What is the true discharge rate and pattern of the striatal projection neurons in Parkinson’s disease and Dystonia?
- Department of Medical Neurobiology, Institute of Medical Research Israel - Canada (IMRIC), The Hebrew University - Hadassah Medical School, Israel
- The Edmond and Lily Safra Center for Brain Sciences, The Hebrew University, Israel
- Department of Neurosurgery, Hadassah University Hospital, Israel
- University of Bordeaux, UMR 5293, IMN, France
- CNRS, UMR 5293, IMN, France
- CHU de Bordeaux, IMN Clinique, France
Figures
Figure 1
A 3D rendering of group-based microelectrode track trajectories in the posterior putamen.
(A) Posterior view of the microelectrode track trajectories from both PD and dystonic patients. An axial image from the normalized scan, at the level of the rostral midbrain, is shown as a backdrop. …
Figure 2
Striatal firing rate in parkinsonian (PD) and dystonic (DYST) patients decreases as isolation quality of the units increases.
(A) Examples of full-length (left panels) and 1 s (middle panels) striatal spiking recordings. Above the spiking activity is the digital display of the detection (spike train) of the sorted unit …
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Figure 2—source data 1
Firing rate and isolation score of all units in PD.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig2-data1-v2.xls
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Figure 2—source data 2
Firing rate and isolation score of all units in Dystonia.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig2-data2-v2.xls
Figure 3 with 5 supplements
No drastic or specific change in the features (median ±MAD values) of striatal neuronal activity in parkinsonian (PD) and dystonic (DYST) patients.
Comparison of the firing rate (first column), the coefficient of variation (CV) of the inter-spike interval (ISI) (second column), the β power of the multi-unit activity (MUA, spiking activity) …
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Figure 3—source data 1
Spiking features of all units in PD.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig3-data1-v2.xls
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Figure 3—source data 2
Spiking features of the well-isolated units in PD.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig3-data2-v2.xls
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Figure 3—source data 3
Spiking features of the well-isolated and stationary units in PD.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig3-data3-v2.xls
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Figure 3—source data 4
Spiking features of all units in Dystonia.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig3-data4-v2.xls
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Figure 3—source data 5
Spiking features of the well-isolated units in Dystonia.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig3-data5-v2.xls
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Figure 3—source data 6
Spiking features of the well-isolated and stationary units in Dystonia.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig3-data6-v2.xls
Figure 3—figure supplement 1
No drastic or specific change in the features (mean ± SEM values) of striatal neuronal activity in parkinsonian (PD) and dystonic (DYST) patients.
Same conventions as Figure 3, except that each bar indicates the mean value and error bars represent SEMs. Same y-axis scales as in Figure 3 and Figure 3—figure supplement 5. Numbers in parentheses …
Figure 3—figure supplement 2
Comparison of the spiking features between the putative well-isolated and stationary SPNs and TANs in PD patients.
(A) Classification of striatal neuron subtypes. Each dot represents a single neuron colored according to its subtype. X-axis: firing rate in spk/s. Y-axis: CV of the ISI. Z-axis: score of the PC1 of …
Figure 3—figure supplement 3
Comparison of the spiking features between the putative well-isolated and stationary SPNs and TANs in dystonic patients.
Same conventions as Figure 3—figure supplement 2.
Figure 3—figure supplement 4
Disease effects on the outliers of the different features of striatal neuronal activity.
Box plots showing the maxima values (i.e., values ≥ 2 SDs of the mean value) of the firing rate (first column), the coefficient of variation (CV) of the inter-spike interval (ISI) (second column), …
Figure 3—figure supplement 5
Median (upper panels) and mean (lower panels) values of the main features of striatal neuronal activity in parkinsonian (PD) and dystonic (DYST) patients.
Figure 4
Inclusion of non-stationary units can erroneously increase the striatal firing rate in parkinsonian (PD) and dystonic (DYST) patients.
(A) Examples of well-isolated (non-stationary and stationary) units recorded in the striatum of PD patients. Grey trace is the band-pass filtered signal and depicts the spiking activity. Above the …
Figure 5
Distributions of the striatal firing rate are skewed to the right in parkinsonian (PD) and dystonic (DYST) patients.
(A) Firing rate of all sorted units regardless of their isolation quality. (B) Firing rate of the well-isolated stationary units only. Skewness = 2.34 and 3.94 for PD and dystonic patients, …
Figure 6 with 1 supplement
No evidence for burst patterns in the striatal spiking activity of parkinsonian (PD) and dystonic (DYST) patients.
(A) Time interval histograms of the inter-spike intervals (ISI) of the well-isolated (isolation score ≥0.6) stationary units. For better visualization, 191 and 292 ISIs > 0.5 s were removed from the …
Figure 6—figure supplement 1
No evidence for burst patterns in the striatal spiking activity of parkinsonian (PD) and dystonic (DYST) patients.
Same conventions as Figure 6, except that the analysis was only conducted on the subset of ≥10 s-MER segments with striatal well-isolated stationary units.
Figure 7
Absence of oscillatory spiking activity in the striatum of parkinsonian (PD) and dystonic (DYST) patients.
Average (mean ± SEM) power spectrum densities (PSDs) of (A) all spiking activities and (B) only spiking activities recorded in the vicinity of well-isolated stationary units. Insets: Average PSDs of …
Figure 8
No locking between spike and β LFP oscillations in the striatum of parkinsonian (PD) and dystonic (DYST) patients.
(A) Average (mean ± SEM) PSDs of striatal LFPs. In the insets, the ordinates are truncated for better visualization of the power. Abscissas are in log scale. N is the number of LFPs averaged. (B) …
Figure 9
Cluster analysis using discharge properties does not reveal well-separated subpopulations of striatal units in parkinsonian (PD) and dystonic (DYST) patients.
2D k-means cluster analysis with k = 2, using the firing rate and the CV of the ISIs of each unit as input parameters. Analysis was performed when considering all (upper panels), only the …
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Figure 9—source data 1
2D k-means cluster analysis for all units in PD.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig9-data1-v2.xls
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Figure 9—source data 2
2D k-means cluster analysis for the well-isolated units in PD.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig9-data2-v2.xls
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Figure 9—source data 3
2D k-means cluster analysis for the well-isolated and stationary units in PD.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig9-data3-v2.xls
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Figure 9—source data 4
2D k-means cluster analysis for all units in Dystonia.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig9-data4-v2.xls
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Figure 9—source data 5
2D k-means cluster analysis for the well-isolated units in Dystonia.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig9-data5-v2.xls
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Figure 9—source data 6
2D k-means cluster analysis for the well-isolated and stationary units in Dystonia.
- https://cdn.elifesciences.org/articles/57445/elife-57445-fig9-data6-v2.xls
Videos
Video 1
3D rotating view of group-based microelectrode trajectories.
Tables
Table 1
Patient demographic information.
| Patient no. | Disease | Surgery side | Trajectories | Gender | Age at onset | Age at surgery | Disease duration (y) |
|---|---|---|---|---|---|---|---|
| 1 | PD | bilateral | R(2) ; L(1) | M | 40 | 62 | 22 |
| 2 | PD | unilateral | R(1) | F | 45 | 62 | 17 |
| 3 | PD | bilateral | R(2) ; L(2) | F | 50 | 62 | 12 |
| 4 | PD | unilateral | L(1) | F | 45 | 62 | 17 |
| 5 | PD | unilateral | R(2) | F | 49 | 60 | 11 |
| 6 | PD | bilateral | R(2) ; L(2) | F | 66 | 72 | 6 |
| 7 | PD | bilateral | R(2) ; L(1) | F | 43 | 59 | 16 |
| 8 | PD | bilateral | R(2) ; L(2) | F | 54 | 68 | 14 |
| 9 | PD | bilateral | R(2) ; L(2) | F | 55 | 62 | 7 |
| 10 | PD | bilateral | R(2) ; L(2) | F | 46 | 58 | 12 |
| 11 | PD | bilateral | R(2) ; L(2) | F | 41 | 57 | 16 |
| 12 | PD | bilateral | R(2) ; L(2) | M | 53 | 66 | 13 |
| 13 | PD | unilateral | L(2) | F | 53 | 63 | 10 |
| 14 | PD | bilateral | R(2) ; L(2) | M | 35 | 44 | 9 |
| 15 | PD | bilateral | R(1) ; L(1) | M | 41 | 57 | 16 |
| 16 | PD | unilateral | R(2) | M | 50 | 57 | 7 |
| 17 | Dystonia (NG) | bilateral | R(1) ; L(2) | F | 36 | 56 | 20 |
| 18 | Dystonia (NG) | bilateral | R(2) ; L(2) | M | 44 | 49 | 5 |
| 19 | Dystonia (NG) | bilateral | R(1) ; L(2) | F | 45 | 65 | 20 |
| 20 | Dystonia (NG) | bilateral | R(2) ; L(1) | F | 58 | 60 | 2 |
| 21 | Dystonia (NG) | bilateral | R(2) ; L(2) | F | 13 | 19 | 6 |
| 22 | Dystonia (NG) | bilateral | R(1) ; L(1) | F | 60 | 63 | 2 |
| 23 | Dystonia (NG) | bilateral | R(2) ; L(2) | M | 60 | 62 | 2 |
| 24 | Dystonia(NG) | bilateral | R(2) ; L(2) | F | 69 | 71 | 2 |
| 25 | Dystonia (G) | bilateral | R(2) ; L(2) | M | 16 | 25 | 9 |
| 26 | Dystonia (G) | bilateral | R(2) ; L(2) | M | 12 | 18 | 6 |
| 27 | Dystonia (G) | bilateral | R(1) ; L(2) | M | 24 | 39 | 15 |
| 28 | Dystonia (G) | bilateral | R(2) ; L(2) | M | 39 | 54 | 15 |
| 29 | Dystonia (G) | bilateral | R(1) ; L(2) | M | 53 | 56 | 3 |
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PD patients (5 males and 11 females) were 60.7 ± 6.1 years old and with a disease duration of 12.8 ± 4.4 years (mean ± standard deviation, SD). Dystonic patients (7 males and six females) were 49.0 ± 18.0 years old and with a disease duration of 8.2 ± 6.9 years (mean ± standard deviation, SD). NG: non-genetic; G: genetic; R: right; L: left; Numbers in parentheses indicate the number of microelectrode trajectories; M: male; F: female.
