Perceptual awareness and its loss in unilateral neglect and extinction
Introduction
Unilateral spatial neglect is a relatively common and disabling neurological disorder after unilateral brain damage. It is characterized by a lack of awareness for sensory events located towards the contralesional side of space (e.g. towards the left following a right lesion), together with a loss of the orienting behaviours, exploratory search and other actions that would normally be directed toward that side. Neglect patients often behave as if half of their world no longer exists. In daily life, they may be oblivious to objects and people on the neglected side of the room, may eat from only one side of their plate, read from only one end of a newspaper page, and make-up or shave only one side of their face. The spatial bias towards one side can also be apparent in many simple paper-and-pencil tests. When required to search for and mark all target shapes on a page, the patients may cancel only those towards the ipsilesional side. When bisecting a horizontal line, they may err towards that side, and when drawing from memory, or copying a picture, they may omit details from the contralesional side (Fig. 1).
The characteristic spatial bias of neglect patients has been observed in some form for all of the sensory modalities (vision, audition, touch, proprioception, even smell; see Bellas et al., 1988, Heilman et al., 1993, Mesulam, 1981, Vallar et al., 1995). Analogous spatial biases may also be apparent in motor-output systems, as we discuss later (e.g. with eye or hand movements being biased towards the ‘good’ ipsilesional side; see Bisiach et al., 1990, Coslett et al., 1990, Heilman et al., 1985). Some patients may neglect their own contralesional limbs, attempting to climb out of bed without moving these, even though they have no primary motor weakness on that side. Others may be paralyzed on the contralesional side, yet remain unaware of this. In general, neglect patients often have little insight into their deficits for the affected side, especially in the acute stage. In the longer term, they may acknowledge that they can ‘miss things’ on the affected side, yet continue to do so.
Thus, neglect ostensibly involves a dramatic loss of awareness, and of appropriate action, for sensory events towards the affected side. The paradox is that this can arise even though the primary sensory pathways for processing the neglected information may all still be intact. That is, patients may show profound neglect for sights, sounds and touches towards the affected side, even though they are by no means blind, deaf or insensitive on this side. Here we will argue, in keeping with recent advances in neglect research, that this paradox can be resolved to some extent by relating the plight of neglect patients to particular aspects of normal cognition. Even neurologically healthy people can fail to see, hear or feel salient stimuli, provided that their selective attention is engaged elsewhere, as we shall describe (see also Merikle, Smilek, & Eastwood in this volume). Perceptual awareness is not determined solely by the stimuli impinging on our senses, but also by which of these stimuli we choose to attend. This choice seems pathologically restricted in neglect patients, with their attention strongly biased towards events on the ipsilesional side.
Section snippets
Basic anatomy of neglect, and multiple components to the clinical syndrome
Unilateral spatial neglect can be observed in some form after various unilateral brain lesions, but is most common and long-lasting in humans when the damage involves the inferior parietal lobe, particularly in the right hemisphere. Studies seeking to determine the critical cortical areas, by looking for overlap in the lesions of different cases, have pointed to the angular and supramarginal gyri (Fig. 2A), corresponding to Brodmann areas 39 and 40 (Heilman et al., 1993, Leibovitch et al., 1998
Neglect as a window on the neural basis of awareness, and the contrast with blindsight
Clinical descriptions of neglect were documented by German neurologists a century ago (e.g. Loeb, 1885, Oppenheim, 1885, Poppelreuter, 1917, Zingerle, 1913). However, the syndrome subsequently received less systematic attention than other classical neurological syndromes (such as aphasia or agnosia), perhaps because of the paucity of suitable theoretical ideas or analogies for grappling with it. Moreover, despite the dramatic loss of awareness for one side, neglect was rarely considered in
The spatial nature of neglect, and further contrasts with primary sensory loss
The loss of awareness in neglect differs from that in blindsight in its spatial nature also. The visual field cut of an occipital patient is absolutely tied to a region on the retina, in accordance with the damage to the retinotopic map in primary visual cortex. Usually there is a fairly sharp demarcation between the affected region and the intact region, often corresponding to one sensory hemifield versus the other in patients with unilateral damage.
This is very different from the spatial
Attentional perspectives on neglect
By now we hope to have convinced the reader that there is more to neglect than primary sensory loss. Neglect patients can be unaware of sights, sounds, touches and body parts towards their left in daily life, even though they are not blind, deaf or insensitive on that side. As we foreshadowed earlier, this seeming paradox may be resolved by considering that, in some circumstances, this applies to neurologically healthy individuals also, when their attention is engaged elsewhere. We can fail to
Extinction as a difficulty in attending to multiple targets
The analogy with normal attention seems particularly apt for one aspect of the neglect syndrome that we mentioned earlier, namely extinction during double simultaneous stimulation. Recall that many neglect patients can detect a single left-sided event in isolation, missing this only when presented in combination with another event further to its right. Such extinction can actually be found within hemifields as well as between them, but for simplicity we will stick to the example of two events
Preserved ‘preattentive’ processing in extinction: grouping effects
Recent patient studies show that considerable processing can still take place prior to the level at which extinction arises. As a first approximation, such processing typically corresponds well with that considered to take place ‘preattentively’ in the normal system (see Merikle et al. in this volume). As in normals, this processing can determine which information will attract attention and reach awareness in the patients, and which will escape awareness.
In normal vision, the limitation in
Task effects on extinction
In standard visual extinction studies, the patient is asked to report whether anything is seen on the left, the right, on both sides, or not at all. A seemingly minor change to this task can have a dramatic effect on what the patient reports seeing. Vuilleumier and Rafal (1999) presented stimuli in one, two, or four possible locations across hemifields (Fig. 5). When asked to report where the shapes appeared (i.e. on the left, right or both sides), as usually required, three right-parietal
The fate of extinguished stimuli
The previous section focused on factors determining whether a stimulus will be extinguished from awareness in the patients. The results implied some preserved processing for contralesional events, with this (preattentive) processing determining which perceptual units will go on to act as competitors (for attention), and thus which will reach awareness. We turn now to consider the fate of those contralesional stimuli which are extinguished, losing the competition and thus escaping awareness.
Anatomy of conscious and unconscious perception in relation to neglect and extinction
The accumulating evidence for considerable unconscious processing in neglect patients has now reached the point where it raises specific questions about the underlying anatomical substrates. Here again our discussion will concentrate mostly on vision, as this is best understood, though similar principles may apply to other modalities. The visual system of primates includes many distinct cortical areas, organized hierarchically in both parallel and serial pathways (Felleman & Van Essen, 1991).
The neural fate of extinguished stimuli: neurophysiological measures
In the previous sections, we speculatively related the modulation of extinction by factors such as grouping or emotional salience, and the preserved unconscious processing for extinguished stimuli, to activation of known neural pathways. More direct evidence for such activation would be provided by measuring neural activity directly in the patients, with functional imaging or event-related potentials. Such methods have been widely used to study normal attention (e.g. Corbetta et al., 1990,
Cellular properties of the parietal lobe in relation to neglect and extinction
Single-cell recording in awake behaving monkeys has provided dramatic insights into the computational properties of neurons in the parietal lobe and related structures (e.g. see Andersen, Snyder, Bradley, & Xing, 1997, for review). Much of this evidence comes from recordings in posterior parietal cortex, in and around the intraparietal sulcus, though explorations continue into further parietal areas, and similar cellular properties have even been reported in a few of the other brain areas
Do parietal spatial circuits play a special role in perceptual awareness?
Early studies of blindsight (Weiskrantz, 1986) led to suggestions that visual awareness may depend on early visual areas of cortex. More recently, Crick and Koch (1995) sceptically asked ‘Are we aware of neural activity in primary visual cortex?’, to which we can now reply ‘Not in the absence of coupled parietal activity’ (see Rees et al., 2000, Vuilleumier et al., 2000). The evidence from neglect and extinction indicates that considerable sensory processing in the occipito-temporal visual
Moving beyond intuitions to the neural basis of awareness
There is currently much excitement about the possibility of relating awareness to neural substrates, and studies of neglect and extinction have much to offer this growing field. However, any pronouncements of ‘consciousness explained’ remain premature. Part of the problem is that neuroscientists wrestling with intriguing neurological or neurophysiological data often have, at best, only intuitive notions of what awareness constitutes in psychological or philosophical terms (see Block in this
Acknowledgements
Thanks to Alan Allport, Stanislas Dehaene, Masud Husain, Nancy Kanwisher, Jason Mattingley, Alex Pouget, Bob Rafal, Geraint Rees, Tim Shallice, Tony Jack, Noam Sagiv, Russ Poldrack, Eliot Hazeltine, Diane Swick, and Sophie Schwartz. The authors' research is supported by grants from the Medical Research Council (UK), Wellcome Trust, Human Frontiers Science Organization, and Swiss National Science Foundation.
References (250)
- et al.
Visual neglect and left-sided context effects
Brain & Cognition
(1991) Some essential differences between consciousness and attention, perception, and working memory
Consciousness & Cognition
(1997)- et al.
The nature of unilateral neglect in the olfactory system
Neuropsychologia
(1988) - et al.
Level of processing for stimuli in an “extinguished” visual field
Neuropsychologia
(1992) - et al.
Nonconscious reading? Evidence from neglect dyslexia
Cortex
(1994) - et al.
Somatosensory extinction for meaningful objects in a patient with right hemispheric stroke
Neuropsychologia
(1999) - et al.
Unilateral neglect of representational space
Cortex
(1978) - et al.
Hyperamnesia in unilateral neglect
Cortex
(1999) - et al.
Response and habituation of the human amygdala during visual processing of facial expression
Neuron
(1996) - et al.
Responses of neurons in the macaque amygdala to complex social stimuli
Neurosciences
(1990)
Left visuospatial neglect can be worse in far than in near space
Neuropsychologia
The neurobiology of blindsight
Trends in Neuroscience
Functional MRI studies of spatial and nonspatial working memory
Cognitive Brain Research
Parietal hemineglect and motor deficits in the monkey
Neuropsychologia
An experimental investigation on the nature of extinction
Neuropsychologia
Imaging visual recognition: PET and fMRI studies of the functional anatomy of human visual recognition
Trends in Cognitive Sciences
Unconscious perception of “extinguished” visual stimuli: reassessing the evidence
Neuropsychologia
Brain activity related to the perception of illusory contours
NeuroImage
Figural modulation of visuo-spatial neglect: a case study
Neuropsychologia
Homing in on neglect: a case study of visual search
Cortex
Tactile salience influences extinction
Neurology
Frames of reference for mapping tactile stimuli in brain-damaged patients
Journal of Cognitive Neuroscience
What concept of consciousness?
Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule
Journal of Comparative Neurology
Encoding of spatial location by posterior parietal neurons
Science
Multimodal representation of space in the posterior parietal cortex and its use in planning movement
Annual Reviews in Neuroscience
A mathematical model of line bisection behaviour in neglect
Brain
Unilateral spatial agnosia (“inattention”) in patients with cerebral lesions
Brain
Visual attention and objects: evidence for hierarchical coding of location
Journal of Experimental Psychology: Human Perception and Performance
Visual extinction and stimulus repetition
Journal of Cognitive Neuroscience
Phenomena of fluctuation, extinction, and completion in visual perception
Archives of Neurology and Psychiatry
Electrophysiological studies of face perception in humans
Journal of Cognitive Neuroscience
Visual processing without awareness: evidence from unilateral neglect
Journal of Cognitive Neuroscience
Functional MRI of the primary somatosensory cortex in extinction to simultaneous bilateral tactile stimuli (abstract)
Neurology
The spatial features of unilateral neglect
Dyschiria: an attempt at its systematic explanation
Perceptual and premotor factors of unilateral neglect
Neurology
Unilateral neglect, representational schema and consciousness
Brain
Subcortical neglect: neuropsychological, SPECT, and neuropathological correlations with anterior choroidal artery territory infarction
Annals of Neurology
Visual disorientation with special reference to lesions of the right hemisphere
Brain
Perception and communication
Object-based attention in visual neglect: conceptual and empirical distinctions
The physiological basis of attentional modulation in extrastriate visual areas
Nature Neuroscience
Responses of neurons in inferior temporal cortex during memory-guided visual search
Journal of Neurophysiology
Some experiments on the recognition of speech, with one and two ears
Journal of the Acoustic Society of America
Response code activation by stimuli in the neglected visual field
Neuropsychology
The parietal reach region (PRR) encodes reaches to auditory targets in an eye-centered reference frame
Society for Neuroscience Abstracts
Selective attention modulates neural processing of shape, color and velocity in humans
Science
Neglect in vision and visual imagery: a double dissociation
Brain
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2021, NeuropsychologiaCitation Excerpt :For example, patients with right hemisphere stroke show a deficit in keeping track of multiple spatial locations, thus demonstrating impaired spatial VWM (Wojciulik et al., 2001; Malhotra et al., 2005; Pisella et al., 2004). Of particular interest is the phenomenon of representational neglect (RN) - a lack of awareness of the left side of mental images derived from long-term memory or evoked by external stimulation and held in VWM (Bartolomeo and Chokron (2002a), Albert, 1973; Bisiach and Luzzatti, 1978, Bartolomeo, 2002; Bartolomeo et al., 1994; Della Sala et al., 2004; Rode et al., 2004; for reviews see Bartolomeo and Chokron (2002a); Corbetta and Shulman, 2011; Driver and Vuilleumier, 2001; Salvato et al., 2014). Although RN and PN most often occur together (Bartolomeo, 2002; Bartolomeo et al., 2005; Bourlon et al., 2008), many cases of “pure” RN have been reported (Beschin et al, 1997, 2000; Guariglia et al., 1993; Ortigue et al., 2001; Piccardi et al., 2008) indicating that these two cognitive deficits can be independent of one another.