http://journal.frontiersin.org/article/10.3389/fnhum.2016.00348/full?
- 1Institute of Psychology, University of Graz, Graz, Austria
- 2BioTechMed Graz, Graz, Austria
- 3Klinik Judendorf-Straßengel, Graz, Austria
Methods: The present study aimed at investigating behavioral and electrophysiological effects of 10 sessions of sensorimotor rhythm (SMR) neurofeedback in a 74-years-old stroke patient (UG20). Based on previous results in healthy young participants, we hypothesized that SMR neurofeedback leads to a decrease in sensorimotor interferences and improved stimulus processing, reflected by changes in event-related potentials (ERPs) and electrophysiological coherence. To assess whether UG20 benefited from the training as much as healthy persons of a similar age, a healthy control group of N = 10 elderly persons was trained as well. Before and after neurofeedback training, participants took part in a multichannel electroencephalography measurement conducted during a non-verbal and a verbal learning task.
Results: Both UG20 and the healthy controls were able to regulate their SMR activity during neurofeedback training. Moreover, in a non-verbal learning task, changes in ERPs and coherence were observed after training: UG20 showed a better performance in the non-verbal learning task and a higher P3 amplitude after training than before, and coherence between central and parietal electrodes decreased after training. The control group also showed a behavioral improvement in the non-verbal learning task and tendencies for higher P3 amplitudes and decreased central-parietal coherence after training. Single-case analyses indicated that the changes observed in UG20 were not smaller than the changes in healthy controls.
Conclusion: Neurofeedback can be successfully applied in a stroke patient and in healthy elderly persons. We suggest that SMR neurofeedback leads to a shutting-down of sensorimotor interferences which benefits semantic encoding and retrieval.
Introduction
Electroencephalography (EEG)-based neurofeedback is a
promising tool for cognitive improvement and rehabilitation. While most
traditional cognitive trainings consist of specific tasks that aim at
improving cognitive functions, neurofeedback is aimed at directly
regulating the brain activity underlying cognitive functioning. An
important possible future area of application for neurofeedback is
cognitive rehabilitation of neurological diseases, such as stroke (Doppelmayr et al., 2007; Hofer et al., 2014),
as neurofeedback might be used to directly up-regulate certain aspects
of brain activity while suppressing dysfunctional activations. During
neurofeedback training, brain signals are recorded, processed and fed
back to participants on a computer screen. In most cases, the feedback
is presented auditorily or visually, for example as moving bars that
have to be steered in a certain direction. This feedback enables
participants to voluntarily control their own electrical brain activity.
During sensorimotor rhythm (SMR)-based neurofeedback,
the power of SMR, a frequency band ranging from 12 to 15 Hz, is
extracted from the EEG signal. SMR is an oscillatory rhythm recorded
over central scalp regions, that is supposed to be originating from the
thalamic nuclei, specifically from ventroposterior lateral and reticular
nuclei (Sterman, 1996, 2000).
SMR is observed when one is motionless but mentally focused and
attentive and is suppressed when motor tasks or motor imagery are
carried out (Pfurtscheller, 1981; Sterman, 1996).
Since the beginnings of neurofeedback research, SMR has been utilized
as a feedback frequency band. Several studies have shown that SMR
neurofeedback training can lead to cognitive improvements, mainly in
memory functions and attention (Vernon et al., 2003; Egner and Gruzelier, 2004; Hoedlmoser et al., 2008; Doppelmayr and Weber, 2011; Kober et al., 2015b).
Underscoring its presumable effect of reducing brain excitability, SMR
neurofeedback has been successfully applied in diseases such as epilepsy
and ADHD (Lubar et al., 1995; Tinius and Tinius, 2000; Sterman and Egner, 2006). It was suggested that SMR might facilitate thalamic inhibitory mechanisms (Sterman, 1996, 2000; Egner and Gruzelier, 2004), and block motor activity that interferes with information processing (Pfurtscheller, 1992; Sterman, 1996).
In accordance with this assumption, we found in a previous study that
SMR-based neurofeedback training of healthy young adults leads to
cognitive improvements related to changes in task-related
electrophysiological parameters. Components of event-related potentials
(ERPs), the N1 and P3, were increased after SMR training as compared to
pre-training, indicating more intensive stimulus processing (Kober et al., 2015b).
Importantly, functional brain connectivity between motor areas and
visual processing areas was reduced after SMR training, while
performance in a verbal memory task was improved. Thus, these results
support the idea that SMR up-training leads to an enhanced blocking of
sensorimotor interference, which might be responsible for the observed
improvements in stimulus processing and memory function (Kober et al., 2015b).
However, these results were obtained in a healthy, young sample and
studies assessing the functionality of SMR neurofeedback in elderly
persons and in persons suffering from neurological diseases, such as
stroke (Doppelmayr et al., 2007; Hofer et al., 2014),
are still scarce. Therefore, we aimed to investigate the effects of SMR
neurofeedback in a single-case of stroke. Around 32% of stroke
survivors still demonstrate cognitive sequelae 3 years after the
incident (Patel et al., 2003).
Particularly long-term deficits in attention, memory and executive
functions are common in stroke patients. Importantly, evidence suggests
that specific neurofeedback protocols have largest effects on specific
cognitive functions. For instance, Theta/Beta neurofeedback has mainly
proven successful in improving attention and executive functions (Monastra et al., 2002; Fox et al., 2005; Duric et al., 2012), while SMR neurofeedback has been consistently found to improve memory functions (Vernon et al., 2003; Hoedlmoser et al., 2008; Hofer et al., 2014; Schabus et al., 2014; Kober et al., 2015b).
Thus, neurofeedback training protocols can be chosen according to the
patient’s cognitive deficits. In the present study, we chose to train a
74-years-old stroke patient with memory impairments with SMR
neurofeedback to investigate training feasibility and the effects of the
training on cognition and electrophysiological parameters. We chose to
train the selected patients due to his very specific cognitive deficits
that comprised memory impairments but no deficits of attention or
executive functions. In a previous study, we found that patients with
heterogeneous lesion locations could reach control over their brain
activity during SMR-based and Upper Alpha-based neurofeedback (Kober et al., 2015a).
Therefore, in the present study we chose to base our patient selection
on the cognitive deficits observed rather than on lesion locations.
Hitherto, there is still a lack of studies assessing the
efficiency and feasibility of neurofeedback protocols in stroke
patients. In two studies reported by Doppelmayr et al. (2007),
inconsistent results were observed regarding the efficiency of alpha
and theta-based neurofeedback in stroke patients. While alpha
neurofeedback proved superior to a control treatment in the first study,
this was not replicated in a second study investigating alpha and theta
neurofeedback. In this second study, neither alpha neurofeedback nor
theta was more efficient than a control treatment. On the other hand, in
a range of case studies, positive effects of neurofeedback on cognitive
performance in stroke patients were reported (Rozelle and Budzynski, 1995; Bearden et al., 2003; Cannon et al., 2010).
Still, these studies lack healthy control groups to assess whether
stroke patients can benefit as much from the training as healthy
persons. Therefore, in the present study we included an elderly control
sample for comparison. Single-case control approaches allow the
comparison of the patient’s improvement with the improvement observed in
the healthy elderly (Crawford and Garthwaite, 2002, 2004). In a recent systematic study on stroke patients, Kober et al. (2015a)
observed improvements in memory functions after SMR-based and Upper
Alpha-based neurofeedback training. Effects were stronger than the
effects of traditional cognitive training in a control group of stroke
patients. While this study provided promising evidence that
neurofeedback might be used as an effective tool for cognitive
rehabilitation in stroke patients, the neuronal basis of the observed
behavioral improvements remained unexplored. Thus, in the present study
we set out to investigate electrophysiological parameters in detail in a
stroke patients and a healthy elderly control group before and after
neurofeedback training. Of note, we selected elderly participants as
controls, as there is evidence that electrophysiological brain activity
changes across the life span (Polich, 1997; Klimesch, 1999; Babiloni et al., 2006; Cummins and Finnigan, 2007; Rossini et al., 2007),
which might also affect the functionality of neurofeedback paradigms.
As neurofeedback studies in older persons are still scarce, an
additional aim of the present study was the assessment of the efficiency
of SMR neurofeedback training in the elderly sample. It has been
demonstrated that across the lifespan, cognitive decline is accompanied
by a broad array of changes in brain activation and structure (Hedden and Gabrieli, 2004; Rabbitt et al., 2007; Finnigan and Robertson, 2011).
Based on such observations, one may assume that self-regulation of
brain activity might be an efficient method to counteract age-related
cognitive declines in older persons.
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