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Cross-training in hemispatial neglect: Auditory sustained attention training ameliorates visual attention deficits

Exploring the Mind| Athletics
March 13, 2023•10 min read

Abstract

Prominent deficits in spatial attention evident in patients with hemispatial neglect are often accompanied by equally prominent deficits in non-spatial attention (e.g., poor sustained and selective attention, pronounced vigilance decrement). A number of studies now show that deficits in non-spatial attention influence spatial attention. Treatment strategies focused on improving vigilance or sustained attention may effectively remediate neglect. For example, a recent study employing Tonic and Phasic Alertness Training (TAPAT), a task that requires monitoring a constant stream of hundreds of novel scenes, demonstrated group-level (n = 12) improvements after training compared to a test–retest control group or active treatment control condition on measures of visual search, midpoint estimation and working memory (DeGutis and Van Vleet, 2010). To determine whether the modality of treatment or stimulus novelty are key factors to improving hemispatial neglect, we designed a similar continuous performance training task in which eight patients with chronic and moderate to severe neglect were challenged to rapidly and continuously discriminate a limited set of centrally presented auditory tones once a day for 9 days (36-min/day). All patients demonstrated significant improvement in several, untrained measures of spatial and non-spatial visual attention, and as a group failed to demonstrate a lateralized attention deficit 24-h post-training compared to a control group of chronic neglect patients who simply waited during the training period. The results indicate that TAPAT-related improvements in hemispatial neglect are likely due to improvements in the intrinsic regulation of supramodal, non-spatial attentional resources.

Introduction

The neglect syndrome refers to a collection of spatial and non-spatial attention deficits that can occur after damage to any number of interconnected cortical or subcortical structures, usually in the right hemisphere (e.g., Friedrich et al., 1998, Husain and Kennard, 1996, Karnath et al., 2001, Heilman et al., 1993, Mesulam, 1990, Mort et al., 2003, Posner et al., 1984). While the severity of impairment can vary widely (Hier et al., 1983), the most obvious problem is that patients do not respond to stimuli on the contra-lesional or “neglected” side of space, often seemingly unaware that anything in that space exists (see Driver and Vuilleumier, 2001).

Patients with neglect also exhibit deficits in attention that are not spatially lateralized such as poor time-challenged successive-signal recognition, poor working memory, and poor sustained attention (Danckert and Ferber, 2006, Heilman et al., 1978, Husain et al., 1997, Malhotra et al., 2005, Malhotra et al., 2009, Parton et al., 2006, Robertson et al., 1997, Van Vleet and Robertson, 2006). Interestingly, these non-spatial deficits in attention are often stronger predictors of persistent (chronic) spatial neglect in the post-acute stroke recovery phase than are the contra-lesional visuo-spatial deficits themselves (Peers et al., 2006, Duncan et al., 1999, Hjaltason et al., 1996, Husain et al., 1997, Robertson et al., 1997). Irrespective of their association with lateralized deficits, growing evidence suggests that deficits in non-spatial attentional resources are a fundamental contributor to the neglect disorder.

Changes in tonic attention, that fluctuate over minutes to hours, and/or phasic attention, that fluctuate over fractions of a second, have been shown to modulate spatial bias. Tonic attention provides the cognitive tone for more complex functions such as working memory and executive control (Strum et al., 1997, Posner, 2008) and reducing tonic attention via administration of a sedative results in the immediate re-emergence of spatial neglect symptoms in recovered patients (Lazar et al., 2002). Phasic attention is typically associated with brief alerting stimuli (e.g., presentation of a loud tone) or the occurrence of an unpredicted, behaviorally relevant stimulus (DeGutis and Van Vleet, 2010, Singh-Curry and Husain, 2009). Phasic attention supports cognitive operations such as orienting and selective attention (Posner, 2008, Husain and Rorden, 2003), both of which are often compromised in patients with neglect.

Only a few studies have systematically targeted tonic or phasic aspects of attention in patients with neglect (DeGutis and Van Vleet, 2010, Robertson et al., 1995, Robertson et al., 1998, Thimm et al., 2006). Studies modulating phasic attention exogenously, from the ‘bottom up’, via presentation of an unexpected alerting tone have shown significant improvement in both time-challenged selective attention [attentional blink (AB); Van Vleet and Robertson, 2006] and spatial attention (Robertson et al., 1998), albeit transiently (on the order of seconds of improvement). Studies modulating phasic attention in a more endogenous manner (‘top–down’), as when waiting for the appearance of a target image in a stream of similar distracters (DeGutis and Van Vleet, 2010) have shown sustained improvements (on the order of days to weeks) in selective and spatial attention (see also Thimm et al., 2006).

While several studies have shown a reduction, and in some cases elimination, of patients’ spatial neglect when trained to achieve a more ready and focused attentional state (DeGutis and Van Vleet, 2010, Robertson et al., 1995, Thimm et al., 2006), training focused on both tonic and phasic attention may be more effective as robust, group-level effects have been difficult to demonstrate without explicitly training both mechanisms.

brain hemispheres

In a recent study, DeGutis and Van Vleet (2010) examined the use of a novel training technique designed to engender a sustained focused state of attention. Twelve patients with chronic, moderate to severe neglect were trained in relatively brief daily epochs of Tonic and Phasic Alertness Training (TAPAT) over 9 days. This task required patients to continuously respond via button press to small, briefly displayed scenes presented at central fixation while inhibiting responses to an infrequent target scene. Task improvement was dependent on the ability to intrinsically foster an alert and ready to respond state (tonic attention), but also to periodically and unpredictably inhibit the prepotent motor response (i.e., phasically alter their attention). One day after treatment ended, patients improved to the point where, as a group, they failed to show a spatial bias on sensitive measures of spatial search and object perception as well as a measure of non-spatial, speeded selective attention. Although benefits of training faded over several weeks in the absence of additional training, the magnitude of the training effect was unexpected given the limited training time (4.5 h total).

The therapeutic mechanism(s) of TAPAT warrant further investigation, as a better understanding of the interaction between spatial and non-spatial attention and the plasticity of these attention networks could lead to key insights into the basic mechanisms of interaction between non-spatial and spatial attention and ultimately lead to more effective treatments for patients with hemispatial neglect. First, because TAPAT involves repeatedly and rapidly allocating attention to visual scenes, it could be that improvements in visuo-spatial attention could be related to the visual processing demands. For example, exercising patients’ capacity to quickly grasp the gist of each scene may have led to more efficient recruitment of occipito-temporal (Epstein and Kanwisher, 1998) and posterior parietal regions (Xu and Chun, 2009) involved in gist perception. Alternatively, stimulus novelty (exposure to hundreds of novel images) may have increased patients’ overall level of arousal (Downar et al., 2002) resulting in improved spatial attention. A third possibility is that TAPAT trained patients to more thoroughly engage their intrinsic regulation of attention (see Robertson et al., 1995), allowing both a higher level of attentional engagement/intensity as well as the ability to sustain this level of engagement during demanding tasks.

If enhancing intrinsic alertness is the primary mechanism of TAPAT, the stimulus modality of training should not matter (i.e., intrinsic alertness mechanisms would be similarly engaged by training with auditory stimuli as visual). Additionally, training intrinsic alertness should depend less on external stimulus factors such as novelty or complexity and more on maintaining a consistent level of engagement. To examine these hypotheses, we designed an auditory version of TAPAT which employed substantially fewer and less complex stimuli than the visual training analog (four tones vs 981 images). Eight patients with chronic and moderate to severe neglect were required to continuously engage in the rapid discrimination of a small set of auditory tones by initiating a button press to all non-target tones (90% of trials) and inhibiting their response to the presentation of a target tone (10% of trials). All sounds were presented centrally following a variable inter stimulus interval (ISI) and target tones were randomly intermixed. As in the original TAPAT study, patients were trained on the task for 9 days, 36-min/day. Prior to training, and at 1 and 14 days post-training, subcomponents of visual attention were evaluated using the following measures: visual conjunction search (CS) (DeGutis and Van Vleet, 2010, List et al., 2008, Van Vleet and Robertson, 2006, Van Vleet and Robertson, 2009), subjective midpoint estimation or landmark (LM) task (DeGutis and Van Vleet, 2010) and spatial and non-spatial selective attention (AB; Hillstrom et al., 2004, Van Vleet and Robertson, 2006).

Section snippets

Patients

Sixteen patients (four females) with chronic neglect gave informed consent before participation, in compliance with the Institutional Review Board of the VA Northern California Health Care System in Martinez, California, USA. Their ages spanned 34–78 years, [mean = 66, standard deviation (SD) = 13.6] and all were right-handed (Table 1). Patients were recruited on the basis of a unilateral lesion (all right-sided) to the cerebral cortex, basal ganglia or thalamus (see Table 1 and Fig. 1). Patients

CS

The CS task requires searching for a target object (i.e., red square) amongst an array of distracters that include same-colored objects (i.e., red triangles) and same-shaped objects (i.e., blue squares, see List et al., 2008 for a more complete description). Thus, patients cannot simply search for the color of an object or the shape of an object, but are required to search for the conjunction of the particular shape and color. Displays contained a central fixation crosshair and 14 items.

Results

Pre-training, there was no significant difference between the TAPAT-auditory and control group in age [t(1,14) = −.04, p = .96], time since brain injury [t(1,14) = .20, p = .84], performance on the CS [t(1,14) = .68, p = .50], LM [t(1, 14) = .71, p = .49], or AB [t(1,13) = −.49, p = .63].

Alternative CS

To assess whether the beneficial effects of training shown in the TAPAT-auditory group generalized to a completely novel condition, we examined patients’ search performance for a novel target on an alternative color-shape CS task (blue triangle as target). Patients in the TAPAT-auditory group were assessed on this task at Times 2 and 3 (Post + 1 Day and Post + 14 Days). A 2 × 2 ANOVA with Side (L, R) and Time (2, 3) as factors revealed a significant Main Effect of Time [F(1,12) = 6.99, p < .05], but not

TAPAT-visual versus TAPAT-auditory training outcomes

Because four patients in the auditory TAPAT group (JS, BW, DW, EB) also participated in visual TAPAT training (DeGutis and Van Vleet, 2010) >1-year prior to the current study, we were able to evaluate the influence of auditory TAPAT versus visual TAPAT on several outcome measures. First, on the TAPAT-auditory training task we compared the mean commission accuracy, correct commission reaction time, and omission accuracy on the first and last day of training. While there were no significant

Discussion

In the current study, we examined the effectiveness of an auditory sustained attention training task, in which patients with neglect were required to continuously engage in the rapid discrimination of a limited number of auditory tones, on visuo-spatial aspects of the neglect syndrome. As all sounds were presented centrally, with infrequent and randomly presented target tones, patients were not required to deploy spatial attention. While it is possible that participants did not perceive the

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