Perceptual Disorders

Abstract

Perceptual disorders are a type of neurobehavioral manifestations: cognitive disorders characterized by an impaired ability to perceive the nature of objects or concepts through use of the sense organs. This article covers spatial neglect and its competing explanations, the agnosias and the two visual systems proposal, complex visual hallucinations and the Charles Bonnet syndrome, Alice in Wonderland syndrome, phantom limb pain and the debate over cortical reorganization, congenital amusia and synesthesia, and the rehabilitation of neglect with prism adaptation.

Keywords: perceptual disorders, spatial neglect, agnosia, hallucinations, phantom limb

Unilateral spatial neglect is a common neurological syndrome following predominantly right hemisphere injuries and is characterized by both spatial and nonspatial deficits (Corbetta & Shulman, 2011). Prosopagnosia is a selective visual agnosia characterized by the inability to recognize the identity of faces, with both acquired forms secondary to brain damage and developmental forms without obvious structural lesions (Corrow et al., 2016).

What Perceptual Disorders Are

MeSH defines Perceptual Disorders as cognitive disorders characterized by an impaired ability to perceive the nature of objects or concepts through use of the sense organs, and notes that these include spatial neglect syndromes, where an individual does not attend to visual, auditory, or sensory stimuli presented from one side of the body. Its entry terms are Hemispatial Neglect, Hemisensory Neglect, Sensory Neglect and Somatosensory Discrimination Disorder. MeSH files the descriptor under neurobehavioral manifestations in three of its trees.

The disorders are defined by a failure of perception rather than of the sense organ itself. Congenital amusia, for example, refers to a musical disability that cannot be explained by prior brain lesion, hearing loss, cognitive deficits, socioaffective disturbance, or lack of environmental stimulation (Peretz et al., 2002). Tactile agnosia followed lesions of ventrolateral somatosensory association cortex and was readily detectable for years after onset, whereas extensive dorsomedial lesions involving anterior and posterior cortices acutely caused severe disruption of somesthetic processing, and sensorimotor function after dorsomedial damage improved considerably (Caselli, 1993).

Types of Perceptual Disorders

MeSH lists eight narrower descriptors beneath perceptual disorders. MeSH is an indexing classification, not a theory of perception: its subtypes record how the literature is indexed and need not be mutually exclusive, and the neglect syndromes named in the entry terms are indexed under the parent rather than as a separate descriptor.

Spatial Neglect

Neglect is common. A systematic review of 41 articles with 6324 participants found an occurrence rate of 29% without considering time post-stroke or diagnostic methods, 38% after right brain damage and 18% after left brain damage, estimated the prevalence after unilateral stroke at 30%, and found higher prevalence with ecological assessments than with tests not directly related to daily life activities (53% vs. 24%) (Esposito et al., 2021).

Neglect reaches beyond what is in front of the eyes. Two patients showing left unilateral neglect were asked to describe imagined perspectives of familiar surroundings, and left-sided details were largely omitted in the descriptions (Bisiach & Luzzatti, 1978). It also reaches into action: six patients with left-sided neglect after right hemisphere infarctions bisected lines significantly better when the line was placed to the right side of the body than to the left, and looking to the left before bisecting did not help, observations that supported the view that patients with hemispatial neglect have hemispatial hypokinesia, although a hemispatial memory defect was offered as an alternative (Heilman & Valenstein, 1979).

Where the damage lies remains contested. An influential account attributed the unilateral neglect syndrome to a dysfunction of a large-scale neurocognitive network, the cortical epicentres of which are located in posterior parietal cortex, the frontal eye fields and the cingulate gyrus, and held that severe contralesional neglect occurs almost exclusively after right hemisphere lesions (Mesulam, 1999). One study argued, contrary to the widely accepted view that neglect is typically associated with lesions of the posterior parietal lobe, that the superior temporal cortex is the neural substrate of spatial neglect in humans, as it is in monkeys (Karnath et al., 2001). A later review argued that neglect is better explained by the dysfunction of distributed cortical networks for the control of attention than by structural damage of specific brain regions: ventral lesions directly impair nonspatial functions partly mediated by a ventral frontoparietal attention network and induce abnormalities in a dorsal frontoparietal network that controls spatial attention (Corbetta & Shulman, 2011). In patients imaged at acute and chronic stages, interhemispheric connectivity in posterior parietal cortex of the structurally intact dorsal network was acutely disrupted but fully recovered, and disconnection of the white matter tracts connecting frontal and parietal cortices was associated with more severe neglect (He et al., 2007). A disconnection account goes further: damage to the long-range white matter pathways connecting parietal and frontal areas within the right hemisphere may constitute a crucial antecedent of neglect, so that neglect would not result from the dysfunction of a single cortical region but from the disruption of large networks made up of distant cortical regions (Bartolomeo et al., 2007).

Agnosia and the Two Visual Systems

The two visual systems hypothesis remains debated. It proposed that the ventral stream of projections from the striate cortex to the inferotemporal cortex plays the major role in the perceptual identification of objects, while the dorsal stream projecting to the posterior parietal region mediates the required sensorimotor transformations for visually guided actions directed at such objects (Goodale & Milner, 1992). Part of the evidence came from a patient with a profound disorder in the perception of object qualities such as shape, orientation and size, whose hand and finger movements were strikingly accurately guided toward the very objects whose qualities she failed to perceive (Goodale et al., 1991). A critical review argued that each of the model's core contrasts between the two streams has either been refuted or found limited empirical support, that the model captures some broad patterns of functional localization but the specializations of the two streams are relative rather than absolute, and that the idea that the ventral and dorsal streams are functionally independent processing pathways should be rejected (Schenk & McIntosh, 2010). A 2018 special issue of Cortex took stock of where the field stands on 'what' and 'how' (de Haan et al., 2018).

Figure 1

Two Visual Streams

Figure 1 summarises the proposal.

The concept of visual agnosia dates to the nineteenth century: an 1890 case report with a contribution to its theory was published in English translation in 1988 (Lissauer, 1988). Agnosias can be narrow. A review of prosopagnosia discusses the diagnosis of acquired and developmental forms, the evidence regarding the selectivity of the defect in relation to the recognition of other objects, written words and voices, its structural and functional basis from imaging and event-related potentials, and recent attempts at rehabilitation of face recognition (Corrow et al., 2016). The same review distinguishes an apperceptive variant of prosopagnosia, a failure in encoding the facial percept, from an associative or amnestic variant, in which facial structure is perceived accurately but the faces of familiar people cannot be recalled, while noting that this is a relative rather than absolute dichotomy that nonetheless remains useful (Corrow et al., 2016). Touch has its own agnosia: ventrolateral lesions of somatosensory association cortex caused tactile agnosia, and the functional differences between ventrolateral and dorsomedial cortices may reflect parallel processing in dual somatosensory systems (Caselli, 1993).

Hallucinations and Distortions

Visually impaired patients may experience complex visual hallucinations, a condition known as the Charles Bonnet syndrome; patients usually possess insight into the unreality of their visual experiences, and the hallucinations are believed to represent release phenomena due to de-afferentation of the visual association areas of the cerebral cortex (Menon et al., 2003).

The Perception and Attention Deficit model has since been revised. It proposed that a combination of impaired attentional binding and poor sensory activation of a correct proto-object, in conjunction with a relatively intact scene representation, biases perception to allow the intrusion of a hallucinatory proto-object into a scene perception (Collerton et al., 2005). Eight models of complex visual hallucinations have been published since 2000, including the Perception and Attention Deficit model, and representatives from each research group agreed an integrated Visual Hallucination Framework that is consistent with current theories of veridical and hallucinatory vision (Collerton et al., 2023).

Alice in Wonderland syndrome is a disorder characterized by distortions of visual perception, the body schema and the experience of time; on the basis of 169 published case descriptions its etiology was divided into 8 main groups, and up to 30% of adolescents report nonclinical symptoms (Blom, 2016). The same review treats these symptoms as distortions of sensory perception rather than hallucinations or illusions, and notes that illusions do have a source in the outside world, albeit one that is often fleetingly misperceived or misinterpreted (Blom, 2016).

Phantom Limb

Phantom pain refers to pain in a body part that has been amputated or deafferented, and evidence has accumulated that it might be a phenomenon of the central nervous system related to plastic changes at several levels of the neuraxis and especially the cortex (Flor et al., 2006). The founding evidence was a very strong direct relationship (r = 0.93) between the amount of cortical reorganization and the magnitude of phantom limb pain, but not non-painful phantom phenomena, after arm amputation (Flor et al., 1995).

The maladaptive plasticity model is contested. Phantom pain after arm amputation is widely believed to arise from maladaptive cortical reorganization, but one study found that the experience of persistent pain is associated with preserved structure and functional organization in the former hand area, and its authors proposed that, contrary to the maladaptive model, cortical plasticity associated with phantom pain is driven by powerful and long-lasting subjective sensory experience (Makin et al., 2013).

Vision can change what the phantom feels. With a mirror placed so that the reflection of the intact hand is superimposed on the felt position of the phantom, six of ten patients felt the phantom move when the normal hand moved, and in four of five patients with painful clenching spasms the spasms were relieved when the mirror was used to facilitate opening of the phantom hand (Ramachandran & Rogers-Ramachandran, 1996).

Auditory Disorders and Synesthesia

What Peretz and colleagues reported as the first documented case of congenital amusia was a middle-aged woman who lacked most basic musical abilities, including melodic discrimination and recognition, despite normal audiometry and above-average intellectual, memory and language skills; psychophysical tests showed severe difficulties with detecting pitch changes (Peretz et al., 2002).

Synesthesia sits at the edge of the category. A review considers its elicited nature, automaticity, prevalence, consistency and perceptual and spatial phenomenology, and its causes in genetic differences in developmental synesthesia and plasticity following sensory loss in acquired synesthesia (Ward, 2013).

Rehabilitation

Prism adaptation is one treatment for neglect. Patients exposed to an optical shift of the visual field to the right improved on their manual body-midline demonstration and on classical neuropsychological tests, and the improvement lasted for at least two hours after prism removal (Rossetti et al., 1998). Whether the gains reach daily life is less certain: a systematic review of 25 intervention and 1 follow-up studies found 32 measurements with significant effects and 15 with non-significant effects, and concluded that there is some evidence suggesting that prism adaptation can improve daily functioning, particularly as measured by reading and writing and direct tests of activities of daily living (Champod et al., 2018).

For the Charles Bonnet syndrome, reassurance and explanation that the visions are benign and do not signify mental illness have a powerful therapeutic effect, and there is no universally effective drug treatment (Menon et al., 2003). In Alice in Wonderland syndrome, treatment should be directed at the suspected underlying condition, although reassurance seems to suffice in about 50% of the cases (Blom, 2016).

Worked Example

The neglect prevalence figures can be turned into counts. Taking the occurrence rates of 38% after right brain damage and 18% after left brain damage (Esposito et al., 2021), an illustrative stroke unit admitting 500 patients with right brain damage and 500 with left brain damage would see about 190 cases of neglect after right brain damage (500 × 0.38 = 190) and 90 after left brain damage (500 × 0.18 = 90), or 280 of 1,000 (28%). The same figures imply that roughly one in three neglect cases in such a unit would follow left brain damage (90 of 280).

Discussion

Three conclusions follow. First, the anatomy of neglect remains contested: one study places its substrate in the superior temporal cortex (Karnath et al., 2001), and a later review explains it by the dysfunction of distributed attention networks rather than damage to a specific region (Corbetta & Shulman, 2011).

Second, the leading accounts have since been revised or challenged. A critical review argued that the ventral and dorsal streams should not be considered functionally independent processing pathways (Schenk & McIntosh, 2010), and a 2018 special issue of Cortex took stock of 'what' and 'how' (de Haan et al., 2018); the Perception and Attention Deficit model has been folded into an integrated framework (Collerton et al., 2023), and the maladaptive account of phantom pain faces a preserved-representation alternative (Makin et al., 2013).

Third, insight and reassurance matter clinically: people with the Charles Bonnet syndrome usually know their hallucinations are unreal (Menon et al., 2003), and reassurance alone seems to suffice in about half of Alice in Wonderland cases (Blom, 2016).

Current Directions

Three lines of work are active. Hallucinations: an integrated framework allows a systematic investigation of relationships between the phenomenology of visual hallucinations and changes in underpinning cognitive structures, and highlights separate factors associated with the onset, persistence and end of specific hallucinations (Collerton et al., 2023). Neglect assessment: ecological assessments and multi-test methods are preferred to a single-cutoff criterion, and more research is needed to understand chronic neglect (Esposito et al., 2021). Rehabilitation: the impact of sample heterogeneity and time since injury on prism adaptation effects should be investigated further (Champod et al., 2018).

Common Misconceptions

“Neglect is just a problem with the eyes.”

Two patients with left unilateral neglect also largely omitted left-sided details when they described imagined perspectives of familiar surroundings (Bisiach & Luzzatti, 1978).

“Seeing things that are not there means mental illness.”

Visually impaired patients may experience complex visual hallucinations and usually possess insight into their unreality (Menon et al., 2003).

“Neglect only follows right-hemisphere stroke.”

Neglect is more common after right brain damage, but neglect after left brain damage is still quite common (Esposito et al., 2021).

Glossary

Agnosia.

A failure of recognition through one sense, such as prosopagnosia for faces or tactile agnosia for objects explored by touch.

Alice in Wonderland syndrome.

A disorder characterized by distortions of visual perception, the body schema and the experience of time.

Charles Bonnet syndrome.

Complex visual hallucinations in visually impaired people, who usually possess insight into their unreality.

Congenital amusia.

A musical disability that cannot be explained by prior brain lesion, hearing loss, cognitive deficits, socioaffective disturbance or lack of environmental stimulation.

Dorsal stream.

Projections from the striate cortex to the posterior parietal region, proposed to mediate sensorimotor transformations for visually guided action.

Hemispatial hypokinesia.

A proposed difficulty in acting within the half of body space opposite a brain lesion, offered to explain line-bisection errors in neglect.

Mirror box.

A vertical mirror that superimposes the reflection of the intact hand on the felt position of a phantom limb.

Phantom pain.

Pain in a body part that has been amputated or deafferented.

Prism adaptation.

Adaptation to prisms that shift the visual field, used to treat neglect with a rightward optical deviation.

Prosopagnosia.

A selective visual agnosia characterized by the inability to recognize the identity of faces, acquired or developmental.

Representational neglect.

Omission of left-sided details when describing imagined perspectives of familiar surroundings.

Spatial neglect.

A failure to attend to stimuli presented from one side of the body, most often after right hemisphere injury.

Synesthesia.

An elicited, automatic and consistent experience, developmental or acquired after sensory loss.

Tactile agnosia.

Impaired tactile object recognition, which followed ventrolateral somatosensory association cortex lesions and persisted for years.

Ventral stream.

Projections from the striate cortex to the inferotemporal cortex, proposed to play the major role in perceptual identification of objects.

Key Researchers

Jan Dirk Blom

Psychiatrist at Leiden University and the Parnassia Psychiatric Institute, The Hague; reviewed the published cases of Alice in Wonderland syndrome. ORCID - Google Scholar - Faculty Page

Maurizio Corbetta

Neurologist at the University of Padua, formerly Washington University in St. Louis; linked with colleagues the behavioral deficits of spatial neglect to a breakdown of functional connectivity in frontoparietal networks, and explains neglect as a dysfunction of distributed attention networks. ORCID - Wikidata - Google Scholar - Faculty Page

Herta Flor

(b. 1954). Neuropsychologist at the Central Institute of Mental Health, Heidelberg University, Mannheim; reported with colleagues a very strong relationship between cortical reorganization and phantom limb pain after arm amputation. Wikipedia - Wikidata - Google Scholar

Melvyn A. Goodale

(b. 1943). Neuroscientist at the University of Western Ontario; reported with colleagues a patient who grasped accurately objects whose shape, orientation and size she could not perceive, and proposed with Milner separate visual pathways for perception and action. ORCID - Wikipedia - Wikidata - Google Scholar - Faculty Page

Kenneth M. Heilman

(1938–2024). Behavioral neurologist at the University of Florida; studied the mechanisms of hemispatial neglect. Wikipedia - Wikidata - Google Scholar - Faculty Page

Tamar R. Makin

Neuroscientist at the MRC Cognition and Brain Sciences Unit, University of Cambridge; found phantom pain associated with preserved structure and function in the former hand area. Wikipedia - Google Scholar - Faculty Page

Isabelle Peretz

Neuropsychologist at the University of Montreal; documented congenital amusia as a disorder of fine-grained pitch discrimination. ORCID - Wikipedia - Wikidata - Google Scholar - Faculty Page

Frequently Asked Questions

What are perceptual disorders?

MeSH defines them as cognitive disorders characterized by an impaired ability to perceive the nature of objects or concepts through use of the sense organs, including spatial neglect syndromes; congenital amusia, for example, cannot be explained by hearing loss (Peretz et al., 2002).

How common is neglect after stroke?

The estimated prevalence of spatial neglect after unilateral stroke is 30%, and it is more common after right than after left brain damage (Esposito et al., 2021).

Does neglect affect imagination too?

Yes: two patients with left unilateral neglect largely omitted left-sided details when describing imagined perspectives of familiar surroundings (Bisiach & Luzzatti, 1978).

What part of the brain is damaged in neglect?

One study places the substrate in the superior temporal cortex (Karnath et al., 2001), while a review explains neglect by the dysfunction of distributed attention networks rather than damage to a specific region (Corbetta & Shulman, 2011).

What is prosopagnosia?

A selective visual agnosia characterized by the inability to recognize the identity of faces, with acquired and developmental forms (Corrow et al., 2016).

Why do some people with poor eyesight see things that are not there?

In the Charles Bonnet syndrome the hallucinations are believed to represent release phenomena due to de-afferentation of the visual association areas of the cortex (Menon et al., 2003).

What causes phantom limb pain?

It has been linked to plastic changes in the central nervous system, especially the cortex (Flor et al., 2006), but one study found it associated with preserved structure and function in the former hand area rather than maladaptive reorganization (Makin et al., 2013).

Does prism adaptation help neglect in daily life?

There is some evidence suggesting that prism adaptation can improve daily functioning, particularly reading and writing and direct tests of activities of daily living (Champod et al., 2018).

References