Review
Spatial neglect and the neural coding of attentional priority

https://doi.org/10.1016/j.neubiorev.2013.01.026Get rights and content

Abstract

The concept of attentional priority plays an increasingly important role in theoretical interpretations of the neurophysiological mechanisms underlying attentional selection. A priority map is a feature-independent, spatiotopic representation of the environment that combines stimulus-driven information with goal-related signals. It emerges from the functional properties of parietal brain regions involved in spatial attention and saccade programming on the one hand, and reaching or grasping movements on the other hand. Here, we explore the value of this concept for the understanding of neuropsychological deficits of attention such as spatial extinction and neglect. We argue that these conditions reflect spatially graded, multisensory deficits affecting a processing level at which stimulus-driven and goal-driven signals interact. These attributes of neglect and extinction agree with the functional characteristics of attentional priority and suggest that components of both disorders can be understood as manifestations of damage or dysfunction affecting the parietal priority map.

Highlights

► We relate spatial neglect to the neural coding of attentional priority. ► Posterior parietal cortex computes priority from sensory and goal-related signals. ► A priority map is a feature-independent representation of the environment. ► Neglect affects feature-independent sensory and goal-related information. ► Some components of neglect are compatible with damage to the putative priority map.

Introduction

One of the greatest mysteries of attention is its high degree of flexibility: attention may select almost any property of the environment, such as regions in space, surfaces, whole objects or isolated object features (Gilbert and Sigman, 2007). Selection may also be guided by expectations, action goals or preferences of the observer (Egeth and Yantis, 1997, Pashler et al., 2001, Simons, 2000). Attention may be focused on a small region or take a more distributed form (Eriksen and St. James, 1986, Pashler, 1998). It can be directed inwardly, such as when we focus on thoughts or emotions, or may actively track a stimulus in the environment. The almost infinite possibilities of attention present two fundamental challenges for theories of attentional selection: first, how can one explain that a single mechanism may succeed to select the ‘right’ one (whatever that be) among multiple stimuli characterized by sensory qualities as unlike as coloured text, a flying insect or the sound of an explosion? Second, how can one account for the capacity of attention to resolve the competition between external conditions (e.g., features defining the stimulus) and internal processes (e.g., action goals of the observer), such as the preference for a particular yellow hue when searching for a car on a parking filled with hundreds of cars of various colours? These questions delimit what may be considered as the criterion problem of attention: attention needs a selection threshold that is independent of specific stimulus features or attentional states of the observer (Ptak, 2012, Wolfe and Horowitz, 2004). Solving the criterion problem is an important step toward comprehending how humans select and act upon stimuli in a complex environment.

Providing answers to the criterion problem will not only advance the understanding of a wide range of phenomena related to attentional selection in healthy observers, but also contribute to a clearer picture of deficits associated with neuropsychological disorders of attention such as spatial neglect. Patients with neglect present a number of heterogeneous symptoms that have alternately been attributed to attentional, representational, or premotor factors. Many experimental studies have focused on dissociations between distinct patients or patient groups, and it is increasingly difficult to provide a common framework that would cover the totality of these symptoms. This is why the current review focuses on one of the core deficits characterizing neglect: the severe, lateralized impairment of spatial attention, which leads to a lack of awareness for visual, auditory or tactile stimuli presented contralateral to the brain damage (Corbetta and Shulman, 2011, Driver and Mattingley, 1998, Kerkhoff, 2001, Milner and McIntosh, 2005). Spatial attention deficits of neglect patients affect all sensory modalities and are easily modulated by goal-driven processes. A better understanding of neglect and other disorders of spatial attention might therefore provide important clues toward a solution of the criterion problem.

Here, we review neurophysiological findings that are of relevance for a better understanding of the criterion problem and we relate these to the deficits of spatial orienting and attention characterizing spatial neglect. We propose that brain regions lying along the dorsal visual stream build a reciprocal network that integrates sensory inputs and behavioural goals and computes an abstract representation of the environment – a priority map. We argue that attentional priority is computed prior to the full identification of a stimulus, and therefore constitutes a suitable mechanism for fast attentional selection. Finally, we propose that lateralized deficits of attention in spatial neglect can be understood as failures to compute the attentional priority of contralesional stimuli and events.

Section snippets

Spatial attention, the dorsal-ventral distinction and reentrant processing

Any theory addressing the neural basis of visual attention must attempt to integrate two highly influential ideas regarding the organisation of visual pathways. The first is that visual information is processed along a hierarchy of segregated areas, progressing from simple to increasingly complex visual features (Colby and Duhamel, 1991, Felleman and Van Essen, 1991, Van Essen and Maunsell, 1983). In parallel, there is a progressive increase of receptive field size from low-level to high-level

Towards a definition of attentional priority

Saliency is a concept that plays a central role in computational and neurophysiological theories of attention (Fecteau and Munoz, 2006, Gottlieb et al., 1998, Itti et al., 1998, Nothdurft, 2000, Parkhurst et al., 2002). It is commonly understood as perceptual singularity that makes a stimulus ‘stand out’ in comparison to its surrounding stimuli. According to this definition saliency denotes the physical (‘bottom-up’) intensity of the signal, such as stimulus size, lightness, colour or abrupt

Priority-based attentional selection: Implications for neglect

To what extent can this priority-based model of attention contribute to the understanding of the intriguing deficits of attentional selection characterizing spatial neglect? Patients with left neglect lack awareness of stimuli presented contralaterally to their brain damage, be it objects, sounds or touches applied to their left body side, even in the absence of motor or sensory loss (Danckert and Ferber, 2006, Driver and Mattingley, 1998, Halligan and Marshall, 1993, Hillis, 2006, Kerkhoff,

Conclusions

This review highlights the role of a neural system computing a feature-independent representation of the environment from combined stimulus-driven and goal-driven inputs that can build the basis of attentional selection. It contrasts with some cognitive models of attention, which emphasize the importance of stimulus saliency as factor that is determinant for the capture of attention. Human actions cannot only be explained by the relations between external variables, but are shaped by different

Acknowledgements

This work was supported by the Swiss National Science Foundation (grant 320030-134591) and the de Reuter Foundation (grant 521).

References (239)

  • J.C. Culham et al.

    Neuroimaging of cognitive functions in human parietal cortex

    Current Opinion in Neurobiology

    (2001)
  • P. D’Erme et al.

    Early rightwards orienting of attention on simple reaction time performance in patients with left-sided neglect

    Neuropsychologia

    (1992)
  • J. Danckert et al.

    Revisiting unilateral neglect

    Neuropsychologia

    (2006)
  • B. de Haan et al.

    Mechanisms and anatomy of unilateral extinction after brain injury

    Neuropsychologia

    (2012)
  • E. De Renzi et al.

    Attentional shift towards the rightmost stimuli in patients with left visual neglect

    Cortex

    (1989)
  • H. Deubel et al.

    Saccade target selection and object recognition: Evidence for a common attentional mechanism

    Vision Research

    (1996)
  • G. di Pellegrino et al.

    Implicitly evoked actions modulate visual selection: evidence from parietal extinction

    Current Biology

    (2005)
  • F. Doricchi et al.

    White matter (dis)connections and gray matter (dys)functions in visual neglect: gaining insights into the brain networks of spatial awareness

    Cortex

    (2008)
  • J. Duncan et al.

    Competitive brain activity in visual attention

    Current Opinion in Neurobiology

    (1997)
  • R. Eramudugolla et al.

    Association between auditory and visual symptoms of unilateral spatial neglect

    Neuropsychologia

    (2007)
  • M.J. Farah et al.

    Unconscious perception of “extinguished” visual stimuli: Reassessing the evidence

    Neuropsychologia

    (1991)
  • M.J. Farah et al.

    Parietal lobe mechanisms of spatial attention: modality-specific or supramodal?

    Neuropsychologia

    (1989)
  • J.H. Fecteau et al.

    Salience, relevance, and firing: a priority map for target selection

    Trends in Cognitive Sciences

    (2006)
  • S. Geeraerts et al.

    A psychophysical study of visual extinction: ipsilesional distractor interference with contralesional orientation thresholds in visual hemineglect patients

    Neuropsychologia

    (2005)
  • C.D. Gilbert et al.

    Brain states: top-down influences in sensory processing

    Neuron

    (2007)
  • L. Golay et al.

    Dynamic modulation of visual detection by auditory cues in spatial neglect

    Neuropsychologia

    (2005)
  • R.A. Andersen

    Encoding of intention and spatial location in the posterior parietal cortex

    Cerebral Cortex

    (1995)
  • R.A. Andersen et al.

    Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque

    Journal of Neuroscience

    (1990)
  • R.A. Andersen et al.

    Intentional maps in posterior parietal cortex

    Annual Review of Neuroscience

    (2002)
  • R.A. Andersen et al.

    Encoding of spatial location by posterior parietal neurones

    Science

    (1985)
  • R.A. Andersen et al.

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

    Annual Review of Neuroscience

    (1997)
  • B. Anderson

    A mathematical model of line bisection behaviour in neglect

    Brain

    (1996)
  • B.B. Averbeck et al.

    Statistical analysis of parieto-frontal cognitive-motor networks

    Journal of Neurophysiology

    (2009)
  • M. Avillac et al.

    Multisensory integration in the ventral intraparietal area of the macaque monkey

    The Journal of Neuroscience: The Official Journal of the Society for Neuroscience

    (2007)
  • P. Bartolomeo

    A parietofrontal network for spatial awareness in the right hemisphere of the human brain

    Archives of Neurology

    (2006)
  • P. Bartolomeo et al.

    Modulating the attentional bias in unilateral neglect: the effects of the strategic set

    Experimental Brain Research

    (2001)
  • P. Bartolomeo et al.

    Brain networks of visuospatial attention and their disruption in visual neglect

    Frontiers in Human Neuroscience

    (2012)
  • P. Bartolomeo et al.

    Left unilateral neglect as a disconnection syndrome

    Cerebral Cortex

    (2007)
  • A. Battaglia-Mayer et al.

    The over-representation of contralateral space in parietal cortex: a positive image of directional motor components of neglect?

    Cerebral Cortex

    (2005)
  • L. Battelli et al.

    Bilateral deficits of transient visual attention in right parietal patients

    Brain

    (2003)
  • G.C. Baylis et al.

    Visual extinction and stimulus repetition

    Journal of Cognitive Neuroscience

    (1993)
  • P.M. Bays et al.

    Integration of goal- and stimulus-related visual signals revealed by damage to human parietal cortex

    Journal of Neuroscience

    (2010)
  • S. Ben Hamed et al.

    Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis

    Experimental Brain Research. Experimentelle Hirnforschung. Experimentation Cerebrale

    (2001)
  • N.P. Bichot et al.

    Parallel and serial neural mechanisms for visual search in macaque area V4

    Science

    (2005)
  • N.P. Bichot et al.

    Effects of similarity and history on neural mechanisms of visual selection

    Nature Neuroscience

    (1999)
  • J. Binder et al.

    Distinct syndromes of hemineglect

    Archives of Neurology

    (1992)
  • J.W. Bisley et al.

    Neuronal activity in the Lateral Intraparietal Area and spatial attention

    Science

    (2003)
  • J.W. Bisley et al.

    Attention, intention, and priority in the parietal lobe

    Annual Review of Neuroscience

    (2010)
  • J.W. Bisley et al.

    A rapid and precise on-response in posterior parietal cortex

    Journal of Neuroscience

    (2004)
  • E. Blaser et al.

    Measuring the amplification of attention

    Proceedings of the National Academy of Sciences of the United States of America

    (1999)
  • Cited by (35)

    • Task relevance and negative reward modulate the disengagement deficit of patients with spatial neglect

      2022, Neuropsychologia
      Citation Excerpt :

      Previous studies have proposed a variety of cognitive mechanisms that could explain attentional selection, such as decreased perceptual noise (Lu and Dosher, 1998), increased target saliency (Arcizet et al., 2011) or increased neural gain (i.e., narrowing of the bandwidth of neural responses to a given stimulus; Hillyard et al., 1998). In addition to these pure ‘bottom-up’ models, several authors posit that spatial attention reflects dynamic adjustments within a spatiotopic priority map, which is located within dorsal fronto-parietal areas (Bourgeois et al., 2020; Chelazzi et al., 2014; Fecteau and Munoz, 2006; Ptak, 2012; Ptak and Fellrath, 2013). Priority can be stimulus-driven or influenced by motivational factors and behavioral goals of the observer.

    • The prioritisation of motivationally salient stimuli in hemi-spatial neglect may be underpinned by goal-relevance: A meta-analytic review

      2022, Cortex
      Citation Excerpt :

      The reason that inattention occurs specifically for the contralesion side of space under perceptual load is likely due to the dysfunctional spatial mapping of priority. In neglect priority is shifted to the ipsilesional side of space, making the contralesion side of space the least ‘relevant’ region, and ipsilesion side of space most ‘relevant’ (Ptak & Fellrath, 2013). A central idea of load theory is that goal-relevant stimuli are prioritised over irrelevant stimuli when perceptual capacity is limited (Lavie, 1995; 2005).

    • Object recognition and visual agnosia

      2021, Encyclopedia of Behavioral Neuroscience: Second Edition
    View all citing articles on Scopus
    View full text