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Article: Doing better than your best: loud auditory stimulation yields improvements in maximal voluntary force

Anzak, Anam / Tan, Huiling / Pogosyan, Alek / Brown, Peter

Experimental brain research. 2011 Jan., v. 208, no. 2

2011

Abstract: Could task performance be constrained by our ability to fully engage necessary neural processing through effort of will? The StartReact phenomenon suggests that this might be the case, as voluntary reaction times are substantially reduced by loud sounds. ...

Abstract	Could task performance be constrained by our ability to fully engage necessary neural processing through effort of will? The StartReact phenomenon suggests that this might be the case, as voluntary reaction times are substantially reduced by loud sounds. Here, we show that loud auditory stimulation can also be associated with an improvement in the force and speed of force development when 18 healthy subjects are repeatedly asked to make a maximal grip as fast and as strongly as possible. Peak grip force was increased by 7.2 ± 1.4% (SEM) (P < 0.0001), and the rate of force development was increased by 17.6 ± 2.0% (P ≪ 0.00001), when imperative visual cues were accompanied by a loud auditory stimulus rather than delivered alone. This implies that loud auditory stimuli may allow motor pathways to be optimised beyond what can be achieved by effort of will alone.
Language	English
Dates of publication	2011-01
Size	p. 237-243.
Publisher	Springer-Verlag
Publishing place	Berlin/Heidelberg
Document type	Article
ZDB-ID	1201-4
ISSN	1432-1106 ; 0014-4819
ISSN (online)	1432-1106
ISSN	0014-4819
DOI	10.1007/s00221-010-2474-1
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Excessive neural synchrony in Machado-Joseph disease responsive to subthalamic nucleus stimulation.

Anzak, Anam / Little, Simon / Hulse, Natasha / Andrews, Thomasin / Brown, Peter / Samuel, Michael / Ashkan, Keyoumars

Movement disorders : official journal of the Movement Disorder Society

2015 Volume 30, Issue 3, Page(s) 437–438

MeSH term(s)	Brain/physiopathology ; Deep Brain Stimulation/methods ; Evoked Potentials/physiology ; Humans ; Machado-Joseph Disease/pathology ; Machado-Joseph Disease/therapy ; Male ; Middle Aged ; Subthalamic Nucleus/physiology
Language	English
Publishing date	2015-02-17
Publishing country	United States
Document type	Case Reports ; Letter ; Video-Audio Media
ZDB-ID	607633-6
ISSN	1531-8257 ; 0885-3185
ISSN (online)	1531-8257
ISSN	0885-3185
DOI	10.1002/mds.26173
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Article ; Online: Doing better than your best: loud auditory stimulation yields improvements in maximal voluntary force.

Anzak, Anam / Tan, Huiling / Pogosyan, Alek / Brown, Peter

Experimental brain research

2010 Volume 208, Issue 2, Page(s) 237–243

Abstract	Could task performance be constrained by our ability to fully engage necessary neural processing through effort of will? The StartReact phenomenon suggests that this might be the case, as voluntary reaction times are substantially reduced by loud sounds. Here, we show that loud auditory stimulation can also be associated with an improvement in the force and speed of force development when 18 healthy subjects are repeatedly asked to make a maximal grip as fast and as strongly as possible. Peak grip force was increased by 7.2 ± 1.4% (SEM) (P < 0.0001), and the rate of force development was increased by 17.6 ± 2.0% (P < 0.00001), when imperative visual cues were accompanied by a loud auditory stimulus rather than delivered alone. This implies that loud auditory stimuli may allow motor pathways to be optimised beyond what can be achieved by effort of will alone.
MeSH term(s)	Acoustic Stimulation ; Adult ; Cues ; Female ; Hand Strength/physiology ; Humans ; Male ; Muscle Contraction/physiology ; Muscle, Skeletal/physiology ; Photic Stimulation/methods ; Psychoacoustics ; Young Adult
Language	English
Publishing date	2010-11-10
Publishing country	Germany
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1201-4
ISSN	1432-1106 ; 0014-4819
ISSN (online)	1432-1106
ISSN	0014-4819
DOI	10.1007/s00221-010-2474-1
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Article ; Online: Bilateral functional connectivity of the basal ganglia in patients with Parkinson's disease and its modulation by dopaminergic treatment.

Little, Simon / Tan, Huiling / Anzak, Anam / Pogosyan, Alek / Kühn, Andrea / Brown, Peter

PloS one

2013 Volume 8, Issue 12, Page(s) e82762

Abstract: Parkinson's disease is characterised by excessive subcortical beta oscillations. However, little is known about the functional connectivity of the two basal ganglia across hemispheres and specifically the role beta plays in this. We recorded local field ... ...

Abstract	Parkinson's disease is characterised by excessive subcortical beta oscillations. However, little is known about the functional connectivity of the two basal ganglia across hemispheres and specifically the role beta plays in this. We recorded local field potentials from the subthalamic nucleus bilaterally in 23 subjects with Parkinson's disease at rest, on and off medication. We found suppression of low beta power in response to levodopa (t22 = -4.4, p<0.001). There was significant coherence between the two sides in the beta range in 19 of the subjects. Coherence was selectively attenuated in the low beta range following levodopa (t22 = -2.7; p = 0.01). We also separately analysed amplitude co-modulation and phase synchronisation in the beta band and found significant amplitude co-modulation and phase locking values in 17 and 16 subjects respectively, off medication. There was a dissociable effect of levodopa on these measures, with a significant suppression only in low beta phase locking value (t22 = -2.8, p = 0.01) and not amplitude co-modulation. The absolute mean values of amplitude co-modulation (0.40 ± 0.03) and phase synchronisation (0.29 ± 0.02) off medication were, however, relatively low, suggesting that the two basal ganglia networks may have to be approached separately with independent sensing and stimulation during adaptive deep brain stimulation. In addition, our findings highlight the functional distinction between the lower and upper beta frequency ranges and between amplitude co-modulation and phase synchronization across subthalamic nuclei.
MeSH term(s)	Action Potentials/drug effects ; Basal Ganglia/drug effects ; Basal Ganglia/physiopathology ; Beta Rhythm/drug effects ; Electroencephalography Phase Synchronization/drug effects ; Humans ; Levodopa/pharmacology ; Levodopa/therapeutic use ; Middle Aged ; Nerve Net/drug effects ; Nerve Net/physiopathology ; Parkinson Disease/drug therapy ; Parkinson Disease/physiopathology ; Subthalamic Nucleus/drug effects ; Subthalamic Nucleus/physiopathology
Chemical Substances	Levodopa (46627O600J)
Language	English
Publishing date	2013-12-20
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2267670-3
ISSN	1932-6203 ; 1932-6203
ISSN (online)	1932-6203
ISSN	1932-6203
DOI	10.1371/journal.pone.0082762
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Article ; Online: Improvements in rate of development and magnitude of force with intense auditory stimuli in patients with Parkinson's disease.

Anzak, Anam / Tan, Huiling / Pogosyan, Alek / Djamshidian, Atbin / Ling, Helen / Lees, Andrew / Brown, Peter

The European journal of neuroscience

2011 Volume 34, Issue 1, Page(s) 124–132

Abstract: Patients with Parkinson's disease can show brief but dramatic normalization of motor activity in highly arousing situations, a phenomenon often termed paradoxical kinesis. We sought to mimic this in a controlled experimental environment. Nine patients ... ...

Abstract	Patients with Parkinson's disease can show brief but dramatic normalization of motor activity in highly arousing situations, a phenomenon often termed paradoxical kinesis. We sought to mimic this in a controlled experimental environment. Nine patients with Parkinson's disease and nine age-matched healthy controls were asked to grip a force dynamometer as quickly and strongly as possible in response to a visual cue. A loud (96 dB) auditory stimulus was delivered at the same time as the visual cue in ~50% of randomly selected trials. In patients with Parkinson's disease, the experiment was conducted after overnight withdrawal of antiparkinsonian drugs and again 1 h after patients had taken their usual morning medication. Patients showed improvements in the peak rate of force development and the magnitude of force developed when loud auditory stimuli accompanied visual cues. Equally, they showed improvements in the times taken to reach the peak rate of force development and their maximal force. The paradoxical facilitatory effect of sound was similar whether patients were off or on their usual antiparkinsonian medication, and could be reproduced in age-matched healthy controls. We conclude that motor improvement induced by loud auditory stimuli in Parkinson's disease is related to a physiological phenomenon which survives both with and after withdrawal of antiparkinsonian medication. The potential independence of the mediating pathways from the dopaminergic system provides impetus for further investigation as it may yield a novel nondopaminergic target for therapeutic manipulation in Parkinson's disease.
MeSH term(s)	Acoustic Stimulation ; Aged ; Antiparkinson Agents/therapeutic use ; Cues ; Hand Strength/physiology ; Humans ; Male ; Middle Aged ; Motor Activity/physiology ; Neuropsychological Tests ; Parkinson Disease/drug therapy ; Parkinson Disease/physiopathology ; Psychomotor Performance/physiology ; Reaction Time
Chemical Substances	Antiparkinson Agents
Language	English
Publishing date	2011-06-06
Publishing country	France
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	645180-9
ISSN	1460-9568 ; 0953-816X
ISSN (online)	1460-9568
ISSN	0953-816X
DOI	10.1111/j.1460-9568.2011.07735.x
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Article ; Online: Subthalamic nucleus gamma oscillations mediate a switch from automatic to controlled processing: a study of random number generation in Parkinson's disease.

Anzak, Anam / Gaynor, Louise / Beigi, Mazda / Foltynie, Thomas / Limousin, Patricia / Zrinzo, Ludvic / Brown, Peter / Jahanshahi, Marjan

NeuroImage

2012 Volume 64, Page(s) 284–289

Abstract: In paced random number generation (RNG) participants are asked to generate numbers between 1 and 9 in a random fashion, in synchrony with a pacing stimulus. Successful task performance can be achieved through control of the main biases known to exist in ... ...

Abstract	In paced random number generation (RNG) participants are asked to generate numbers between 1 and 9 in a random fashion, in synchrony with a pacing stimulus. Successful task performance can be achieved through control of the main biases known to exist in human RNG compared to a computer generated series: seriation, cycling through a set of available numbers, and repetition avoidance. A role in response inhibition and switching from automatic to controlled processing has previously been ascribed to the subthalamic nucleus (STN). We sought evidence of frequency-specific changes in STN oscillatory activity which could be directly related to use of such strategies during RNG. Local field potentials (LFPs) were recorded from depth electrodes implanted in the STN of 7 patients (14 sides) with Parkinson's disease (PD), when patients were on dopaminergic medication. Patients were instructed to (1) generate a series of 100 numbers between 1 and 9 in a random fashion, and (2) undertake a control serial counting task, both in synchrony with a 0.5 Hz pacing stimulus. Significant increases in LFP power (p ≤ 0.05) across a narrow gamma frequency band (45-60 Hz) during RNG, compared to the control counting task, were observed. Further, the number of 'repeated pairs' (a decline in which reflects repetition avoidance bias in human RNG) was positively correlated with these gamma increases. We therefore suggest that STN gamma activity is relevant for controlled processing, in particular the active selection and repetition of the same number on successive trials. These results are consistent with a frequency-specific role of the STN in executive processes such as suppression of habitual responses and 'switching-on' of more controlled processing strategies.
MeSH term(s)	Biological Clocks ; Brain Mapping ; Brain Waves ; Cognition ; Feedback, Physiological ; Female ; Humans ; Inhibition, Psychological ; Male ; Mathematics ; Middle Aged ; Neuronal Plasticity ; Parkinson Disease/physiopathology ; Subthalamic Nucleus/physiopathology
Language	English
Publishing date	2012-08-30
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1147767-2
ISSN	1095-9572 ; 1053-8119
ISSN (online)	1095-9572
ISSN	1053-8119
DOI	10.1016/j.neuroimage.2012.08.068
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Article ; Online: Subcortical evoked activity and motor enhancement in Parkinson's disease.

Anzak, Anam / Tan, Huiling / Pogosyan, Alek / Khan, Sadaquate / Javed, Shazia / Gill, Steven S / Ashkan, Keyoumars / Akram, Harith / Foltynie, Thomas / Limousin, Patricia / Zrinzo, Ludvic / Green, Alexander L / Aziz, Tipu / Brown, Peter

Experimental neurology

2015 Volume 277, Page(s) 19–26

Abstract: Enhancements in motor performance have been demonstrated in response to intense stimuli both in healthy subjects and in the form of 'paradoxical kinesis' in patients with Parkinson's disease. Here we identify a mid-latency evoked potential in local field ...

Abstract	Enhancements in motor performance have been demonstrated in response to intense stimuli both in healthy subjects and in the form of 'paradoxical kinesis' in patients with Parkinson's disease. Here we identify a mid-latency evoked potential in local field potential recordings from the region of the subthalamic nucleus, which scales in amplitude with both the intensity of the stimulus delivered and corresponding enhancements in biomechanical measures of maximal handgrips, independent of the dopaminergic state of our subjects with Parkinson's disease. Recordings of a similar evoked potential in the related pedunculopontine nucleus - a key component of the reticular activating system - provide support for this neural signature in the subthalmic nucleus being a novel correlate of ascending arousal, propagated from the reticular activating system to exert an 'energizing' influence on motor circuitry. Future manipulation of this system linking arousal and motor performance may provide a novel approach for the non-dopaminergic enhancement of motor performance in patients with hypokinetic disorders such as Parkinson's disease.
MeSH term(s)	Acoustic Stimulation ; Adult ; Aged ; Antiparkinson Agents/therapeutic use ; Cues ; Deep Brain Stimulation/methods ; Electromyography ; Evoked Potentials/drug effects ; Evoked Potentials/physiology ; Female ; Hand Strength/physiology ; Humans ; Levodopa/therapeutic use ; Male ; Middle Aged ; Motor Activity/drug effects ; Motor Activity/physiology ; Parkinson Disease/physiopathology ; Parkinson Disease/therapy ; Photic Stimulation ; Psychoacoustics ; Reaction Time/drug effects ; Reaction Time/physiology ; Subthalamic Nucleus/physiology
Chemical Substances	Antiparkinson Agents ; Levodopa (46627O600J)
Language	English
Publishing date	2015-12-11
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	207148-4
ISSN	1090-2430 ; 0014-4886
ISSN (online)	1090-2430
ISSN	0014-4886
DOI	10.1016/j.expneurol.2015.12.004
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Article ; Online: A gamma band specific role of the subthalamic nucleus in switching during verbal fluency tasks in Parkinson's disease.

Anzak, Anam / Gaynor, Louise / Beigi, Mazda / Limousin, Patricia / Hariz, Marwan / Zrinzo, Ludvic / Foltynie, Thomas / Brown, Peter / Jahanshahi, Marjan

Experimental neurology

2011 Volume 232, Issue 2, Page(s) 136–142

Abstract: Objective: Decline in verbal fluency is the most consistent and persistent cognitive impairment documented after deep brain stimulation of the subthalamic nucleus in Parkinson's disease. The mechanisms of this deficit are unclear. We aimed to identify ... ...

Abstract	Objective: Decline in verbal fluency is the most consistent and persistent cognitive impairment documented after deep brain stimulation of the subthalamic nucleus in Parkinson's disease. The mechanisms of this deficit are unclear. We aimed to identify and characterise verbal fluency related processing within the subthalamic nucleus through analysis of local field potentials. Methods: Local field potentials were recorded from deep brain stimulation electrodes implanted in the subthalamic nuclei of 8 patients (16 sides) with Parkinson's disease, when patients were on medication. Patients performed phonemic and semantic verbal fluency tasks and a control word repetition task to control for the motor output involved in response generation. Results: Significant increases in local field potential Power (p ≤ 0.05) were seen across a broad gamma frequency band (30-95 Hz) during both verbal fluency tasks, after controlling for motor output. Increases in gamma local field potential Power of +7.5% ± 2.3% (SEM) in the semantic fluency task and +6.9% ± 2.0% in the phonemic fluency task were derived when averaging across all electrode contact pairs. Gamma changes recorded from contacts lying in the left hemisphere (dominant in verbal fluency) correlated with average number of correct responses generated (r=0.81 p=0.015) and measures of 'switching' (r=0.79 p=0.020) particularly strongly in the semantic fluency task. Interpretation: Frequency specific power changes observed during task performance are consistent with involvement of the subthalamic nucleus in switching during verbal fluency. Antagonism of such task-related activity with high frequency stimulation of this nucleus may explain the impairments reported.
MeSH term(s)	Deep Brain Stimulation/adverse effects ; Executive Function/physiology ; Female ; Frontal Lobe/cytology ; Frontal Lobe/physiology ; Humans ; Language Tests ; Male ; Middle Aged ; Neural Pathways/cytology ; Neural Pathways/physiology ; Parkinson Disease/physiopathology ; Parkinson Disease/therapy ; Phonetics ; Semantics ; Speech Disorders/etiology ; Speech Disorders/physiopathology ; Subthalamic Nucleus/cytology ; Subthalamic Nucleus/physiopathology
Language	English
Publishing date	2011-08-18
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	207148-4
ISSN	1090-2430 ; 0014-4886
ISSN (online)	1090-2430
ISSN	0014-4886
DOI	10.1016/j.expneurol.2011.07.010
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Article ; Online: Complementary roles of different oscillatory activities in the subthalamic nucleus in coding motor effort in Parkinsonism.

Tan, Huiling / Pogosyan, Alek / Anzak, Anam / Ashkan, Keyoumars / Bogdanovic, Marko / Green, Alexander L / Aziz, Tipu / Foltynie, Thomas / Limousin, Patricia / Zrinzo, Ludvic / Brown, Peter

Experimental neurology

2013 Volume 248, Page(s) 187–195

Abstract: The basal ganglia may play an important role in the control of motor scaling or effort. Recently local field potential (LFP) recordings from patients with deep brain stimulation electrodes in the basal ganglia have suggested that local increases in the ... ...

Abstract	The basal ganglia may play an important role in the control of motor scaling or effort. Recently local field potential (LFP) recordings from patients with deep brain stimulation electrodes in the basal ganglia have suggested that local increases in the synchronisation of neurons in the gamma frequency band may correlate with force or effort. Whether this feature uniquely codes for effort and whether such a coding mechanism holds true over a range of efforts is unclear. Here we investigated the relationship between frequency-specific oscillatory activities in the subthalamic nucleus (STN) and manual grips made with different efforts. The latter were self-rated using the 10 level Borg scale ranging from 0 (no effort) to 10 (maximal effort). STN LFP activities were recorded in patients with Parkinson's Disease (PD) who had undergone functional surgery. Patients were studied while motor performance was improved by dopaminergic medication. In line with previous studies we observed power increase in the theta/alpha band (4-12 Hz), power suppression in the beta band (13-30 Hz) and power increase in the gamma band (55-90 Hz) and high frequency band (101-375 Hz) during voluntary grips. Beta suppression deepened, and then reached a floor level as effort increased. Conversely, gamma and high frequency power increases were enhanced during grips made with greater effort. Multiple regression models incorporating the four different spectral changes confirmed that the modulation of power in the beta band was the only independent predictor of effort during grips made with efforts rated <5. In contrast, increases in gamma band activity were the only independent predictor of effort during grips made with efforts ≥5. Accordingly, the difference between power changes in the gamma and beta bands correlated with effort across all effort levels. These findings suggest complementary roles for changes in beta and gamma band activities in the STN in motor effort coding. The latter function is thought to be impaired in untreated PD where task-related reactivity in these two bands is deficient.
MeSH term(s)	Aged ; Alpha Rhythm/physiology ; Antiparkinson Agents/therapeutic use ; Beta Rhythm/physiology ; Deep Brain Stimulation ; Electroencephalography ; Female ; Hand Strength/physiology ; Humans ; Levodopa/therapeutic use ; Male ; Middle Aged ; Neurons/physiology ; Parkinson Disease/drug therapy ; Parkinson Disease/physiopathology ; Parkinson Disease/therapy ; Subthalamic Nucleus/physiopathology
Chemical Substances	Antiparkinson Agents ; Levodopa (46627O600J)
Language	English
Publishing date	2013-06-15
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	207148-4
ISSN	1090-2430 ; 0014-4886
ISSN (online)	1090-2430
ISSN	0014-4886
DOI	10.1016/j.expneurol.2013.06.010
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Article ; Online: Subthalamic nucleus activity optimizes maximal effort motor responses in Parkinson's disease.

Anzak, Anam / Tan, Huiling / Pogosyan, Alek / Foltynie, Thomas / Limousin, Patricia / Zrinzo, Ludvic / Hariz, Marwan / Ashkan, Keyoumars / Bogdanovic, Marko / Green, Alexander L / Aziz, Tipu / Brown, Peter

Brain : a journal of neurology

2012 Volume 135, Issue Pt 9, Page(s) 2766–2778

Abstract: The neural substrates that enable individuals to achieve their fastest and strongest motor responses have long been enigmatic. Importantly, characterization of such activities may inform novel therapeutic strategies for patients with hypokinetic ... ...

Abstract	The neural substrates that enable individuals to achieve their fastest and strongest motor responses have long been enigmatic. Importantly, characterization of such activities may inform novel therapeutic strategies for patients with hypokinetic disorders, such as Parkinson's disease. Here, we ask whether the basal ganglia may play an important role, not only in the attainment of maximal motor responses under standard conditions but also in the setting of the performance enhancements known to be engendered by delivery of intense stimuli. To this end, we recorded local field potentials from deep brain stimulation electrodes implanted bilaterally in the subthalamic nuclei of 10 patients with Parkinson's disease, as they executed their fastest and strongest handgrips in response to a visual cue, which was accompanied by a brief 96-dB auditory tone on random trials. We identified a striking correlation between both theta/alpha (5-12 Hz) and high-gamma/high-frequency (55-375 Hz) subthalamic nucleus activity and force measures, which explained close to 70% of interindividual variance in maximal motor responses to the visual cue alone, when patients were ON their usual dopaminergic medication. Loud auditory stimuli were found to enhance reaction time and peak rate of development of force still further, independent of whether patients were ON or OFF l-DOPA, and were associated with increases in subthalamic nucleus power over a broad gamma range. However, the contribution of this broad gamma activity to the performance enhancements observed was only modest (≤13%). The results implicate frequency-specific subthalamic nucleus activities as substantial factors in optimizing an individual's peak motor responses at maximal effort of will, but much less so in the performance increments engendered by intense auditory stimuli.
MeSH term(s)	Acoustic Stimulation ; Adult ; Aged ; Deep Brain Stimulation ; Electrodes, Implanted ; Female ; Hand Strength/physiology ; Humans ; Male ; Middle Aged ; Motor Activity/physiology ; Parkinson Disease/physiopathology ; Parkinson Disease/therapy ; Subthalamic Nucleus/physiopathology
Language	English
Publishing date	2012-08-01
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80072-7
ISSN	1460-2156 ; 0006-8950
ISSN (online)	1460-2156
ISSN	0006-8950
DOI	10.1093/brain/aws183
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