The Subthalamic Microlesion Story in Parkinson's Disease: Electrode Insertion-Related Motor Improvement with Relative Cortico-Subcortical Hypoactivation in fMRI

Jech, Robert; Mueller, Karsten; Urgošík, Dušan; Sieger, Tomáš; Holiga, Štefan; Růžička, Filip; Dušek, Petr; Havránková, Petra; Vymazal, Josef; Růžička, Evžen

doi:10.1371/journal.pone.0049056

Cited by 56 publications

(61 citation statements)

References 99 publications

(151 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…An electrode penetration to the STN has an impact on the EM parameters as well. It causes a transitory microlesion [40] prolonging the latency of reflexive saccades [41] which are already prolonged due to Parkinson’s disease [42]. Unlike microlesion, deep brain stimulation has an opposite effect on the STN as the latency of visually initiated reflexive saccades become shorter and normalized [41], [43], [44] while their gain is growing [45].…”

Section: Discussionmentioning

confidence: 99%

Basal Ganglia Neuronal Activity during Scanning Eye Movements in Parkinson’s Disease

et al. 2013

Self Cite

View full text Add to dashboard Cite

The oculomotor role of the basal ganglia has been supported by extensive evidence, although their role in scanning eye movements is poorly understood. Nineteen Parkinsońs disease patients, which underwent implantation of deep brain stimulation electrodes, were investigated with simultaneous intraoperative microelectrode recordings and single channel electrooculography in a scanning eye movement task by viewing a series of colored pictures selected from the International Affective Picture System. Four patients additionally underwent a visually guided saccade task. Microelectrode recordings were analyzed selectively from the subthalamic nucleus, substantia nigra pars reticulata and from the globus pallidus by the WaveClus program which allowed for detection and sorting of individual neurons. The relationship between neuronal firing rate and eye movements was studied by crosscorrelation analysis. Out of 183 neurons that were detected, 130 were found in the subthalamic nucleus, 30 in the substantia nigra and 23 in the globus pallidus. Twenty percent of the neurons in each of these structures showed eye movement-related activity. Neurons related to scanning eye movements were mostly unrelated to the visually guided saccades. We conclude that a relatively large number of basal ganglia neurons are involved in eye motion control. Surprisingly, neurons related to scanning eye movements differed from neurons activated during saccades suggesting functional specialization and segregation of both systems for eye movement control.

show abstract

Section: Discussionmentioning

confidence: 99%

Basal Ganglia Neuronal Activity during Scanning Eye Movements in Parkinson’s Disease

et al. 2013

Self Cite

View full text Add to dashboard Cite

show abstract

“…A fair number of functional imaging studies examining motor circuitry of PD [14]–[18] embodied the UPDRS-III in statistical analyses to reveal correlations between the clinical presentation of the disease and the blood-oxygen level dependent (BOLD) signal amplitude (Table 1). Correspondingly and noticeably, the UPDRS-III ‘in’ approach presented here identified a strong relationship between the total UPDRS-III score, midline subscore and BOLD responses in the basal ganglia regardless of the treatment condition.…”

Section: Discussionmentioning

confidence: 99%

“…This way we were able to equalize particular clinical symptoms between the investigated patients intra/inter-individually, thus ‘simulated homogeneity’ with respect to a certain symptom. To our knowledge, this and our previous fMRI study [18] are the only studies which considered using UPDRS-III in the analyses to account for the symptomatic variability of PD. Here, akinesia and rigidity were demonstrated as primarily responsive to levodopa treatment, as documented by the scores (Figure 2, bottom bar-plot).…”

Section: Discussionmentioning

confidence: 99%

Motor Matters: Tackling Heterogeneity of Parkinson’s Disease in Functional MRI Studies

et al. 2013

Self Cite

View full text Add to dashboard Cite

To tackle the heterogeneity of Parkinson’s disease symptoms, most functional imaging studies tend to select a uniform group of subjects. We hypothesize that more profound considerations are needed to account for intra/inter-subject clinical variability and possibly for differing pathophysiological processes. Twelve patients were investigated using functional magnetic resonance imaging during visually-guided finger tapping. To account for disease heterogeneity, the motor score and individual symptom scores from the Unified Parkinson’s Disease Rating Scale (UPDRS-III) were utilized in the group-level model using two approaches either as the explanatory variable or as the effect of interest. Employment of the UPDRS-III score and symptom scores was systematically tested on the resulting group response to the levodopa challenge, which further accentuated the diversity of the diseased state of participants. Statistics revealed a bilateral group response to levodopa in the basal ganglia. Interestingly, systematic incorporation of individual motor aspects of the disease in the modelling amended the resulting activity patterns conspicuously, evidencing a manifold amount of explained variability by the particular score. In conclusion, the severity of clinical symptoms expressed in the UPDRS-III scores should be considered in the analysis to attain unbiased statistics, draw reliable conclusions and allow for comparisons between research groups studying Parkinson’s disease using functional magnetic resonance imaging.

show abstract

“…A subjective rating of the emotional content of the pictures was not elicited during the surgery, to avoid possible contamination of neuronal activity by voluntary movements during the rating process. Emotional valence and arousal ratings for each picture in the task were assessed before the initiation of chronic DBS at 4-5 wk after implantation, with a sufficient delay after surgery to allow cessation of any transitory microlesion effect related to penetration of the DBS electrode (84). No patient had any change in medication regimen after the surgery.…”

Section: Methodsmentioning

confidence: 99%

Distinct populations of neurons respond to emotional valence and arousal in the human subthalamic nucleus

Sieger

Serranová

Růžička

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

View full text Add to dashboard Cite

Both animal studies and studies using deep brain stimulation in humans have demonstrated the involvement of the subthalamic nucleus (STN) in motivational and emotional processes; however, participation of this nucleus in processing human emotion has not been investigated directly at the single-neuron level. We analyzed the relationship between the neuronal firing from intraoperative microrecordings from the STN during affective picture presentation in patients with Parkinson's disease (PD) and the affective ratings of emotional valence and arousal performed subsequently. We observed that 17% of neurons responded to emotional valence and arousal of visual stimuli according to individual ratings. The activity of some neurons was related to emotional valence, whereas different neurons responded to arousal. In addition, 14% of neurons responded to visual stimuli. Our results suggest the existence of neurons involved in processing or transmission of visual and emotional information in the human STN, and provide evidence of separate processing of the affective dimensions of valence and arousal at the level of single neurons as well.emotion | basal ganglia | subthalamic nucleus | single neuron | arousal A t one time, the subthalamic nucleus (STN), which is an important target for deep brain stimulation (DBS) in the treatment of motor symptoms in Parkinson's disease (PD), was considered an important regulator of motor function (1, 2); however, the occurrence of postoperative neuropsychiatric complications has expanded interest in the nonmotor function of the STN (3, 4). Animal and human studies have already demonstrated the additional functional role of the STN in emotional and motivational processes (5-12). In addition, recent functional MRI studies found STN activation in response to emotional stimuli in healthy subjects (13,14). Therefore, we hypothesized that emotional activity-related neurons should exist in the STN. Participation of the STN in processing emotion has not yet been investigated directly at the single-neuron level in humans. Nonetheless, single-neuron activity related to a priori defined emotional categories (e.g., positive vs. negative) has been detected in a few human brain regions, including the hippocampus, amygdala, and prefrontal and subcallosal cortex (15-18).It has been proposed that emotional behavior is organized along two psychophysiological dimensions: emotional valence, varying from unpleasant to pleasant, and arousal, varying from low to high (19). The individual assessment of these dimensions is closely correlated with somatic and autonomic measures of emotions (20,21). Contrary to a priori categories, they can better reflect emotional characteristics of the stimulus in an individual context, and they take into account interindividual differences based on specific behavioral determinants, such as affective disposition and personality traits (22).In this study, we aimed to detect single-neuron firing pattern changes in the STN that are related to emotional arousal and valence from the in...

show abstract

The Subthalamic Microlesion Story in Parkinson's Disease: Electrode Insertion-Related Motor Improvement with Relative Cortico-Subcortical Hypoactivation in fMRI

Cited by 56 publications

References 99 publications

Basal Ganglia Neuronal Activity during Scanning Eye Movements in Parkinson’s Disease

Basal Ganglia Neuronal Activity during Scanning Eye Movements in Parkinson’s Disease

Motor Matters: Tackling Heterogeneity of Parkinson’s Disease in Functional MRI Studies

Distinct populations of neurons respond to emotional valence and arousal in the human subthalamic nucleus

Contact Info

Product

Resources

About