Cortico-Striatal Oscillations Are Correlated to Motor Activity Levels in Both Physiological and Parkinsonian Conditions

Moënne‐Loccoz, Cristóbal; Astudillo-Valenzuela, Carolina; Skovgård, Katrine; Salazar-Reyes, Carolina A.; Barrientos, Sebastián A.; Garcia-Nuñez, Ximena Paz; Cenci, M. Angela; Petersson, Per; Fuentes-Flores, Romulo

doi:10.3389/fnsys.2020.00056

Cited by 11 publications

(6 citation statements)

References 62 publications

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“…We also found that ChI spiking is time-locked to movement onset, and tracks the animal’s stepping cycle in the 1–4 Hz delta frequency range. Studies have reported that certain neurons in the motor cortex, thalamus, and cerebellum have spikes phase locked to LFP delta oscillations 10 – 14 , 51 , and projections from these areas to the striatum exhibit stepping cycle-dependent activity 10 – 14 . Thus, the movement-dependent entrainment of cellular delta rhythms observed in ChIs likely originates from movement-related synaptic inputs.…”

Section: Discussionmentioning

confidence: 99%

Striatal cholinergic interneuron membrane voltage tracks locomotor rhythms in mice

et al. 2023

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Rhythmic neural network activity has been broadly linked to behavior. However, it is unclear how membrane potentials of individual neurons track behavioral rhythms, even though many neurons exhibit pace-making properties in isolated brain circuits. To examine whether single-cell voltage rhythmicity is coupled to behavioral rhythms, we focused on delta-frequencies (1–4 Hz) that are known to occur at both the neural network and behavioral levels. We performed membrane voltage imaging of individual striatal neurons simultaneously with network-level local field potential recordings in mice during voluntary movement. We report sustained delta oscillations in the membrane potentials of many striatal neurons, particularly cholinergic interneurons, which organize spikes and network oscillations at beta-frequencies (20–40 Hz) associated with locomotion. Furthermore, the delta-frequency patterned cellular dynamics are coupled to animals’ stepping cycles. Thus, delta-rhythmic cellular dynamics in cholinergic interneurons, known for their autonomous pace-making capabilities, play an important role in regulating network rhythmicity and movement patterning.

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Section: Discussionmentioning

confidence: 99%

Striatal cholinergic interneuron membrane voltage tracks locomotor rhythms in mice

et al. 2023

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“…44 Bradykinesia in PD is currently thought to reflect a corticosubcortical network disorder implying abnormal functional connections among the fronto-basal-gangliathalamocortical motor loop and the cerebellum. [7][8][9][10]45 By contrast, parkinsonian rigidity likely arises from abnormal inputs from GPi and substantia nigra pars reticulata to the pontobulbar reticular formation, leading to hyperactive descending projections (dorsal and medial reticulospinal tracts) directed to propriospinal as well as spinal Ia and Ib interneurons. [11][12][13] This in turn results in hyperexcitability of gamma and alpha motoneurons responsible for increased muscle tone.…”

Section: Bradykinesia and Rigidity Differently Progress After Stn-dbsmentioning

confidence: 99%

“…6 However, several recent observations suggest that bradykinesia and rigidity may reflect at least partly independent mechanisms. Whereas bradykinesia would prominently reflect a network dysfunction in the corticobasal-ganglia-thalamocortical loop, [7][8][9][10] rigidity more likely arises from functional changes in specific brainstem circuits and descending neuronal pathways to the spinal cord. [11][12][13] Hence, to better clarify possible pathophysiological differences and thus disentangle bradykinesia and rigidity in people with PD, innovative ad hoc designed studies are crucially warranted.…”

mentioning

confidence: 99%

Disentangling Bradykinesia and Rigidity in Parkinson's Disease: Evidence from Short‐ and Long‐Term Subthalamic Nucleus Deep Brain Stimulation

Zampogna,

Suppa,

Bove

et al. 2024

Annals of Neurology

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ObjectiveBradykinesia and rigidity are considered closely related motor signs in Parkinson disease (PD), but recent neurophysiological findings suggest distinct pathophysiological mechanisms. This study aims to examine and compare longitudinal changes in bradykinesia and rigidity in PD patients treated with bilateral subthalamic nucleus deep brain stimulation (STN‐DBS).MethodsIn this retrospective cohort study, the clinical progression of appendicular and axial bradykinesia and rigidity was assessed up to 15 years after STN‐DBS in the best treatment conditions (ON medication and ON stimulation). The severity of bradykinesia and rigidity was examined using ad hoc composite scores from specific subitems of the Unified Parkinson's Disease Rating Scale motor part (UPDRS‐III). Short‐ and long‐term predictors of bradykinesia and rigidity were analyzed through linear regression analysis, considering various preoperative demographic and clinical data, including disease duration and severity, phenotype, motor and cognitive scores (eg, frontal score), and medication.ResultsA total of 301 patients were examined before and 1 year after surgery. Among them, 101 and 56 individuals were also evaluated at 10‐year and 15‐year follow‐ups, respectively. Bradykinesia significantly worsened after surgery, especially in appendicular segments (p < 0.001). Conversely, rigidity showed sustained benefit, with unchanged clinical scores compared to preoperative assessment (p > 0.05). Preoperative motor disability (eg, composite scores from the UPDRS‐III) predicted short‐ and long‐term outcomes for both bradykinesia and rigidity (p < 0.01). Executive dysfunction was specifically linked to bradykinesia but not to rigidity (p < 0.05).InterpretationBradykinesia and rigidity show long‐term divergent progression in PD following STN‐DBS and are associated with independent clinical factors, supporting the hypothesis of partially distinct pathophysiology. ANN NEUROL 2024

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“…Brain structures Experimentally reported frequency shifts/differences Gamma (∼30-100Hz) Neocortex Hippocampus (Traub et al, 1996;Gregoriou et al, 2009;Lima et al, 2010;Ray and Maunsell, 2010;Ahmed and Mehta, 2012;Bosman et al, 2012;Jia et al, 2013;Roberts et al, 2013;van Pelt and Fries, 2013;Lowet et al, 2017) Beta (∼15-35Hz) Neocortex Basal ganglia (Salmelin and Hari, 1994;Neuper and Pfurtscheller, 2001;Kilavik et al, 2012;Lundqvist et al, 2016;Canessa et al, 2020;Moënne-Loccoz et al, 2020) Alpha (∼8-12Hz) Neocortex Thalamus (Haegens et al, 2014;Zhang et al, 2018;Green et al, 2022;Sato, 2022) Theta (∼4-10Hz) Neocortex Hippocampus (Giocomo et al, 2007;Goutagny et al, 2009;Axmacher et al, 2010;Patel et al, 2012;Zhang and Jacobs, 2015;Zhang et al, 2018) Delta (∼1-4Hz)…”

Section: Frequency-bandsmentioning

confidence: 99%

Tuning Neural Synchronization: The Role of Variable Oscillation Frequencies in Neural Circuits

Lowet

Weerd

Roberts

et al. 2022

Front. Syst. Neurosci.

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Brain oscillations emerge during sensory and cognitive processes and have been classified into different frequency bands. Yet, even within the same frequency band and between nearby brain locations, the exact frequencies of brain oscillations can differ. These frequency differences (detuning) have been largely ignored and play little role in current functional theories of brain oscillations. This contrasts with the crucial role that detuning plays in synchronization theory, as originally derived in physical systems. Here, we propose that detuning is equally important to understand synchronization in biological systems. Detuning is a critical control parameter in synchronization, which is not only important in shaping phase-locking, but also in establishing preferred phase relations between oscillators. We review recent evidence that frequency differences between brain locations are ubiquitous and essential in shaping temporal neural coordination. With the rise of powerful experimental techniques to probe brain oscillations, the contributions of exact frequency and detuning across neural circuits will become increasingly clear and will play a key part in developing a new understanding of the role of oscillations in brain function.

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Cortico-Striatal Oscillations Are Correlated to Motor Activity Levels in Both Physiological and Parkinsonian Conditions

Cited by 11 publications

References 62 publications

Striatal cholinergic interneuron membrane voltage tracks locomotor rhythms in mice

Striatal cholinergic interneuron membrane voltage tracks locomotor rhythms in mice

Disentangling Bradykinesia and Rigidity in Parkinson's Disease: Evidence from Short‐ and Long‐Term Subthalamic Nucleus Deep Brain Stimulation

Tuning Neural Synchronization: The Role of Variable Oscillation Frequencies in Neural Circuits

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