Altered Local Field Potential Relationship Between the Parafascicular Thalamic Nucleus and Dorsal Striatum in Hemiparkinsonian Rats

Abstract

The thalamostriatal pathway is implicated in Parkinson's disease (PD); however, PD-related changes in the relationship between oscillatory activity in the centromedian-parafascicular complex (CM/Pf, or the Pf in rodents) and the dorsal striatum (DS) remain unclear. Therefore, we simultaneously recorded local field potentials (LFPs) in both the Pf and DS of hemiparkinsonian and control rats during epochs of rest or treadmill walking. The dopamine-lesioned rats showed increased LFP power in the beta band (12 Hz-35 Hz) in the Pf and DS during both epochs, but decreased LFP power in the delta (0.5 Hz-3 Hz) band in the Pf during rest epochs and in the DS during both epochs, compared to control rats. In addition, exaggerated low gamma (35 Hz-70 Hz) oscillations after dopamine loss were restricted to the Pf regardless of the behavioral state. Furthermore, enhanced synchronization of LFP oscillations was found between the Pf and DS after the dopamine lesion. Significant increases occurred in the mean coherence in both theta (3 Hz-7 Hz) and beta bands, and a significant increase was also noted in the phase coherence in the beta band between the Pf and DS during rest epochs. During the treadmill walking epochs, significant increases were found in both the alpha (7 Hz-12 Hz) and beta bands for two coherence measures. Collectively, dramatic changes in the relative LFP power and coherence in the thalamostriatal pathway may underlie the dysfunction of the basal ganglia-thalamocortical network circuits in PD, contributing to some of the motor and non-motor symptoms of the disease.

Keywords: Dorsal striatum; Local field potential; Parafascicular thalamic nucleus; Parkinson’s disease; Synchronization.

Fig. 1

Verification of recording sites in the Pf and DS. A, C Representative images of cresyl violet-stained coronal sections through the Pf (A) and DS (C), showing the locations of the electrode tips (arrows). B, D Three schematics showing the sites of recording electrodes in the Pf (B) and DS (D) of both control (black dots, n = 7) and dopamine-lesioned rats (gray dots, n = 7). Numbers represent the distance from bregma in the anteroposterior plane. Pf: parafascicular thalamic nucleus; DS: dorsal striatum.

Fig. 2

LFP activity in the Pf during rest episodes. A, B Representative scalograms showing the time-frequency plots of LFP power in control (A) and lesioned (B) rats. C Averaged Welch power spectra across frequency in the control and lesioned groups. D Mean relative LFP power in the Pf within the series of frequency ranges 0.5 Hz–3 Hz, 3 Hz–7 Hz, 7 Hz–12 Hz, 12 Hz–35 Hz, and 70 Hz–100 Hz in control (n = 7) and lesioned (n = 7) rats (*P < 0.05, **P < 0.001; Pf, parafascicular thalamic nucleus).

Fig. 3

LFP activity in the Pf during treadmill walking epochs. A, B Representative scalograms showing the time-frequency plots of LFP power in control (A) and lesioned (B) rats. C Averaged Welch power spectra across frequency in control and lesioned groups. D Mean relative LFP power in the Pf in the frequency ranges 0.5 Hz–3 Hz, 3 Hz–7 Hz, 7 Hz–12 Hz, 12 Hz–35 Hz, and 70 Hz–100 Hz in control (n = 6) and lesioned (n = 7) rats (*P < 0.05; Pf, parafascicular thalamic nucleus).

Fig. 4

LFP activity in the DS during rest episodes. A, B Representative scalograms showing time-frequency plots of LFP power in control (A) and lesioned (B) rats. C Averaged Welch power spectra across frequency in both control and lesioned groups. D Mean relative LFP power in the DS in the series of frequency ranges 0.5 Hz–3 Hz, 3 Hz–7 Hz, 7 Hz–12 Hz, 12 Hz–35 Hz, and 70 Hz–100 Hz in control (n = 7) and lesioned (n = 7) rats (*P < 0.05).

Fig. 5

LFP activity in the DS during the treadmill walking epochs. A, B Representative scalograms showing time-frequency plots of LFP power in control (A) and lesioned (B) rats. C Averaged Welch power spectra across frequency in control and lesioned groups. D Mean relative LFP power in the DS in the series of frequency ranges 0.5 Hz–3 Hz, 3 Hz–7 Hz, 7 Hz–12 Hz, 12 Hz–35 Hz, and 70 Hz–100 Hz in control (n = 6) and lesioned (n = 7) rats (*P < 0.05).

Fig. 6

LFP coherence of Pf-DS during rest epochs. A, C Mean coherence values in the series of frequency bands 0.5 Hz–3 Hz, 3 Hz–7 Hz, 7 Hz–12 Hz, 12 Hz–35 Hz, 35 Hz–70 Hz, and 70 Hz–100 Hz (A) and averaged coherence values across frequency (C). B, D Mean phase coherence values in the series of frequency bands 0.5 Hz–3 Hz, 3 Hz–7 Hz, 7 Hz–12 Hz, 12 Hz–35 Hz, 35 Hz–70 Hz, and 70 Hz–100 Hz (B) and polar plots of phase coherence values in the (β) 12–35 Hz band (D) (*P < 0.05, **P < 0.001; Pf, parafascicular thalamic nucleus; DS, dorsal striatum).

Fig. 7

LFP coherence of Pf-DS during treadmill walking epochs. A, C Mean coherence values in the series of frequency bands 0.5 Hz–3 Hz, 3 Hz–7 Hz, 7 Hz–12 Hz, 12 Hz–35 Hz, 35 Hz–70 Hz, and 70 Hz–100 Hz (A) and averaged coherence values across frequency (C). B, D Mean phase coherence values in the series of frequency bands 0.5 Hz–3 Hz, 3 Hz–7 Hz, 7 Hz–12 Hz, 12 Hz–35 Hz, 35 Hz–70 Hz, and 70 Hz–100 Hz (B) and polar plots of phase coherence values in the (α) 7–12 Hz and (β) 12–35 Hz bands (*P < 0.05, **P < 0.001; Pf, parafascicular thalamic nucleus; DS, dorsal striatum).