Dynamics of Parkinsonian Oscillations Mediated by Transmission Delays in a Mean-field Model of the Basal Ganglia

Overview

Journal Front Cell Neurosci

Specialty Cell Biology

Date 2024 Mar 29

PMID 38550919

Authors

Atefeh Asadi

Mojtaba Madadi Asl

Alireza Valizadeh

Matjaz Perc

Affiliations

Soon will be listed here.

Abstract

Introduction: Neural interactions in the brain are affected by transmission delays which may critically alter signal propagation across different brain regions in both normal and pathological conditions. The effect of interaction delays on the dynamics of the generic neural networks has been extensively studied by theoretical and computational models. However, the role of transmission delays in the development of pathological oscillatory dynamics in the basal ganglia (BG) in Parkinson's disease (PD) is overlooked.

Methods: Here, we investigate the effect of transmission delays on the discharge rate and oscillatory power of the BG networks in control (normal) and PD states by using a Wilson-Cowan (WC) mean-field firing rate model. We also explore how transmission delays affect the response of the BG to cortical stimuli in control and PD conditions.

Results: Our results show that the BG oscillatory response to cortical stimulation in control condition is robust against the changes in the inter-population delays and merely depends on the phase of stimulation with respect to cortical activity. In PD condition, however, transmission delays crucially contribute to the emergence of abnormal alpha (8-13 Hz) and beta band (13-30 Hz) oscillations, suggesting that delays play an important role in abnormal rhythmogenesis in the parkinsonian BG.

Discussion: Our findings indicate that in addition to the strength of connections within and between the BG nuclei, oscillatory dynamics of the parkinsonian BG may also be influenced by inter-population transmission delays. Moreover, phase-specificity of the BG response to cortical stimulation may provide further insight into the potential role of delays in the computational optimization of phase-specific brain stimulation therapies.

References

Planert H, Szydlowski S, Hjorth J, Grillner S, Silberberg G . Dynamics of synaptic transmission between fast-spiking interneurons and striatal projection neurons of the direct and indirect pathways. J Neurosci. 2010; 30(9):3499-507. PMC: 6634087. DOI: 10.1523/JNEUROSCI.5139-09.2010. View

Stoffers D, Bosboom J, Deijen J, Wolters E, Berendse H, Stam C . Slowing of oscillatory brain activity is a stable characteristic of Parkinson's disease without dementia. Brain. 2007; 130(Pt 7):1847-60. DOI: 10.1093/brain/awm034. View

Bevan M, Wilson C . Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J Neurosci. 1999; 19(17):7617-28. PMC: 6782508. View

Calabresi P, Picconi B, Tozzi A, Ghiglieri V, Di Filippo M . Direct and indirect pathways of basal ganglia: a critical reappraisal. Nat Neurosci. 2014; 17(8):1022-30. DOI: 10.1038/nn.3743. View

Magill P, Pogosyan A, Sharott A, Csicsvari J, Bolam J, Brown P . Changes in functional connectivity within the rat striatopallidal axis during global brain activation in vivo. J Neurosci. 2006; 26(23):6318-29. PMC: 6675195. DOI: 10.1523/JNEUROSCI.0620-06.2006. View

Kerr C, van Albada S, Neymotin S, Chadderdon G, Robinson P, Lytton W . Cortical information flow in Parkinson's disease: a composite network/field model. Front Comput Neurosci. 2013; 7:39. PMC: 3635017. DOI: 10.3389/fncom.2013.00039. View

Kondabolu K, Roberts E, Bucklin M, McCarthy M, Kopell N, Han X . Striatal cholinergic interneurons generate beta and gamma oscillations in the corticostriatal circuit and produce motor deficits. Proc Natl Acad Sci U S A. 2016; 113(22):E3159-68. PMC: 4896681. DOI: 10.1073/pnas.1605658113. View

Wichmann T, DeLong M . Basal ganglia discharge abnormalities in Parkinson's disease. J Neural Transm Suppl. 2006; (70):21-5. DOI: 10.1007/978-3-211-45295-0_5. View

Cagnan H, Pedrosa D, Little S, Pogosyan A, Cheeran B, Aziz T . Stimulating at the right time: phase-specific deep brain stimulation. Brain. 2016; 140(1):132-145. PMC: 5226063. DOI: 10.1093/brain/aww286. View

10.

Bergman H, Wichmann T, Karmon B, DeLong M . The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol. 1994; 72(2):507-20. DOI: 10.1152/jn.1994.72.2.507. View

11.

McConnell G, So R, Hilliard J, Lopomo P, Grill W . Effective deep brain stimulation suppresses low-frequency network oscillations in the basal ganglia by regularizing neural firing patterns. J Neurosci. 2012; 32(45):15657-68. PMC: 3502634. DOI: 10.1523/JNEUROSCI.2824-12.2012. View

12.

Humphries M, Stewart R, Gurney K . A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. J Neurosci. 2006; 26(50):12921-42. PMC: 6674973. DOI: 10.1523/JNEUROSCI.3486-06.2006. View

13.

Bahuguna J, Tetzlaff T, Kumar A, Hellgren Kotaleski J, Morrison A . Homologous Basal Ganglia Network Models in Physiological and Parkinsonian Conditions. Front Comput Neurosci. 2017; 11:79. PMC: 5572265. DOI: 10.3389/fncom.2017.00079. View

14.

Madadi Asl M, Valizadeh A, Tass P . Propagation delays determine neuronal activity and synaptic connectivity patterns emerging in plastic neuronal networks. Chaos. 2018; 28(10):106308. DOI: 10.1063/1.5037309. View

15.

Steiner L, Barreda Tomas F, Planert H, Alle H, Vida I, Geiger J . Connectivity and Dynamics Underlying Synaptic Control of the Subthalamic Nucleus. J Neurosci. 2019; 39(13):2470-2481. PMC: 6435833. DOI: 10.1523/JNEUROSCI.1642-18.2019. View

16.

Mallet N, Ballion B, Le Moine C, Gonon F . Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J Neurosci. 2006; 26(14):3875-84. PMC: 6674115. DOI: 10.1523/JNEUROSCI.4439-05.2006. View

17.

Valsky D, Heiman Grosberg S, Israel Z, Boraud T, Bergman H, Deffains M . What is the true discharge rate and pattern of the striatal projection neurons in Parkinson's disease and Dystonia?. Elife. 2020; 9. PMC: 7462612. DOI: 10.7554/eLife.57445. View

18.

Gerstner W, Kempter R, van Hemmen J, Wagner H . A neuronal learning rule for sub-millisecond temporal coding. Nature. 1996; 383(6595):76-81. DOI: 10.1038/383076a0. View

19.

Pavlides A, Hogan S, Bogacz R . Improved conditions for the generation of beta oscillations in the subthalamic nucleus--globus pallidus network. Eur J Neurosci. 2012; 36(2):2229-39. DOI: 10.1111/j.1460-9568.2012.08105.x. View

20.

Burke S, Barnes C . Neural plasticity in the ageing brain. Nat Rev Neurosci. 2005; 7(1):30-40. DOI: 10.1038/nrn1809. View