David T. Wilkinson

The relevance of behavioural measures for functional-imaging studies of cognition

The psychological structure of cognition is often inferred from conjoint measures of behaviour (such as reaction time) and brain activation (such as cerebral blood flow). In many experiments these measures produce divergent results. One example is where a significant pattern of brain activation occurs without a corresponding change in overt behaviour. In such circumstances, can cognitive theory be informed from brain-activation data alone? Or, given the more established link between behaviour and cognition, is behavioural corroboration necessary?

Galvanic vestibular stimulation speeds visual memory recall

The experiments of Alessandro Volta were amongst the first to indicate that visuo-spatial function can be altered by stimulating the vestibular nerves with galvanic current. Until recently, the beneficial effects of the procedure were masked by the high levels of electrical current applied, which induced nystagmus-related gaze deviation and spatial disorientation. However, several neuropsychological studies have shown that much weaker, imperceptible currents that do not elicit unpleasant side-effects can help overcome visual loss after stroke. Here, we show that visual processing in neurologically healthy individuals can also benefit from galvanic vestibular stimulation. Participants first learnt the names of eight unfamiliar faces and then after a short delay, answered questions from memory about how pairs of these faces differed. Mean correct reaction times were significantly shorter when sub-sensory, noise-enhanced anodal stimulation was administered to the left mastoid, compared to when no stimulation was administered at all. This advantage occurred with no loss in response accuracy, and raises the possibility that the procedure may constitute a more general form of cognitive enhancement.

Switching between the forest and the trees: Brain systems involved in local/global changed-level judgments

Visual targets can be coded, in relative terms, at either the local or the global level of stimuli. Previous studies have indicated that targets are identified more slowly when they appear at a new hierarchical level, compared to when they reappear at the same level as in the previous trial. In the present study, we used measures of reaction time and event-related fMRI to investigate factors affecting this switch cost. In particular, we examined the effects of the number of repeated-level trials preceding a switch and whether the cue to switch was either externally or internally mediated. At the behavioral level we found that (1) the time taken to identify a target on a changed-level trial is longer following four repeated-level trials compared to two repeated-level trials, but that runs of six do not produce additional costs over four, and (2) targets can be identified faster following externally cued switches compared to internally mediated switches. We then show that these behavioral effects are associated with distinct patterns of neural activation. Switches performed after two repeated-level trials preferentially activated the precuneus, while those performed after both four and six activated bilateral inferior parietal cortex and motor hand area. Relative to external switches, internal switches activated the putamen, while both kinds of switch conjointly activated the large-scale network proposed to underlie internal/external switches in nonhierarchical tasks. Our data further clarify the mechanisms mediating hierarchical selection.

Improvement of a face perception deficit via subsensory galvanic vestibular stimulation

The remediative effect of galvanic vestibular stimulation (GVS) was investigated in a patient who, following right hemisphere damage, is profoundly unable to recognize faces. We administered a two-alternative forced choice match-to-sample task in which the patient had to choose which of two faces matched a sample face presented directly above, while bipolar, transcutaneous current was applied to the left and right vestibular nerves at a level below the patients sensory threshold. Performance improved beyond the chance-level observed prestimulation, and relied on reversing the electrode polarity across two separate blocks of trials, such that each mastoid received positive current for one block and then negative charge for the next. Although our study involved only a single case, the data provide preliminary evidence that a deficit in perceptual face matching can be reduced by GVS. This raises the intriguing possibility that other unilateral visual disorders may also respond in such a manner.

Improvement of a figure copying deficit during subsensory galvanic vestibular stimulation

We describe the effects of galvanic vestibular stimulation (GVS) on an individual who, following right hemisphere stroke, is unable to copy figures accurately. His copies contain most of the constituent elements, but are poorly integrated and drawn in a seemingly haphazard manner. To test whether GVS could help overcome these difficulties, we administered the Rey-Osterrieth complex figure copy task while manipulating both the presence and laterality of the galvanic signal. The signal was applied at a level that was too low to elicit sensation which ensured that the individual was unaware of either when or on what side he was being stimulated. Relative to a sham condition, two consecutive blocks of GVS increased both the accuracy with which the main configural elements of the figure were reconstructed, and there was some, albeit less consistent evidence, that these were drawn in a more wholistic as opposed to piecemeal manner. Improvement was not reliant on the polarity of the stimulating electrodes. These results suggest that GVS can help overcome difficulties in the perception and/or reconstruction of hierarchical visual form, and thereby uncover a new link between vestibular information processing and visual task performance.

Galvanic vestibular stimulation in hemi-spatial neglect

Hemi-spatial neglect is an attentional disorder in which the sufferer fails to acknowledge or respond to stimuli appearing in contralesional space. In recent years, it has become clear that a measurable reduction in contralesional neglect can occur during galvanic vestibular stimulation, a technique by which transmastoid, small amplitude current induces lateral, attentional shifts via asymmetric modulation of the left and right vestibular nerves. However, it remains unclear whether this reduction persists after stimulation is stopped. To estimate longevity of effect, we therefore conducted a double-blind, randomized, dose-response trial involving a group of stroke patients suffering from left-sided neglect (n = 52, mean age = 66 years). To determine whether repeated sessions of galvanic vestibular stimulation more effectively induce lasting relief than a single session, participants received 1, 5, or 10 sessions, each lasting 25 min, of sub-sensory, left-anodal right-cathodal noisy direct current (mean amplitude = 1 mA). Ninety five percent confidence intervals indicated that all three treatment arms showed a statistically significant improvement between the pre-stimulation baseline and the final day of stimulation on the primary outcome measure, the conventional tests of the Behavioral Inattention Test. More remarkably, this change (mean change = 28%, SD = 18) was still evident 1 month later. Secondary analyses indicated an allied increase of 20% in median Barthel Index (BI) score, a measure of functional capacity, in the absence of any adverse events or instances of participant non-compliance. Together these data suggest that galvanic vestibular stimulation, a simple, cheap technique suitable for home-based administration, may produce lasting reductions in neglect that are clinically important. Further protocol optimization is now needed ahead of a larger effectiveness study.

The Effects of Interdistracter Similarity on Search Processes in Superior Parietal Cortex

The superior parietal lobe has been associated with the spatial integration of visual features, an important step in the detection of particular form conjunctions. However, behavioral research has indicated that when target items can be segmented from neighboring distracters via similarity grouping, detection may not rely on spatial integration. The question therefore arises as to whether the superior parietal cortex is an integral component of conjunction search or only important in the absence of certain grouping relations. Here, we acquired measures of reaction time and event-related fMRI, while subjects searched for conjunction targets in displays containing either homogeneous or heterogeneous distracters. We confirm that under conditions of low distracter similarity, search involves parietal-motor areas associated with spatial selection. However, we also demonstrate that under conditions of high distracter similarity, search is instead associated with activation of right temporal-parietal cortex. These results suggest that the superior parietal cortex is not a necessary component of visual conjunction search and highlight a new role for the right temporal-parietal cortex in perceptual grouping.

The effects of stimulus symmetry on landmark judgments in left and right visual fields.

Line bisection impairment is greater following right compared to left hemisphere damage, suggesting that some of the underlying visuo-spatial mechanisms may be lateralised. One important perceptual component of line bisection is estimating stimulus midpoint. Here, we used a modified version of the perceptual landmark task to examine, in healthy individuals, how the midpoint of a stimulus is apprehended, and if the cerebral hemispheres are equally as efficient in performing such a task. We show that the right, relative to the left, hemisphere is both faster and more accurate at apprehending prebisected lines, but no better at apprehending misbisected lines. We then demonstrate that the right hemisphere advantage stems from a specialisation in detecting stimulus symmetry; by associating prebisected lines with the presence of display symmetry, transect location can be inferred without having to explicitly calculate the midpoint of lines. The findings provide a further reason why right hemisphere damage is so deterimental to perceptual line bisection. In addition, the data indicate that the detection of visual symmetry is preferentially lateralised to the right hemisphere.

Unilateral damage to the right cerebral hemisphere disrupts the apprehension of whole faces and their component parts.

Although most cases of acquired prosopagnosia are accompanied by bilateral brain lesions, a number also arise following right unilateral lesions. The prevailing consensus is that right hemisphere damage disrupts the configural apprehension of faces, which in turn forces a reliance on part-based processing. Here we describe a patient who following right hemisphere damage is not only unable to apprehend the configural aspects of faces, but is also unable to apprehend their component parts when these are presented within a whole, upright face. Intriguingly, the patient is able to apprehend face parts when these are presented in isolation, within inverted faces, or in unfamiliar, scrambled arrangements. Furthermore, the patient can make use of configural information to detect local changes in non-face stimuli. The findings uncover a hitherto unreported form of impairment following right unilateral damage, and raise questions about the role of the left hemisphere in processing local information.

The effect of repeated sessions of galvanic vestibular stimulation on target cancellation in visuo-spatial neglect: Preliminary evidence from two cases

Objective: In recent years it has emerged that the attentional disorder of visuo-spatial neglect can be overcome via artificial stimulation of the balance system. One means of achieving this is via galvanic vestibular stimulation (GVS), a simple procedure in which tiny, electrical currents are discharged to the part of the scalp overlying the vestibular nerves. Attempts to remediate neglect with GVS have utilized only a single session of stimulation and, although this can induce spontaneous recovery, symptoms resurface soon after stimulation. This study assessed whether repeated sessions induce longer carry-over. Methods: Two individuals diagnosed with neglect post-stroke received 5 days of sub-sensory, left anodal GVS. Performance was assessed via the letter and star cancellation tasks of the Behavioural Inattention Test on four occasions; 3 days before the start of stimulation, on the first and last day of stimulation and 3-days after stimulation. Results: Analyses of variance indicated that both participants missed significantly fewer targets in both tasks on the fifth day of stimulation compared to baseline. More so, this improvement was still evident at follow-up 3 days later. Conclusion: The results strengthen the need for a larger, sham-controlled trial to establish whether repeated GVS provides lasting relief from neglect.