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Optimizing Microsurgical Skills With EEG Neurofeedback

Optimizing Microsurgical Skills With EEG Neurofeedback

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BMC Neuroscience
Research article
Optimizing microsurgical skills with EEG neurofeedback 
 TomasRos*
1
, MerrickJMosele
2
, PhilipABloom
3
, LarryBenjamin
4
,LesleyAParkinson
5
and JohnHGruzelie
1
 Address:
1
Department of Psychology, Goldsmiths, University of London, London, UK,
2
Department of Optometry and Visual Science, City University, London, UK,
3
 Western Eye Hospital, London, UK,
4
Department of Ophthalmology, Stoke Mandeville Hospital, Aylesbury, UK and
5
Brainhealth, The Diagnostic Clinic, London, UK Email: TomasRos*-t.ros@gold.ac.uk; MerrickJMoseley-m.j.moseley@city.ac.uk; PhilipABloom-philipbloom@zoo.co.uk;LarryBenjamin-larry.benjamin@btopenworld.com; LesleyAParkinson-lesleyparkinsoncp@hotmail.com;JohnHGruzelier-j.gruzelier@gold.ac.u* Corresponding author 
Abstract
Background:
By enabling individuals to self-regulate their brainwave activity in the field of optimalperformance in healthy individuals, neurofeedback has been found to improve cognitive and artisticperformance. Here we assessed whether two distinct EEG neurofeedback protocols could developsurgical skill, given the important role this skill plays in medicine.
Results:
National Health Service trainee ophthalmic microsurgeons (N = 20) were randomlyassigned to either Sensory Motor Rhythm-Theta (SMR) or Alpha-Theta (AT) groups, a randomizedsubset of which were also part of a wait-list 'no-treatment' control group (N = 8). Neurofeedback groups received eight 30-minute sessions of EEG training. Pre-post assessment included a skills labsurgical procedure with timed measures and expert ratings from video-recordings by consultantsurgeons, together with state/trait anxiety self-reports. SMR training demonstrated advantagesabsent in the control group, with improvements in surgical skill according to 1) the expert ratings:overall technique (d = 0.6, p < 0.03) and suture task (d = 0.9, p < 0.02) (judges' intraclass correlationcoefficient = 0.85); and 2) with overall time on task (d = 0.5, p = 0.02), while everyday anxiety (trait)decreased (d = 0.5, p < 0.02). Importantly the decrease in surgical task time was strongly associatedwith SMR EEG training changes (p < 0.01), especially with continued reduction of theta (4–7 Hz)power. AT training produced marginal improvements in technique and overall performance time,which were accompanied by a standard error indicative of large individual differences.Notwithstanding, successful within session elevation of the theta-alpha ratio correlated positivelywith improvements in overall technique (r = 0.64, p = 0.047).
Conclusion:
SMR-Theta neurofeedback training provided significant improvement in surgicaltechnique whilst considerably reducing time on task by 26%. There was also evidence that ATtraining marginally reduced total surgery time, despite suboptimal training efficacies. Overall, thedata set provides encouraging evidence of optimised learning of a complex medical specialty vianeurofeedback training.
Published: 24 July 2009
BMC Neuroscience
2009,
10
:87doi:10.1186/1471-2202-10-87Received: 23 February 2009Accepted: 24 July 2009This article is available from: http://www.biomedcentral.com/1471-2202/10/87© 2009 Ros et al; licensee BioMed Central Ltd.This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
 
BMC Neuroscience 
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:87http://www.biomedcentral.com/1471-2202/10/87Page 2 of 10
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Background
 The use of EEG biofeedback technology (neurofeedback)to self-regulate brainwave frequencies with the aim of recovering or optimising function and performance isbecoming increasingly established. Its clinical applica-tions include the treatment of epilepsy [1], attentionhyperactivity disorders [2] and addiction [3]. Meanwhile it has also assumed a role in optimising performance inhealthy individuals within fields as diverse as cognition,sport and artistry [4], including NASA research aimed at minimizing pilot error [5]. In particular, recent studiesreport significant improvements in attention [6,7], mem- ory [8], mental rotation [9], mood [10], dance [11] and musical performance [12]. The set of skills required to undertake surgical and micro-surgical procedures includes many of the cognitive andsensorimotor skills which neurofeedback has been shownto enhance. The demands on those undergoing surgicaltraining are considerable and often stressful [13,14].  There may also exist time pressures on those seeking toacquire surgical skills and the availability of expert train-ers is often at a premium. To this end there is investment in developing and evaluating procedures to enhance sur-gical training and performance such as simulation, video, virtual reality, motion tracking and mental training [15-17] In this study, we examine the effect of two neurofeed-back protocols on the acquisition of microsurgical skillsby a group of trainee ophthalmic surgeons. Specifically,fast wave training has been shown to facilitate sustainedattention providing a relaxed attentional focus andincreasing working memory [6-8], of particular impor- tance for surgery which requires agility, concentration andstamina for long periods of time [18,19]. The sensory  motor rhythm neurofeedback protocol helps relax themotor system which is vital in complex sensory-motor performance [4,11]. On the other hand slow wave train- ing may benefit both stamina and morale, for aside fromrelaxation, this protocol enhances mood and well-being,through putative action on the limbic emotion system[10,31] Ophthalmic surgery, by virtue of the scale at   which surgery is undertaken and the extreme adverse con-sequence of error, provides an ideal model with which toevaluate the potential benefits of neurofeedback. In brief,surgical performance in a skills laboratory [14] wasassessed by means of two principal measures, surgicaltime and technique, representing the main critical dimen-sions in surgical proficiency: pace and accuracy [20,21]. Our initial hypothesis was that neurofeedback training  would be able to successfully modify these measures withthe aim of enhancing individual surgical skills-scheduled within the context of standardized and ongoing medicaltraining – by modulating general cerebral function (viamechanisms of neuroplasticity) towards more 'effica-cious' neural information processing appropriate to boththe execution, as well as the retention, of fine sensorimo-tor maneuvers. In this regard surgeons were neither expected nor instructed to emulate or recollect 'neurofeed-back conditions' on their own immediately prior to or during their performances, rather it was envisaged that theneuromodulatory effects of sustained control of the EEG would cumulate and be simultaneously active during thecourse of the multiple surgical training sessions as well asduring the final performance. The first protocol, known as SMR-Theta, aims to elevatethe low beta "Sensorimotor Rhythm" [SMR] (12–15 Hz) while concurrently suppressing theta activity (4–7 Hz),and has been shown to enhance perceptual sensitivity andattentional performance in healthy subjects [4,6,7] result- ing in decreased somatosensory and motor interference inbasal ganglia/thalamocortical circuits [1,22]. This most  likely occurs through the reinforcement of GABAergic inhibitory oscillations, such as those implicated in senso-rimotor gating [23], the genesis of sleep spindles [24], and in reduction of seizure thresholds [25]. On the other hand, latest research points to a possible relationshipbetween the SMR rhythm and long term potentiation(LTP), widely regarded as the main mechanism behindlong term memory. For example, stimulating bursts of oscillations in this frequency range induced long-termmodifications of excitatory neocortical synapses [26].Moreover, 7–14 Hz spindling has also been proposed to'open molecular gates of plasticity [27], by activating Ca
2
+currents prior to transition to stage 1 sleep. This role infacilitating sensorimotor control and memory has clear implications for microsurgical performance. The secondprotocol, commonly referred to as Alpha-Theta (AT), aimsto raise the ratio of theta (5–8 Hz) over alpha (8–11 Hz)activity levels during a wakeful eyes-closed condition inorder to induce a deep relaxation state, given the associa-tion between theta activity and meditative states [28] andthe wakefulness-to-sleep transition [29]. It has been espe-cially employed as a complementary therapy in post-trau-matic stress disorder (PTSD) [30], substance abuse [3], and has been shown to increase wellbeing in socially  withdrawn students [10], as well as enhance artistry inmusic and dance performance [11,12]. Its impact on motivation and mood is thought to be mediated throughlimbic activation and its effects on creativity and sensori-motor performance mediated through its influence onlong distance connectivity [31]. SMR-Theta feedback was visual with eyes open and included a 10 second break after 170 seconds, for a total of 8 such training 'periods', whereas ALPHA training was auditory and subjects weretold to relax in an eyes closed condition, which was unin-terrupted for a full 27 minutes.
Results
One-way ANOVA disclosed no statistically significant dif-ferences between SMR, AT, and control groups in thenumber of days that elapsed between pre- and post-train-
 
BMC Neuroscience 
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ing assessments (F(2,25) = 0.34, p = 0.72). Furthermore,one-way ANOVAs confirmed that there were no statisti-cally significant initial baseline differences between SMR, AT, and control groups in years of prior training (F(2,25)= 0.53, p = 0.59) or on initial baseline measures of surgicaltime [OVERALL: F(2,25) = 0.45, p = 0.64; TASK: F(2,25) =0.48, p = 0.63; PAUSE: F(2,25) = 0.12, p = 0.89; SUTURE:F(2,25) = 0.85, p = 0.44], technique [(OVERALL: (F(2,25)= 0.52, p = 0.60; SUTURE: (F(2,25) = 0.13, p = 0.88], andanxiety [STATE: F(2,20) = 0.5, p = 0.61; TRAIT: F(2,20) =0.78, p = 0.47]. Direct t-test comparisons between AT andSMR groups did not reveal significant differences betweeninitial baseline measures of surgical time [TASK: t 
18
= -0.68, p = 0.51], or technique [(OVERALL: t 
18
= 0.92, p =0.37]. Equally, there were no statistically significant initialbaseline differences between EEG training ratios of median split SMR (F(1,79) = 0.77, p = 0.38) and AT (F(1,96) = 0.83, p = 0.37) groups according to higher andlower performance change scores in task time and overalltechnique, respectively. No significant differences weredetected for initial baseline measures of surgical time or technique between low and high performers within SMR and AT groups respectively.
Surgical Time
Results averaged across tasks are shown in Fig 1, together  with the individual "suture" task. A TIME × GROUPrepeated measures ANOVA disclosed in line with hypoth-eses a main effect of TIME for task time (F(1,25) = 4.92, p= 0.036), as seen in Fig 1. Paired t-tests confirmed that the26% mean improvement (effect size d = 0.49) following SMR training differed significantly pre-post (8:41 min and6:24 min: t 
9
= 2.80, p = 0.021), whereas the 12% meanimprovement in the AT group was not significant (7:16min and 6:24 min: t 
9
= 1.20, p = 0.26), in comparison toa negligible change in the control group (7:12 min and7:04 min: t 
7
= 0.13, p = 0.90). Moreover, the SMR-groupexhibited a significant decrease in the duration of thesuture task (t 
9
= 2.26, p = 0.050). Regarding overall per-formance time, there was only a weak tendency for animprovement (SMR-group: t 
9
= 1.51, p = 0.083, one tailed; AT-group: t 
9
= 1.37, p = 0.10 one tailed; control group: t 
7
= 0.21, n.s.). There was no significant change in the meanpause time for any of the groups, although interestingly there was a non-significant average increase for the SMR-group (t 
9
= -0.61, p = 0.56). As can be seen from Table1,the average baseline task time for the SMR group (8:41) was slightly higher, albeit non-significantly, than in the AT (7:16) and control (7:12) groups. At post assessment,both SMR (6:24) and AT (6:24) neurofeedback groupsdemonstrated a lower final time in comparison to thecontrol (7:04) group, although the difference was not sig-nificant according to a one-way ANOVA (F(2,25) = 0.131,p = 0.878). A similar relationship was seen for the individ-ual 'suture' task (Table1). In summary there was a signif-icant improvement in task time following SMR training,from a level that was non-significantly longer than in theother groups prior to training to a level comparable to the AT group following training. There were no significant changes in the AT and control groups. The reduction intask time in the SMR group was also paralleled by a reduc-tion in the suture task, regarded as the most complex of the tasks.
Mean pre-post change in surgical performance time
Figure 1Mean pre-post change in surgical performance time
.For Alpha-Theta (AT), SMR-Theta (SMR), and control (C)groups. In contrast to the control group, there is a significantreduction in total time on task as well as in the suture task for the SMR group. Marginal improvement is also seen inoverall performance time for both SMR and AT groups.Error bars signify the standard error of the mean (SEM).
Table 1: Mean pre and post values of surgical times andtechnique scores.
ATSMRCprepostprepostprepostOverall time (min)09:2608:1211:0009:3209:1408:58s.d.03:1402:1106:2608:1801:3904:14Task time07:1606:2408:4106:2407:1207:04s.d.02:1801:4705:3603:3701:4303:39Pause time (min)02:1001:4802:1903:0802:0201:54s.d.01:3600:3001:1104:4800:3300:46Suture time (min)03:3302:5704:4503:0003:2003:48s.d.01:5200:5903:3201:4701:3403:24Overall technique (%)82.284.079.683.781.881.6s.d.5.74.17.36.25.64.9Suture technique (%)78.179.475.081.577.877.7s.d.12.78.79.25.310.16.7Alpha-Theta (AT), SMR-Theta (SMR), and control (C) groups andstandard deviations (s.d.)

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