was also correlated with V1 size asymmetry (p = 0.03), such that poorer readers showed less left hemisphere bias relative to the right hemisphere. Our findings support the view that dyslexic children have abnormal visuospatial attention and interhemispheric V1 asymmetry, relative to chronological age-matched peers, and that these factors may contribute to inter-individual variation in reading performance in children.

View all citing articles on Scopus

View full text

Full-length reviewA neuronal model of attentional spotlight: parietal guiding the temporal

Abstract

Introduction

Section snippets

A model of attention that incorporates a novel view of convergence of parallel pathways in vision

Psychophysical consequences

Relation to other models

Conclusions

Acknowledgements

Vision Res.

Neuropsychologia

Vision Res.

Vision Res.

Curr. Opin. Neurobiol.

Neuropsychologia

Ophthalmic Physiol. Opt.

Trends Neurosci.

Vision Res.

Int. J. Psychophysiol.

Behav. Brain Res.

Neuropsychologia

Vision Res.

Int. J. Psychophysiol.

Trends Neurosci.

Curr. Opin. Neurobiol.

Cognit. Psychol.

Neurosci. Lett.

Multimodal integration for the representation of space in the posterior parietal cortex

Philos. Trans. R. Soc. London, Ser. B, Biol. Sci.

Multimodal representation of space in the posterior parietal cortex and its use in planning movements

Annu. Rev. Neurosci.

The effects of contrast, stimulus duration and spatial frequency on visible persistence in normal and specifically disabled readers

J. Exp. Psychol., Hum. Percept. Perform.

Physiological organization of layer 4 in macaque striate cortex

J. Neurosci.

Visual topography of area TEO in the macaque

J. Comp. Neurol.

Information processing and attention dysfunctions in schizophrenia

Schizophr. Bull.

Allocation of visual attention in good and poor readers

Percept. Psychophysiol.

Unmasking visual masking: a look at the `why' behind the veil of the `how'

Psychol. Rev.

Selective suppression of the magnocellular visual pathway during saccadic eye movements

Nature

Local circuits in primary visual cortex of the macaque monkey

Annu. Rev. Neurosci.

Schizophrenia: an information processing model

Aust. N. Z. J. Psychol.

A neural basis for visual search in inferior temporal cortex

Nature

Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area

J. Neurophysiol.

Visual interactions with luminance and chromatic stimuli

J. Opt. Soc. Am. A

Superior parietal cortex activation during spatial attention shifts and visual feature conjunction

Science

Human cortical mechanisms of visual attention during orienting and search

Philos. Trans. R. Soc. London, Ser. B

Impaired attention, genetics and the pathophysiology of schizophrenia

Schizophr. Bull.

Function of the thalamic reticular complex: the searchlight hypothesis

Proc. Natl. Acad. Sci. U.S.A.

Functional magnetic resonance imaging of early visual pathways in dyslexia

J. Neurosci.

Somatosensory, multisensory, and task-related neurons in cortical area 7b (PF) of unanaesthetized monkeys

J. Neurophysiol.

Expectancy and visual–spatial attention effects on vision

J. Exp. Psychol., Hum. Percept. Perform.

Coordination of what and where in visual attention

Perception

Converging levels of analysis in the cognitive neuroscience of visual attention

Philos. Trans. R. Soc. London, Ser. B

Abnormal processing of visual motion in dyslexia revealed by functional brain imaging

Nature

Mixed parvocellular and magnocellular geniculate signals in visual area V4

Nature

Responses in macaque visual area V4 following inactivation of the parvocellular and magnocellular LGN pathways

J. Neurosci.

Parietal contributions to visual feature binding: Evidence from a patient with bilateral lesions

Full-length review
A neuronal model of attentional spotlight: parietal guiding the temporal