Neuropsychologia 50 (2012) 1072–1079

Contents lists available at SciVerse ScienceDirect

Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia

Review

Rehabilitation of neglect: An update

Georg Kerkhoff a,∗ , Thomas Schenk b
a
Saarland University, Clinical Neuropsychology Unit and University Ambulance, Saarbruecken, Germany
b
Erlangen University, Dept. of Neurology, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Spatial neglect is a characteristic sign of damage to the right hemisphere and is typically characterized
Received 6 September 2011 by a failure to respond to stimuli on the left side. With about a third of stroke victims showing initial
Received in revised form 11 January 2012 signs of neglect, it is a frequent but also one of the most disabling neurological syndromes. Despite
Accepted 12 January 2012
partial recovery in the first months after stroke one third of these patients remain severely disabled in
Available online 28 January 2012
all daily activities, have a poor rehabilitation outcome and therefore require specific treatment. The last
decades have seen an intensive search for novel, more effective treatments for this debilitating disorder.
Keywords:
An impressive range of techniques to treat neglect has been developed in recent years. Here, we describe
Brain damage
Extinction
those techniques, review their efficacy and identify gaps in the current research on neglect therapy.
Treatment © 2012 Elsevier Ltd. All rights reserved.
Optokinetic stimulation
Vestibular
Brain stimulation
Motor
Dysphagia
Review

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1072
2. Early exploration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1073
3. Seeing straight . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1073
3.1. Optokinetic stimulation (OKS) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1073
3.2. Neck-muscle vibration (NMV) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1074
3.3. Caloric- and galvanic-vestibular stimulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1074
3.4. Prism adaptation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1075
4. Classics and newcomers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1075
5. Mix and match . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1075
6. Scotomas in neglect research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1077
6.1. Nonvisual neglect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1077
6.2. Sensory extinction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1077
6.3. Transfer and treatment intensity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1077
6.4. Funding for rehabilitation research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1078
7. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1078
Acknowledgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1078
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1078

Abbreviations: OKS, optokinetic stimulation; CVS, caloric vestibular stimulation; 1. Introduction

FES, functional electrical stimulation; GVS, galvanic vestibular stimulation; NMV,
neck muscle vibration; PA, visuo-motor prism adaptation; TMS, transcranial mag- Neglect is a challenging and complex disorder. Typically, it is
netic stimulation; TDCS, transcranial direct current stimulation; VR, virtual reality;
defined as the impaired or lost ability to respond to sensory stimuli
VST, visual scanning therapy.
∗ Corresponding author at: Saarland University, Clinical Neuropsychology Unit & (visual, auditory, tactile, olfactory) presented in the contralesional
University Ambulance, Building A.1.3., D-66123 Saarbruecken, Germany. hemispace of a neurological patient (Kerkhoff, 2001). In addition
E-mail address: [email protected] (G. Kerkhoff). to sensory neglect, motor neglect may occur and manifest itself as

0028-3932/$ – see front matter © 2012 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuropsychologia.2012.01.024
 G. Kerkhoff, T. Schenk / Neuropsychologia 50 (2012) 1072–1079 1073

the reduced use or nonuse of the contralesional extremities during scanning and related visual tasks like reading and line bisection
walking or bimanual activities. performance, but fails to improve non-visual neglect. For example,
But neglect is not just challenging to define and understand it in the study by Schindler, Kerkhoff, Karnath, Keller, and Goldenberg
also poses a challenge to our health system. The clinical, sociode- (2002) visual scanning training led to measurable improvements in
mographic as well as epidemiological relevance of spatial neglect as reading and visual search, but not in tactile search. In contrast neck-
a disease is substantial: every year about 3–5 million patients suffer muscle vibration in combination with visual scanning training led
from neglect after stroke (Corbetta, Kincade, Lewis, Snyder, & Sapir, to significantly greater improvements in reading and visual search,
2005), and this incidence will continuously increase due to a rising but also in tactile search. Likewise, Kerkhoff et al. (2012, this issue)
incidence of cerebro-vascular diseases in our aging western soci- found improvements in visual and auditory neglect after optoki-
eties and a shift to western life habits in the newly industrialized netic training with pusuit eye movements in 3 neglect patients, but
countries. Spontaneous recovery occurs but will not necessarily only unimodal (visual) improvements after visual scanning training
eliminate all signs of neglect. More importantly about a third of in 3 other neglect patients, without any effect on auditory neglect.
all patients manifest a chronic form of neglect and show clear VST is also quite time-consuming and thus quite costly. A mini-
signs of neglect even more than a year after their neurological mum of 40 treatment sessions (each about 50 min long) are needed
incident (Karnath, Rennig, Johannsen, & Rorden, 2011; Rengachary, to achieve stable results (Antonucci et al., 1995; Kerkhoff, 1998a).
He, Shulman, & Corbetta, 2011). Neglect interferes with rehabilita- This requires a substantial commitment from the therapist and the
tion attempts aimed at improving other symptoms of the patients patient. Commitment from the patient is often difficult to obtain
(such as hemiparesis) and if left untreated will therefore lead to a given the well-known association between anosognosia (lack of
poor rehabilitation outcome. It seems clear that the development insight) and unilateral neglect (Vallar, Bottini, & Sterzi, 2003). Given
of effective treatments for neglect should be a high priority. For the these shortcomings of VST it is therefore hardly surprising that
purpose of this special issue on unilateral neglect, we provide an many researchers in the field were looking for alternatives. These
overview over existing treatment options but also identify some came in the form of several sensory stimulation techniques. Those
of the gaps in current research on neglect-therapy. It is sobering stimulation techniques have two things in common, they require
to observe that while significant progress has been made, many less compliance and cooperation from the patient and they all aim
of the gaps that were identified in previous reviews can still be to restore the patient’s eye-, head- and body-orientation to the
found today. For this reason we will ask at the end of our review veridical straight-ahead direction.
whether there are structural reasons that can explain the persis-
tence with which important questions remain not only unanswered
3. Seeing straight
but effectively unexamined.
Karnath (2006) argued that the core-deficit in unilateral neglect
is an orientation bias to the right. Even at rest right brain-damaged
2. Early exploration
patients with neglect will show a 30◦ deviation of eye and head ori-
entation to the right (Fruhmann-Berger & Karnath, 2005). On the
The first attempts to treat patients with unilateral neglect
basis of these and similar findings Karnath and Dieterich (2006)
focused on the obvious problem that these patients seemed to
suggested that neglect results from damage to the multisensory
explore only half of their visual world. The therapeutic answer
cortex (localized in the right superior temporal cortex, insula and
to this problem was provided by Diller and Weinberg (1977) who
temporo-parietal junction) in which vestibular, auditory, neck-
used visual displays that contained multiple items and asked their
proprioceptive and visual input is combined to create higher order
patients to find specific items on these displays. It was hoped that
spatial representations of our body’s position in relation to our
through practice and guiding feedback from the therapist patients
environment. Given the multisensory nature of this representation
would learn to guide their eyes to the hitherto neglected con-
Karnath (2006) suggested that it should be possible to use sensory
tralesional space. This approach was borrowed from Poppelreuter
signals from different modalities to counteract the rightward bias
(1917) who had used a similar approach in his treatment of patients
in neglect patients. Research in the past identified a number of pos-
with visual field defects. Visual scanning or visual exploration ther-
sible cues which the brain can use to compute the body’s position
apy (VST or VET) as it came to be known rapidly established itself
in space (e.g. vestibular, visual or proprioceptive signals) and iden-
as the treatment of choice. Today many different versions are avail-
tified numerous ways to induce a bias in that system. The four best
able. These versions differ mainly in three respects: size of the
researched techniques are caloric, galvanic or optokinetic stimu-
display and method of presentation and instructions. The display
lation and neck vibration. There is a fifth technique which uses a
can either be as small as a magazine or as big as the screen in
more indirect way to affect our sense of where we are in relation
a home-cinema. The stimuli might be presented on a piece of
to the world around us and it is called prismatic adaptation. All
paper, presented on a computer screen or projected with a beamer.
five techniques can be used to induce a leftward orientation bias
Patients might be instructed to describe all items on a display or
and might therefore be used to neutralize the pathological right-
only search for a specific object embedded among other distractor
ward bias found in neglect patients. Most studies who examined
items. While for many years it has become the de-facto standard for
the influence of those manipulations on neglect demonstrated at
neglect therapy only a few studies examined its efficacy. Kerkhoff,
least transient improvement of neglect symptoms and thus pro-
Mün␤inger, Haaf, Eberle-Strauss, and Stögerer (1992) compared
vided general support for the idea that a rightward orientation bias
the impact of VST on patients with visual field deficits and those
lies at the heart of the neglect syndrome. But do these interventions
with neglect and found that patients with visual field deficits
provide viable treatment options? This question will be addressed
benefit significantly more from this treatment than patients with
in the following subsections.
neglect. A similar finding was reported by Antonucci, Guariglia,
Judica, Magnotti, Paolucci, and Pizzamiglio (1995). The same group
could however show that VST is better than an unspecific cognitive 3.1. Optokinetic stimulation (OKS)
training (Antonucci et al., 1995).
However a major weakness of the VST therapy is its specificity, The technique of optokinetic stimulation (OKS) exploits the
i.e. some but not all neglect-associated symptoms seem to improve fact that for the perception of our body in space we also use
with VST (Kerkhoff, 1998a). Typically, VST training improves visual visual information, in particular visual motion information. If we
1074 G. Kerkhoff, T. Schenk / Neuropsychologia 50 (2012) 1072–1079

look at a large visual display that fills our field of vision and rotated toward the right but also that the trunk is rotated toward
moves to the left, we have the impression that our body rotates the left. The type of (verbally reported) illusion depends on the
toward the right. We accordingly try to compensate for this per- experimental setup. The setup determines whether subjects have
ceived rotation to the right by re-orienting ourselves to the left. the impression (and verbally report) that the head is moving rela-
This phenomenon could be exploited to counteract the rightward- tive to the fixed trunk or the trunk is moving relative to the fixed
orientation-bias in neglect. Pizzamiglio, Frasca, Guariglia, Incoccia, head. Both types of mechanisms induced by NMW neutralize the
and Antonucci (1990) tested this idea and found a significant rightward orientation bias and thereby reduce neglect symptoms.
reduction of neglect symptoms. However, these benefits were of The validity of this prediction has been demonstrated in a series
a transient nature. (Kerkhoff, 2002) and colleagues later tested of studies by Karnath and his colleagues (Karnath, Christ, & Hartje,
with much smaller moving visual displays presented on conven- 1993; Karnath, Fetter, & Dichgans, 1996; Karnath, 1995). Unsur-
tional PC-monitors (17 ) potential therapeutic effects in patients prisingly these effects are transient with some after-effect and one
with neglect. Such smaller devices leave the periphery of the visual might therefore ask whether repetitive application of this tech-
field free of motion and primarily test the pursuit system. This nique might lead to stable benefits. Unfortunately treatment based
technique evokes an optokinetic nystagmus but not the subjective on neck vibration has attracted little research. At the moment only
impression of body rotation. Kerkhoff (2002) investigated in a pilot two studies have been published.
study with three right-brain damaged neglect patients whether Schindler et al. (2002) evaluated in a controlled crossover treat-
the repetitive application of small-field OKS may induce lasting ment study whether repetitive application of contralesional neck
improvements in visual neglect. All subjects received standard vibration (NMV) in combination with standard visual exploration
visual exploration training (3 sessions per week) throughout the training is superior to visual exploration training given without
complete course of the pilot study. During a 2-week baseline period neck vibration. Twenty neglect patients were randomly allocated
all subjects were tested four times in a variety of neglect tests to two groups (n = 10 each). Each group received 15 sessions of
to exclude effects of spontaneous recovery and/or test repetition. the respective training for 3 weeks (5 per week), after which
During this period, no significant improvements in any test were the two treatments were reversed and another 15 treatment ses-
seen (despite the visual exploration training being performed). sions with the other treatment were given (crossover design). The
After the fourth baseline test, repetitive optokinetic stimulation results show uniformly larger treatment gains during the neck
was given for 5 sessions (each with 45 min duration, delivered vibration + exploration training (regardless of the time when it
in a period of 10–14 days). After OKS-training, auditory neglect was received) as compared to exploration training without con-
and neglect dyslexia were substantially improved. Likewise, visual comitant neck vibration. Significant improvements in the visual
cancellation performance had significantly improved in all three straight ahead, cancellation and reading were obtained after the
patients after OKS. These improvements remained stable after a combined treatment. Furthermore, the improvements transferred
2-week-follow-up in all cases. Interestingly, these improvements to a tactile search task in peripersonal space thus showing multi-
were obtained in two modalities of neglect (vision and audition) modal efficacy. Moreover, the improvements transferred to several
which underlines the multimodal efficiency of small-field OKS activities of daily living as rated before and after the treatment
as already documented with short-term optokinetic stimulation. blocks by nurses who were ‘blind’ to the treatment type. Accord-
These positive findings were mostly confirmed in later studies, all ing to these ratings, combined neck vibration and visual exploration
using small-field OKS stimulation stimulating the pursuit system treatment led to greater improvements in reaching, grasping, trans-
(Keller, Lefin-Rank, Losch, & Kerkhoff, 2009, Kerkhoff et al., this fers from/to bed and wheelchair, and dressing as compared to pure
issue; Kerkhoff, Keller, Ritter, & Marquardt, 2006; Schröder, Wist, & visual exploration treatment. In a subsequent study with 5 neglect
Hömberg, 2008; Thimm et al., 2009). There is however an interest- patients studied in a single case experimental design it was shown
ing exception: Pizzamiglio et al. (2004) found no significant benefits that NMV alone yielded comparable and lasting improvements
with full-field OKS training. It is therefore interesting to look at the in visual neglect, without concurrent visual exploration training
features which distinguish Pizzamiglio et al.’s study from studies (Johannsen, Ackermann, & Karnath, 2003). In summary it appears
which achieve positive results. It turns out that in the Pizzamiglio- that NMV provides a viable treatment option for neglect. To apply
study patients were asked to refrain from pursuit eye-movements NMV vibrating equipment is required and in the past this may have
whereas in the other studies such eye-movements were encour- deterred clinicians from employing this treatment procedure more
aged. It therefore appears that smooth pursuit eye movements are frequently.
an important therapeutic ingredient of the OKS training. This con-
clusion is corroborated by functional imaging data: Konen, Kleiser, 3.3. Caloric- and galvanic-vestibular stimulation
Seitz, and Bremmer (2005) showed that active tracking of OKS dis-
plays yields more widespread activations in the parieto-temporal Cold water (caloric) vestibular stimulation (CVS) of the con-
cortex of healthy subjects than passive “stare-gazing”. In summary tralesional ear (usually the left) or warm water stimulation of
it seems that OKS is an effective treatment for neglect but it is the ipsilesional ear (the right in patients with left neglect) stim-
also clear that even this technique requires some amount of active ulates the horizontal ear canal of the vestibular system and
patient-participation. induces a vestibular nystagmus, i.e. reflexive, rhythmical oscilla-
tions of the eyeballs consisting of quick and a slow phase, together
3.2. Neck-muscle vibration (NMV) with a deviation of the so-called ‘Schlagfeld’ of the nystagmus.
CVS reduces sensory neglect in visual exploration and straight
The logic underlying neck-muscle vibration is not dissimilar to ahead tests for some 10–15 min. This procedure also improves
that underlying OKS. We only feel that our head is looking straight neglect-related disturbances of the body scheme, unawareness
if the proprioceptive signals from our neck-muscles indicate that of hemiplegia and postural imbalance as well (Rode et al., 1992;
both muscles are stretched to the same extent. Vibration over the Rode, Perenin, Honoré, & Boisson, 1998; Rode, Tiliket, Charlopain,
left neck-muscles induces an illusory lengthening of the stimulated & Boisson, 1998). CVS also improves the deviation of the subjective
muscles. The effect is a paradoxic illusion of a continuous, constant visual straight ahead (Karnath, 1994) and improves somatosen-
movement to one side. This illusion is present as long as the vibra- sory neglect phenomena for a similar time period (Vallar, Guariglia,
tory stimulus is applied on the muscle(s). Vibration over the left & Rusconi, 1997; Vallar et al., 2003). Hence, this type of sensory
neck muscles does not only evoke the impression that the head is stimulation exerts multimodal positive effects on many aspects of
 G. Kerkhoff, T. Schenk / Neuropsychologia 50 (2012) 1072–1079 1075

the neglect syndrome. CVS in healthy subjects leads to a strong goggles could also be used to neutralize the rightward bias of
activation of a large cortico-subcortical network including pari- neglect patients. Rossetti et al. (1998) tested this idea and found
etal, temporal, insular and subcortical regions of the hemisphere not only a significant reduction of neglect symptoms but also found
contralateral to the cold-water-stimulated ear (Bottini et al., 1994, that the prism-induced alleviation of neglect symptoms will last for
2001). Despite its short-term effectiveness, caloric stimulation has at least 2 h and thus much longer than the alleviation obtained with
not been evaluated as a tool for long-term or repetitive stimulation. OKS, NMV and caloric stimulation. It is partly the simplicity of the
This is largely due to the vestibular habituation phenomenon asso- procedure but also the fact that the effects on neglect seem so sta-
ciated with repeated caloric stimulation. The typical side effects of ble which accounts for the fact that this procedure has attracted in
this stimulation like vertigo and vomiting encountered in normal recent years more research than all of the other treatment options
subjects are not experienced by neglect patients (Rode, Perenin, combined. Another article in this special issue deals with the theo-
et al., 1998). retical and clinical insights that have been produced by this intense
Galvanic-vestibular stimulation (GVS) stimulates the vestibu- research activity. We will therefore only provide a brief summary
lar system electrically via small intensities of current from two on the use of prism adaptation as a tool for neglect rehabilitation
electrodes (one anode and one cathode) applied to the left and in this section.
right mastoids (or vice versa) behind the ears of the subject (see Despite its early promise it now appears that a single session or
Utz, Dimova, Oppenlander, & Kerkhoff, 2010, for a detailed recent even a few sessions of prism adaptation are insufficient to produce
review). Underneath the mastoids the vestibular nerve runs from stable benefits. Using a single session of prism adaptation and com-
the inner ear toward vestibular brain stem nuclei, which in turn paring this to a single session of pointing without prism goggles,
are interconnected with thalamic relay stations (nucleus ventro- Rousseaux, Bernati, Saj, and Kozlowski (2006) found no significant
posterolateralis). From there, ascending vestibular fiber pathways improvement of neglect symptoms specific to prism adaptation.
reach a number of cortical vestibular areas including area 2cv near More recently Nys, Seurinck, and Dijkerman (2008) used a proto-
the central sulcus, area 3a,b in the somatosensory cortex, parietal col which included four training sessions and found a short-term
area 7a, and the parieto-insularvestibular-cortex (PIVC; Guldin & but no long-term advantage for training with prismatic goggles. In
Grüsser, 1998). Although for the vestibular modality there seems contrast protocols using 10 or more sessions of prism adaptation
to be no primary cortex as in the visual, auditory or tactile modality, found reliable, generalizable benefits which lasted for at least 5
the above-mentioned array of multiple, interconnected vestibular weeks after the end of the therapy (Frassinetti, Angeli, Meneghello,
cortical areas is thought to be under the control of the PIVC. GVS is Avanzi, & Ladavas, 2002). This finding was again confirmed in a
an attractive technique for research and treatment since the appli- more recent study (Serino, Barbiani, Rinaldesi, & Ladavas, 2009).
cation is relatively easy and safe as long as safety guidelines are One study using a randomized placebo-controlled design did not
adhered to (Utz, Korluss, et al., 2011). Studies with neglect patients find a significant treatment advantage for the prismatic training,
show that CVS and GVS have a similar immediate effect on neglect but the goggles used in this study were much weaker (6◦ as com-
symptoms (Utz, Keller, Kardinal, & Kerkhoff, 2011). Studies with pared to 10◦ or even 20◦ ) than in other studies (Turton, O’Leary,
neglect patients show that CVS and GVS have similar effects on Gabb, Woodward, & Gilchrist, 2010). The number of sessions (i.e. 10
neglect symptoms. One might speculate that repetitive application training sessions) used in the study by Turton et al. (2010) was the
of CVS and GVS might induce improvements which outlast the stim- same as in two studies which provided evidence of positive effects
ulation period. However, currently there is only one study where (Ladavas, Bonifazi, Catena, & Serino, 2011; Serino et al., 2009). We,
this approach has been tried. Kerkhoff et al. (2011) used repetitive therefore, think it is most likely that weak goggles rather than too
GVS to treat tactile extinction. They found stable treatment effects few trainings sessions are responsible for the negative outcome of
which outlasted the stimulation period (see Section 6.2). But in gen- the Turton et al. study.
eral it is too early to judge the long-term therapeutic potential of In summary it appears that repetitive prism adaptation can pro-
this technique. duce significant treatment benefits. But by now it is also clear that
a treatment using prism adaptation is not necessarily less time-
3.4. Prism adaptation consuming than other forms of neglect therapy.

Prism adaptation is another technique that can be used to cor-

4. Classics and newcomers
rect the rightward orientational bias of patients with neglect. In
the typical case of prism adaptation, as applied to neglect patients,
Recent reviews have typically focused on the sensory stim-
subjects wear right-shifting wedge prisms. As a consequence every-
ulation methods which we reviewed in Section 2. This is
thing is seen as shifted to the right. However, when subjects point
understandable and reflects the fact that sensory stimulation
to where they see the visual target they will notice that their hand
methods have recently attracted significantly more research than
ends up to the right of the real target location. Given the opportu-
other treatment techniques. However, a review on neglect-therapy
nity to observe at least part of their hand movements, they can
would be incomplete without mentioning some of the newer and
compensate for the right-shifting errors and over time achieve
some of the classic but now often neglected treatment options.
more accurate pointing movements. After the adaptation period the
Those options range from low-tech eye-patch techniques to high
prism goggles will be removed and subjects will be asked to point
tech TMS treatments. The clinical evidence base for all of these
to visual targets but this time they cannot see their own hand and
techniques is currently too sparse to judge their potential and
therefore cannot judge the accuracy of their pointing movements.
efficiency. We therefore decided to simply provide a table which
In this situation a so-called post-prismatic after-effect is observed.
provides some details on the techniques and list relevant studies
Subjects will now point consistently to the left of the visual target.
(see Table 1).
Another way to assess this after-effect is to ask subjects to close
their eyes and indicate with their outstretched arm what they per-
ceive as the straight-ahead direction. It can be observed that after 5. Mix and match
the adaptation phase, the direction of their straight-ahead is rotated
toward the left (for a review of the prism adaptation procedure, During the last two decades a significant number of new options
see (Redding & Wallace, 2006; Redding, Rossetti, & Wallace, 2005). for the treatment of neglect patients have been introduced. The
This observation suggests that prism adaptation with right-shifting challenge today is thus to decide how to mix and match the
1076 G. Kerkhoff, T. Schenk / Neuropsychologia 50 (2012) 1072–1079

Table 1
List of novel and promising modulation or treatment techniques for patients with spatial neglect Harvey.

Technique Reference Sample Outcome

Repetitive TMS (theta-burst) of the left parietal Nyffeler, Cazzoli, Hess, and N = 11 patients with left visual Transient improvements in visual
cortex Muri (2009) neglect exploration in left hemispace after 2–4
sessions of Theta-Burst TMS; positive
after-effects maintained up to 32 h
post-stimulation after 4 TBS. Theta-Burst
TMS may thus promote faster recovery
from neglect, when repetitively applied
20 sessions of left parietal TMS Song et al. (2009) 2 × 7 patients with left visual rTMS improved line cancellation and line
neglect bisection selectively in the group
receiving rTMS in addition to
conventional neglect rehabilitation
(scanning). rTMS might thus promote
treatment-induced recovery from
neglect
Transcranial direct current stimulation (TDCS) Sparing et al. (2009) 10 patients with left visual Direct current stimulation of the parietal
of the left- vs. right parietal cortex neglect cortex transiently modulated visual
neglect in a polarity-specific way.
Repetitive stimulation may potentially
reveal therapeutic effects in neglect
patients
Visuomotor feedback training (patients are Harvey, Hood, North, and 2 × 7 patients with left visual Assessment after the experimenter-led
presented with horizontally extended Robertson (2003) neglect (one group of 7 took 3-day intervention showed that patients
wooden rods and asked to lift them) part in the visuomotor in the intervention group improved in a
feedback training, the other third of all neglect tests. Patients
group of 7 was assigned to the performed a further 2-week patient-led
control condition (no training. The 1-month post-training
treatment)) assessment showed improved in 46% of
the neglect tests. These are promising
results which so far have largely been
neglected
Combination of visual scanning training plus Polanowska, Seniow, Paprot, 2 × 20 patients with left visual Additional left-hand electrical
functional electric stimulation (FES) of the Lesniak, and Czlonkowska, neglect, most of them with somatosensory stimulation increased the
left hand (2009) leftsided paresis/plegia effects of visual scanning training at
1-month post-test; leftsided
somatosensory deficits did not weaken
the positive effect. This may be
particularly helpful for the treatment of
patients with hemisensory loss
Functional electric stimulation (FES) of the left Harding and Riddoch (2009) 4 patients with left visual FES improved visual neglect in 3 of the 4
forearm neglect and patients; stable results at 6-months-post
hemiparesis/-plegia treatment
Right-half field eye-patching in combination Tsang, Sze, and Fong (2009) 2 × 17 patients with left visual Greater improvements of the group that
with conventional occupational therapy vs. neglect received right-half field eye patching in
sole occupational therapy addition to conventional occupational
neglect therapy than in the group
without eye patching in conventional
neglect tests, but only partially in
impairment tests (partially in eating,
bathing, dressing)
Interactive virtual environment training for Katz et al. (2005) 8 vs. 11 patients with left Both groups improved, but the group
safe street crossing of neglect patients visual neglect receiving virtual reality training of street
crossing improved more in some
measures of the virtual reality tests and
in some measures of real street crossing.
VR-training may be an additional helpful
tool to address problems of daily life
such as street crossing, moving in traffic
situations

treatment options that are available. Mixing and matching in this combined NMV with visual scanning and compared this combi-
context means matching the treatment options to the patient, nation to visual scanning therapy on its own. They found a clear
selecting those treatments which are superior to others and com- superiority for the combined therapy. More recently Saevarsson,
bining them in ways that will enhance the treatment outcome. Kristjansson, and Halsband (2010) showed that combining NMV
Currently this process is based on instinct and also – we sus- with prism adaptation is again significantly more effective than
pect – on habit and available resources. This is unavoidable since NMV on its own and Schröder et al. (2008) reported that combin-
there are currently no evidence-based recommendations which ing visual exploration therapy either with OKS or with TENS yields
could help the clinicians to match the treatment to the patient, better results than visual exploration therapy on its own. They also
select the best treatment and combine it with other techniques found that adding OKS is more advantageous than adding TENS.
in the most advantageous way. However, there is some progress Thus, at the moment it might appear that any multi-component
with respect to the last question. In this section we will describe therapy is better than any mono-therapy. This presumption is how-
four studies that examined whether multi-component treatments ever contradicted by a recent study from Keller, Lefin-Rank, Losch,
are more effective than mono-therapies. Schindler et al. (2002) and Kerkhoff (2009). They compared OKS + PA with OKS alone and
 G. Kerkhoff, T. Schenk / Neuropsychologia 50 (2012) 1072–1079 1077

found that the combined treatment provides no significant bene- contributes to the swallowing problems in these cases the applica-
fits. A different view could therefore be that what matters more is tion of sensory stimulation techniques, which proved effective in
not how you combine treatment but which treatment you choose. the treatment of visual and auditory neglect, might also ameliorate
It appears that OKS is a fairly effective treatment and its bene- signs of dysphagia in these patients.
fits seem to be largely independent of the context in which it is
presented. Other treatments such as PA, NMV and TENS seem to 6.2. Sensory extinction
produce significant benefits but in less reliable ways and VET on its
own is consistently inferior to any multi-component therapy. This A phenomenon which is often associated with the neglect syn-
suggests a hierarchy of treatments with OKS at the top, PA, NMV drome or sometimes considered to be a minor form of neglect
and TENS in the middle and VET at the bottom of the efficiency by some researchers is extinction. Extinction of sensory stimuli
scale. However, this is largely speculative at the moment and just is defined as the inability to process or attend to the more con-
goes to show that what is really needed are studies which directly tralesionally located stimulus when two stimuli are simultaneously
compare different treatment options against each other and against presented. By definition, the processing of a single stimulus should
a placebo treatment. be only marginally impaired, thereby ruling out gross elementary
sensory deficits (i.e. hemianopia, hemianaesthesia, unilateral hear-
ing loss).
6. Scotomas in neglect research Although extinction is frequently found in different modalities
(visual, haptic, auditory) only a few studies examined the impact of
6.1. Nonvisual neglect neglect therapy on extinction. Those studies used mostly a single
session approach and found regardless of whether they used CVS
Most treatment studies focus on visual neglect and pay lit- (Vallar, Bottini, Rusconi, & Sterzi, 1993), OKS (Nico, 1999), periph-
tle attention to other aspects of the neglect syndrome, namely eral magnetic stimulation (Heldmann, Kerkhoff, Struppler, Havel, &
auditory, somatosensory, haptic forms of neglect, body-neglect, Jahn, 2000) or PA (Maravita et al., 2003) a transient improvement of
motor neglect or representational neglect. This is most likely due signs of sensory stimulation. In a recent multi-session study it was
to the easy availability and practical assessment of visual neglect shown that GVS can lead to reduced tactile extinction, an effect that
by conventional screening tests (i.e. Bells test, Mesulamı̌s test) lasts for more than 3 months (Kerkhoff et al., 2011). The findings
and neglect test batteries (Wilson, Cockburn, & Halligan, 1987). are based on a small group of patients and should be considered
In contrast tests for the assessment of auditory, somatosensory, preliminary, but they suggest that multiple-session sensory stim-
haptic or motor neglect are not widely available and the dis- ulation therapy could also be usefully employed to improve signs
tinction between basic deficits (e.g. hearing loss in the case of of sensory extinction.
auditory neglect or hemiplegia in the case of motor neglect) and
neglect-related deficits in the auditory, haptic, somatosensory and 6.3. Transfer and treatment intensity
motor domain can be difficult. Despite these difficulties it should
be borne in mind that non-visual forms of neglect can be very Bowen and Lincoln (2007) pointed to the dearth of evidence
disabling and should therefore be considered in the evaluation and demonstrating a clear transfer of treatment benefits into the daily
development of neglect treatments. In the case of motor neglect lives of patients. Part of the problem is that there are hardly any
mirror therapy could prove useful. During mirror therapy, a mirror objective and standardized measures that would allow researchers
is placed in the patientı̌s midsagittal plane, presenting the patient to assess how patients cope with real life activities. Most activities
with the mirror image of his or her nonaffected arm (Dohle et al., of daily life (ADL) measures use reports or questionnaires which
2009). The mirror image of the ipsilesional right arm activates the target a wide range of activities and disabilities (e.g. FIM, Granger,
right hemisphere because it is perceived as the contralesional left Hamilton, Linacre, Heinemann, & Wright, 1993), for an exception,
arm in the mirror. Several studies have shown that mirror therapy see the Catherine Bergego Scale (Azouvi et al., 2003). As a conse-
improves arm function (Dohle et al., 2009), hand function (Yavuzer quence these questionnaires are not only lacking in objectivity, they
et al., 2008), and leg function (Sutbeyaz, Yavuzer, Sezer, & Koseoglu, are also often too crude to detect neglect-specific improvements.
2007) in patients with unilateral acute hemiparesis after stroke. To put it simply a patient with recovered neglect and hemiplegia
Interestingly, the study by Dohle et al. (2009) noted also significant will still require help in many situations as a consequence of the
improvements in visuospatial neglect after mirror therapy. Mirror remaining hemiplegia and thus her score on a functional indepen-
therapy might therefore provide an effective add-on treatment to dence measure might therefore not look much improved. But does
rehabilitate motor functions and sensory neglect at the same time. that mean that the therapy leading to the recovery from neglect was
Dysphagia (swallowing disorders) is often observed in patients useless? This patient may still need help, but this help will be easier
with right-hemisphere stroke and left-sided neglect (Andre, Beis, to administer because the patient will cooperate, the patient will
Morin, & Paysant, 2000). These patients tend to neglect food and be able to read and entertain herself better (typically not an item
saliva in their mouth, display a lack of exploratory movements of on most disability scales), will be less likely to bump into obstacles
their tongue toward their left part of the mouth, just as in ocu- and in general will be less frustrated by experiencing her exter-
lar or manual exploration of the contralesional space. The clinical nal environment as strange, confusing and unobliging. The transfer
signs of the disorder include dribbling, choking, retention of food of benefits into the real life is certainly an important issue, but
and an impairment of tactile detection and taste sensation in the the problem here is not just a reluctance of researchers to apply
affected part of the mouth. Affected patients appear to be unaware appropriate measures, it is the lack of valid, objective and sensitive
of their left body (mouth) side, which so far has been largely measures and the lack of an agreed consensus on what we should
ignored in studies looking at the efficacy of neglect therapy. Impor- consider as a significant and relevant improvement.
tantly, neglecting food during swallowing can cause aspiration (i.e. However, another problem might also be that evidence for
food/saliva getting into the trachea and from there into the lungs) transfer of treatment benefits into the patients’ daily lives is missing
of food or saliva and can thereby lead to life-threatening situations. because such transfer might require a different form of treatment.
Despite its clinical relevance there is little empirical research on this Sohlberg and Mateer (2001) have argued that transfer does not hap-
topic. It is currently unclear whether these problems are caused by pen, transfer needs to be trained. Such training of transfer which
loss of sensory or motor function or unilateral neglect. If neglect involves the therapy-guided application of treatment gains to ADL
1078 G. Kerkhoff, T. Schenk / Neuropsychologia 50 (2012) 1072–1079

situations is not a standard component of any of the reviewed tool for a given patient and to know how to combine the different
neglect therapies. However, it might have to become one if we wish available treatments for maximum effect. To answer this challenge
to see evidence of transfer to ADL situations. In this context it is we need empirical evidence which identifies the best treatment,
also worth pointing out that transfer might be related to treatment the optimal amount of treatment sessions, the best combination of
intensity. As previously mentioned early neglect treatment stud- treatments and provides treatment-specific predictors for therapy-
ies found that a minimum of 40 treatment sessions are required to responders. While in recent years some progress has been made in
obtain significant and lasting effects on ADL tasks (Antonucci et al., this respect, much more research is needed. This is also true for a
1995; Kerkhoff, 1998b). The difficulty with more recent treatment number of other topics. While in the past most research focused
studies might lie in the fact that even multi-session protocols rarely on visual neglect other equally relevant aspects such as auditory,
used more than 20 treatment sessions. This points to a more general motor or buccal neglect received little attention. Moreover, neglect
shortcoming of current research on neglect therapy, namely that in childhood has received little attention, and treatment of chil-
there is no systematic effort to establish which intensity (massed or dren with neglect even less (Bollea et al., 2007). We have no doubt
distributed practice) or duration of treatment is needed to achieve that some of these ignored topics will be duly addressed by future
long-lasting and transferable treatment benefits. research. However, there are some gaps in neglect research, which
have a longer history. Reviewers have criticized for some time that
too little research into the long-term effects of neglect-therapy and
6.4. Funding for rehabilitation research
its transferability into daily life are conducted. The fact that little
has changed despite these reminders suggests that the underlying
However, the most relevant scotoma is perhaps not a blindness
problem is not ignorance but lack of available funding resources.
of researchers but a blindness of funding agencies. We tend to
Along with many others we are convinced that today the biggest
return to the same questions (reviews) and bemoan the same
obstacle to progress in neglect rehabilitation is not the lack of ideas
shortcomings: lack of randomized control studies, studies with
but the lack of funding.
too few training sessions, lack of long-term follow-up, no objective
measures of transfer into ADL, no direct comparison of different
treatments, no large-scale, multi-center studies (e.g. Bowen & Acknowledgment
Lincoln, 2007). We could go on describing these shortcomings.
But if researchers fail to address those questions it is surely not This work was partially supported by a grant from the Deutsche
because of ignorance but because of structural weaknesses in the Forschungsgemeinschaft (IRTG 1457 “Adaptive Minds”) to Georg
system and we all know what these structural weaknesses are. Kerkhoff.
Long-term studies can only be performed if the time is provided
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