How is cognition in subthalamic nucleus deep brain stimulation Parkinson’s disease patients?

Barboza e Barbosa, Eduarda Naidel; Fichman, Helenice Charchat

doi:10.1590/1980-57642018dn13-040002

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Dementia & Neuropsychologia

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Views & Reviews • Dement. neuropsychol. 13 (4) • Oct-Dec 2019 • https://doi.org/10.1590/1980-57642018dn13-040002 copy

How is cognition in subthalamic nucleus deep brain stimulation Parkinson’s disease patients?

Como é a Cognição em Pacientes com Doença de Parkinson com Estimulação Cerebral Profunda no Núcleo Subtalâmico? Uma Revisão Sistemática

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

The impairments in cognitive functions such as memory, executive function, visuospatial skills and language in Parkinson’s disease (PD) are drawing increasing attention in the current literature. Studies dedicated to investigating the relationship between subthalamic nucleus deep brain stimulation (STN-DBS) and cognitive functioning are contradictory. This systematic review aims to analyze the impact on the cognitive functioning of patients with PD and STN-DBS. Articles published in the 2007-2017 period were retrieved from the Medline/Pubmed databases using PRISMA criteria. The analysis of 27 articles revealed many conflicting results, precluding a consensus on a cognitive functioning standard and hampering the establishment of a neuropsychological profile for PD patients who underwent STN-DBS surgery. Further studies investigating this relationship are needed.

Key words:
Parkinson’s disease; deep brain stimulation; subthalamic nucleus; cognition

Name	Year	Objective	Result
[1] Cilia et al. Brain networks underlining verbal fluency decline during STN-DBS in Parkinson's disease: An ECD-SPECT study.	2007	To assess changes on evaluation after DBS-STN and their possible correlation with the cognitive result related to the frontal lobe.	Patients with STN-DBS improved motor symptoms and reduced medications, but selectively declined in category fluency.
[2] Klempírová et al. Deep brain stimulation of the subthalamic nucleus and cognitive functions in Parkinson's disease.	2007	To evaluate how STN-DBS affects cognitive functions.	Patients treated by STN-DBS tend to worsen in executive functions and logical memory.
[3] Castelli et al. Apathy and verbal fluency in STN-stimulated PD patients.	2007	To evaluate apathy and its relationship with verbal fluency tasks in patients with PD who underwent STN-DBS.	The results suggest that STN-DBS does not necessarily induce apathy, even if individual patients show moderate postoperative worsening of apathetic symptoms.
[4] Heo et al. The effects of bilateral Subthalamic Nucleus Deep Brain Stimulation (STN-DBS) on cognition in Parkinson disease.	2008	To research STN-DBS effects on cognition and mood.	Bilateral STN-DBS did not lead to a significant overall deterioration in cognitive function. However, it has small, long-term detrimental impacts on memory and frontal lobe function.
[5] Witt et al. Neuropsychological and psychiatric changes after deep brain stimulation for Parkinson's disease: a randomised, multicentre study.	2008	To evaluate DBS neuropsychiatric consequences in patients with PD.	STN-DBS does not reduce overall cognition or affectivity, although there is a selective decrease in frontal cognitive functions and an improvement in anxiety in patients after treatment, changes not affecting improvements in quality of life.
[6] Alberts et al. Bilateral subthalamic stimulation impairs cognitive-motor performance in Parkinson's disease patients.	2008	To determine the effects of unilateral and bilateral STN-DBS on upper extremity motor function and cognitive performance under single and double-task conditions in patients with advanced PD.	Significant declines in cognitive and motor function under modest dual-task conditions with bilateral , but not unilateral STN-DBS.
[7] Lueken et al. Impaired performance on the Wisconsin Card Sorting Test under left- when compared to right-sided deep brain stimulation of the subthalamic nucleus in patients with Parkinson's disease.	2008	To evaluate whether changes in performance on executive tasks after chronic DBS may be predominantly associated with stimulation of only one hemisphere.	The STN is not only involved in motor control, but also participates in functions of the cognitive domain. All patients had a significant improvement in motor symptoms postoperatively. Selected aspects of executive task performance were compromised under left - when compared to right-sided stimulation.
[8] Zangaglia et al. Deep brain stimulation and cognitive functions in Parkinson's disease: A three-year controlled study	2009	To evaluate DBS cognitive and behavioral effects.	Verbal fluency worsening after DBS, but relatively safe surgery from a cognitive point of view, since short-term worsening of front-executive functions was transient.
[9] Williams et al. Deep brain stimulation plus best medical therapy versus best medical therapy alone for advanced Parkinson's disease	2010	To evaluate whether surgery and best medical therapy improved self-reported quality of life more than best medical therapy alone	After 1 year, surgery and best medical therapy improved patient self-reported quality of life more than best medical therapy alone in patients with advanced PD, constituting clinically meaningful differences.
[10] York et al. Relationship between neuropsychological outcome and DBS surgical trajectory and electrode location	2009	To observe whether differences in position of electrode and surgical trajectory of DBS can lead to differential neuropsychological outcome.	Cognitive and emotional changes after 6 months of bilateral STN-DBS may be related to surgical trajectory and positioning of electrodes.
[11] Daniels et al. Risk factors for executive dysfunction after subthalamic nucleus stimulation in Parkinson's disease	2010	To evaluate baseline parameters that contribute to deterioration of cognitive functioning after DBS.	Surgical procedure, exact placement of electrode or postoperative management might be more relevant for a decline in executive functioning after STN-DBS, in addition to factors such as age, high levodopa dosages and high scores on the UPDRS III axial subscore in OFF state.
[12] Castelli et al. Neuropsychological changes 1-year after subthalamic DBS in PD patients: A prospective controlled study	2010	To investigate the neuropsychological effect of STN-DBS in patients with advanced PD.	Phonemic verbal fluency declined one year after STN-DBS, while the other cognitive domains did not change significantly. Only 4 subjects had significant cognitive decline 1 year after surgery.
[13] Fasano et al. Motor and cognitive outcome in patients with Parkinson's disease 8 years after subthalamic implants	2010	To assess long-term PD patients undergoing STN-DBS for 8 years: long-term motor outcome of symptoms that improve in the short and medium-term with STN-DBS; identification of predictors of long-term motor outcome; and long-term cognitive and behavioral outcome.	STN-DBS is a safe procedure regarding cognitive and behavioral morbidity over long-term follow-up. However, the global benefit decreases later in the course of the disease due to the progression of PD and to the appearance of stimulant-resistant medications and symptoms.
[14] Van Wouwe et al. Deep Brain Stimulation of the Subthalamic Nucleus Improves Reward-Based Decision-Learning in Parkinson's Disease	2011	To investigate the effect of STN-DBS on reward-based learning in patients diagnosed with PD.	DBS cognitive effects benefited a subset of relatively younger patients with relatively shorter disease duration in daily-life association-learning situations.
[15] Israeli-Korn et al. Subthalamic Nucleus Deep Brain Stimulation Does Not Improve Visuo-Motor Impairment in Parkinsons Disease	2013	To evaluate how STN-DBS affects visuo-motor coordination in patients with PD.	Clinically-measured "low-level" motor function responds to STN-DBS, but cognitive and "high-level" motor functions related to VMC may not respond to STN-DBS.
[16] Kim et al. Initial cognitive dip after subthalamic deep brain stimulation in Parkinson disease	2013	To examine whether the rate of change in global cognitive functioning during the initial 6 months after STN-DBS differed from the mean 6-month change that occurred between 6 and 36 months after surgery.	The decline in global cognitive function was faster in the first 6 months after surgery, compared to a 6-month period between 6 and 36 months post-surgery.
[17] Yágüez et al. Cognitive predictors of cognitive change following bilateral subthalamic nucleus deep brain stimulation in Parkinson's disease	2014	To specifically establish a detailed neuropsychological profile before and after STN-DBS and identify any pre-surgical cognitive profile that can predict cognitive outcomes after stimulation.	Non-dementia patients with mild impairment in both general intellectual functions and list learning, may be at a greater risk of decline in other aspects of verbal memory after STN-DBS.
[18] Asahi et al. Impact of bilateral subthalamic stimulation on motor/cognitive functions in Parkinson's disease	2014	To systemically assess the impact of bilateral STN-DBS on motor and cognitive functions in patients with PD.	Bilateral STN-DBS can significantly improve cognitive function in a given subgroup of patients whose therapeutic effects on motor function are prominent.
[19] Rizzone et al. Long-term outcome of subthalamic nucleus DBS in Parkinson's disease: From the advanced phase towards the late stage of the disease?	2014	To report the results of a long-term follow-up of patients implanted with DBS bilaterally in two centers.	Despite the STN-DBS long-term safety and efficacy in PD, patients functionality worsened over time, mainly for the onset and progression of levodopa-resistant and non-motor symptoms.
[20] Houvenaghel et al. Reduced Verbal Fluency following Subthalamic Deep Brain Stimulation: A Frontal-Related Cognitive Deficit?	2015	To explore the mechanisms underlying DBS.	Cognitive slowdown and apathy seem to have a more decisive influence on the impairment of phonemic verbal fluency after DBS.
[21] Markser et al. Deep brain stimulation and cognitive decline in Parkinson's disease: The predictive value of electroencephalography	2015	To examine whether clinical recordings of EEG can be used to predict cognitive impairment in PD patients undergoing STN-DBS.	The GTE preoperative score can be used to identify patients with PD who are at high risk of developing cognitive impairment after STN-DBS surgery even though their preoperative cognitive status is normal.
[22] Pham et al. Self-Reported Executive Functioning in Everyday Life in Parkinson's disease after Three Months of Subthalamic Deep Brain Stimulation	2015	To compare self-reported daily executive functioning in patients with PD before and after three months of STN-DBS.	Patients with PD showed significant improvement in daily life executive functioning 3 months after surgery. Anxiety indexes decreased significantly while psychiatric symptoms, including apathy, remained unchanged. Only preoperative depressive mood had predictive value for the improvement of executive function and seems to prevent potentially favorable results from the STN-DBS in some aspects of the executive function.
[23] Tang et al. Evidence of improved immediate verbal memory and diminished category fluency following STN-DBS in Chinese-Cantonese patients with idiopathic Parkinson's disease	2015	To investigate neuropsychological effects of STN-DBS in Chinese-Cantonese patients with PD.	A diminished performance of verbal fluency was observed, on the other hand, an improvement in immediate verbal memory, besides anxiety level were demonstrated.
[24] Tremblay et al. The effects of subthalamic deep brain stimulation on metaphor comprehension and language abilities in Parkinson's disease	2015	To determine the effects of STN-DBS on the comprehension of metaphor and linguistic abilities such as lexical and semantic abilities.	STN-DBS had a significant beneficial effect on motor symptoms in PD, but this stimulation had no effect on metaphor comprehension or any other cognitive ability assessed in this study.
[25] Krishnan et al. The decade after subthalamic stimulation in advanced Parkinson's disease: A balancing act.	2016	To examine the long-term quality of life, motor and cognitive outcomes of bilateral subthalamic nucleus STN DBS and the pre-DBS factors that predict sustained motor benefits at or beyond 7 years from surgery.	Improvements in severity of motor fluctuations, stiffness, and tremor are the most enduring STN-DBS benefits, lasting a decade. However, these are offset by the higher levodopa requirement, and worsening cognitive and axial functions, bradykinesia and dyskinesias.
[26] Vonberg et al. Fabian. Deep Brain Stimulation of the Subthalamic Nucleus Improves Lexical Switching in Parkinson's disease Patients	2016	To outline the nature of verbal fluency dysfunction.	The STN-DBS group task performance was lower than that of healthy controls. In addition to affecting motor symptoms, surgery seems to influence the dynamics of cognitive procedures.
[27] Ventre-Dominey et al. Distinct effects of dopamine vs STN stimulation therapies in associative learning and retention in Parkinson disease	2016	To investigate and compare results of treatment with dopamine versus DBS in the ability of PD patients to acquire and maintain over the successive days their performance in visual working memory	While STN-DBS patients demonstrate more accurate and faster responses in the ON stage than in the OFF stage, regardless of the day of testing, patients using dopamine replacement therapy had more accurate and faster ON response compared to OFF during the first day of learning and then maintained or even improved their performance on the second day after consolidation in both the OFF and ON stages.

Domain	STN-DBS cognitive effects	Articles by
Global Cognitive Functioning/Reasoning	↑ (MMSE)	Lueken et al., 2008; Wouwe et al., 2011
	↑ (DemTect)	Markser et al., 2015
	↑ Addenbrooke	Krishnan et al., 2016
	= (MDRS)	Klempírova et al., 2007; Witt et al., 2008; Daniels et al., 2010
	= (MMSE)	Cilia et al., 2007; Heo et al., 2008; Zanglagia et al., 2009; Israeli-Korn et al., 2013; Asahi et al., 2014
	= (Repeatable Battery For The Assessment of Neuropsychological Status)	Asahi et al., 2014
	= (Wechsler Adult Intelligence Scale)	Asahi et al., 2014
	= (Japanese Adult Reading Test)	Asahi et al., 2014
	= abstract reasoning (Raven Colour Matrices)	Castelli et al., 2007; Castelli et al., 2010; Rizzone et al., 2014
	= (MoCA^* * Indicates different types of versions; )	Tang et al., 2015; Tremblay et al., 2015
	↓ MMSE	York et al., 2009; Kim et al., 2013; Markser et al., 2015; Krishnan et al., 2016
	↓ MDRS	Williams et al., 2010; York et al., 2009; Markser et al., 2015
	↓ Raven	Fasano et al., 2010
Memory	↑ episodic verbal memory (RAVLT^* * Indicates different types of versions; immediate recall)	Tang et al., 2015
	= verbal memory (RKMB)	Heo et al., 2008
	= verbal memory (Benton)	Tang et al., 2015
	= verbal memory (RAVLT^* * Indicates different types of versions; )	Witt et al., 2008; Daniels et al., 2010
	= verbal memory (Bi-syllabic Words Repetition test)	Castelli et al., 2007; Castelli et al., 2010
	= short-term spatial memory (Corsi's Block Tapping Test)	Castelli et al., 2007; Castelli et al., 2010
	= verbal learning (WMS Paired Associate Learning)	Castelli et al., 2007; Castelli et al., 2010
	= memory (Verbal and Digits Span)	Zanglagia et al., 2009
	= memory (MDRS)	Witt et al., 2008
	= memory recognition (verbal and visual Recognition Test)	Yagüez et al., 2014
	↓ immediate, delayed and recognition memory (WMS logical memory)	Klempírova et al., 2007
	↓ delayed memory (RBANS)	Asahi et al., 2014
	↓ episodic verbal memory (RAVLT^* * Indicates different types of versions; immediate and delayed recall)	Fasano et al., 2010; Rizzone et al., 2014
	↓ verbal memory recall (BMPI immediate and delayed memory and learning)	Yagüez et al., 2014
	↓ verbal recognition memory and delayed memory (RKMB)	Heo et al., 2008
Executive Functions	↑ (WCST right categories, right answers, errors nº and non-perseverative errors)	Lueken et al., 2008
	↑ (Stroop effect)	Houvenaghel et al., 2015
	↑ executive functioning (BRIEF-A)	Pham et al., 2015
	↑ visuospatial working memory (working memory tasks)	Ventre-Dominey et al., 2016
	↑ stimulus-action-reward association (Haruno and Kawato task)	Wouwe et al., 2011
	= behavior regulation (BRIEF-A)	Pham et al., 2015
	= semantic verbal fluency (tasks)	Castelli et al., 2007; Castelli et al., 2010; Tremblay et al., 2015
	= phonemic verbal fluency (tasks)	Cilia et al., 2007
	= cognitive flexibility (alternate verbal fluency tasks)	Tremblay et al., 2015
	= cognitive flexibility (Trail Making Test B)	Castelli et al., 2007
	= abstract concept development and cognitive flexibility (WCST^* * Indicates different types of versions; )	Cilia et al., 2007; Castelli et al., 2007; Castelli et al., 2010; Houvenaghel et al., 2015
	= abstract concept development (metaphor comprehension)	Tremblay et al., 2015
	= response initiation and response inhibition (Hayling Sentence Completion Test)	Yagüez et al., 2014
	= working memory (Digit Span)	Daniels et al., 2010; Tang et al., 2015
	= (Stroop effect)	Tang et al., 2015
	= executive functions (Frontal Assessment Battery)	Israeli-Korn et al., 2013
	= processing of outcome errors (Haruno and Kawato task)	Wouwe et al., 2011
	= working memory (n-back DBS STN unilateral task)	Alberts et al., 2008
	↓ logical executive functions (WCST^* * Indicates different types of versions; and Raven)	Zanglagia et al., 2009
	↓ semantic verbal fluency (category task)	Cilia et al., 2007; Witt et al., 2008; York et al., 2009; Daniels et al., 2010; Houvenaghel et al., 2015; Tang et al., 2015; Vonberg et al., 2016
	↓ phonemic verbal fluency (initial recall tasks)	Castelli et al., 2007; Klempírova et al., 2007; Witt et al., 2008; Zanglagia et al., 2009; York et al., 2009; Daniels et al., 2010; Castelli et al., 2010; Fasano et al., 2010; Kim et al., 2013; Yagüez et al., 2014; Houvenaghel et al., 2015; Vonberg et al., 2016
	↓ phonemic and semantic verbal fluency (Delis-Kaplan executive function system)	Williams et al., 2010
	↓ verbal fluency (MDRS Initiative/Perseveration)	Witt et al., 2008
	↓ working memory (Digit Span)	Witt et al., 2008
	↓ cognitive flexibility (WCST^* * Indicates different types of versions; perseverative responses and errors)	Heo et al., 2008; Lueken et al., 2008; Fasano et al., 2010; Rizzone et al., 2014
	↓ (Stroop effect)	Klempírova et al., 2007; Heo et al., 2008; Kim et al., 2013
	↓ interference (Trail Making Test B form)	Klempírova et al., 2007; Kim et al., 2013; Rizzone et al., 2014; Houvenaghel et al., 2015
	↓ planning skills (London Tower)	Klempírova et al., 2007
	↓ working memory (n-back DBS STN bilateral tasks	Alberts et al., 2008
Attention	= (Trail Making Test A and B forms)	Heo et al., 2008; Castelli et al., 2010; Houvenaghel et al., 2015
	= (Stroop)	Witt et al., 2008; Daniels et al., 2010; Tang et al., 2015
	= (MDRS attention)	Witt et al., 2008;
	= (WCST^* * Indicates different types of versions; )	Castelli et al., 2010
	= (Digit Span)	Tang et al., 2015
	↓ (WCST^* * Indicates different types of versions; )	Rizzone et al., 2014
	↓ (RBANS)	Asahi et al., 2014
Perception	= (Visual Object and Space Perception Battery Object Decision task)	Yagüez et al., 2014
Perception	= (Visual Object and Space Perception Incomplete Letters task)	Yagüez et al., 2014
Language	↑ lexical changing and word production	Vonberg et al., 2016
	= (Boston Naming Test^* * Indicates different types of versions; )	Heo et al., 2008; Tang et al., 2015
	= (Graded Naming Test)	Yagüez et al., 2014
	= (lexical decision task and words association task)	Tremblay et al., 2015
	↓ word production	Cilia et al., 2007
	↓ Vocabulary (WASI)	Williams et al., 2010
	↓ fluency tasks (Phonemic and Semantic Verbal Fluency Test)	Rizzone et al., 2014
Visuoconstructive and visuospatial skills	= (MDRS)	Witt et al., 2008
	= visuospatial reasoning (Raven)	Cilia et al., 2007
	= (Benton)	Witt et al., 2008
	= visuospatial organization capacity (Hooper Test)	Tang et al., 2015
	↓ (Corsi's Block Tapping Test forward and backward)	Rizzone et al., 2014
	↓ visuoconstructive skills (RBANS)	Asahi et al., 2014
Motor and sensory coordination	↑ fine motor dexterity and speed (Purdue Pegboard Test)	Wouwe et al., 2011
	= motor and sensory coordination (Purdue Pegboard Test)	Heo et al., 2008
	= (Trail Making Test A)	Klempírova et al., 2007
	= (Stroop Test)	Klempírova et al., 2007

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[1] Eduarda Naidel. Pontifical Catholic University - Rua Marquês de São Vicente, 225 / Gávea - 22451-900 Rio de Janeiro RJ - Brazil. Email: psienbb@gmail.com.