Sensorimotor processing in the basal ganglia leads to transient beta oscillations during behavior

Mirzaei, Amin; Kumar, Arvind; Leventhal, Daniel K.; Mallet, Nicolas; Aertsen, Ad; Berke, Joshua D.; Schmidt, Robert

doi:10.1101/136879

Cited by 13 publications

(18 citation statements)

References 84 publications

(135 reference statements)

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“…Importantly though, these results do not exclude the possibility that the spontaneous and transient β-oscillations classically recorded in dopamine-intact conditions during movements are generated through cortical mechanisms 48,49 . Indeed, it remains to be addressed whether parkinsonian β-oscillations originate from dysregulation in space and time of normal β-oscillations 50,51 or whether they are generated through entirely different circuit mechanisms.…”

Section: Discussionmentioning

confidence: 99%

The globus pallidus orchestrates abnormal network dynamics in a model of Parkinsonism

et al. 2020

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The dynamical properties of cortico-basal ganglia (CBG) circuits are dramatically altered following the loss of dopamine in Parkinson's disease (PD). The neural circuit dysfunctions associated with PD include spike-rate alteration concomitant with excessive oscillatory spikesynchronization in the beta frequency range (12-30 Hz). Which neuronal circuits orchestrate and propagate these abnormal neural dynamics in CBG remains unknown. In this work, we combine in vivo electrophysiological recordings with advanced optogenetic manipulations in normal and 6-OHDA rats to shed light on the mechanistic principle underlying circuit dysfunction in PD. Our results show that abnormal neural dynamics present in a rat model of PD do not rely on cortical or subthalamic nucleus activity but critically dependent on globus pallidus (GP) integrity. Our findings highlight the pivotal role played by the GP which operates as a hub nucleus capable of orchestrating firing rate and synchronization changes across CBG circuits both in normal and pathological conditions.

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Section: Discussionmentioning

confidence: 99%

The globus pallidus orchestrates abnormal network dynamics in a model of Parkinsonism

et al. 2020

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“…A recent study (Mirzaei et al, 2017) tested whether this computational model for beta generation applies in awake behaving animals. This was done by first generating artificial activity patterns, mimicking single-unit activity recorded in the striatum, GPe, and STN of rats performing a cued choice task (Schmidt et al, 2013;Mallet et al, 2016).…”

Section: Mechanisms Of Generating Beta: Bg and Cortexmentioning

confidence: 99%

“…This might reflect a situation in which cortical circuits use beta to maintain stimulus information in working memory (see above) and exert control on subcortical structures to protect them against interference. By contrast, "bottom-up" communication could potentially generate beta in the STN-GPe network due to (non-oscillating) sensory and motor inputs, including ramping activity in STN (Mirzaei et al, 2017). This beta could affect reaction times and propagate through cortex via the mediodorsal thalamus.…”

Section: Mechanisms Of Generating Beta: Bg and Cortexmentioning

confidence: 99%

Beta Oscillations in Working Memory, Executive Control of Movement and Thought, and Sensorimotor Function

et al. 2019

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Beta oscillations (ϳ13 to 30 Hz) have been observed during many perceptual, cognitive, and motor processes in a plethora of brain recording studies. Although the function of beta oscillations (hereafter "beta" for short) is unlikely to be explained by any single monolithic description, we here discuss several convergent findings. In prefrontal cortex (PFC), increased beta appears at the end of a trial when working memory information needs to be erased. A similar "clear-out" function might apply during the stopping of action and the stopping of long-term memory retrieval (stopping thoughts), where increased prefrontal beta is also observed. A different apparent role for beta in PFC occurs during the delay period of working memory tasks: it might serve to maintain the current contents and/or to prevent interference from distraction. We confront the challenge of relating these observations to the large literature on beta recorded from sensorimotor cortex. Potentially, the clear-out of working memory in PFC has its counterpart in the postmovement clear-out of the motor plan in sensorimotor cortex. However, recent studies support alternative interpretations. In addition, we flag emerging research on different frequencies of beta and the relationship between beta and single-neuron spiking. We also discuss where beta might be generated: basal ganglia, cortex, or both. We end by considering the clinical implications for adaptive deep-brain stimulation.

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“…Under physiological conditions, neurons in the basal ganglia engage in brief transient synchronization at beta frequencies, and the dynamics of synchronization are instrumental to basal ganglia function (Feingold et al, 2015;Mirzaei et al, 2017;Tinkhauser et al, 2017a). Conversely, beta activity recorded in the STN is exaggerated in PD (Neumann et al, 2016;Steiner et al, 2017;Tinkhauser et al, 2017a), and clinically effective DBS reduces synchrony in this nucleus (Kühn et al, 2008).…”

Section: Significance Statementmentioning

confidence: 99%

Connectivity and dynamics underlying synaptic control of the Subthalamic Nucleus

et al. 2019

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Adaptive motor control critically depends on the interconnected nuclei of the basal ganglia in the CNS. A pivotal element of the basal ganglia is the subthalamic nucleus (STN), which serves as a therapeutic target for deep brain stimulation (DBS) in movement disorders, such as Parkinson's disease. The functional connectivity of the STN at the microcircuit level, however, still requires rigorous investigation. Here we combine multiple simultaneous whole-cell recordings with extracellular stimulation and post hoc neuroanatomical analysis to investigate intrinsic and afferent connectivity and synaptic properties of the STN in acute brain slices obtained from rats of both sexes. Our data reveal an absence of intrinsic connectivity and an afferent innervation with low divergence, suggesting that STN neurons operate as independent processing elements driven by upstream structures. Hence, synchrony in the STN, a hallmark of motor processing, exclusively depends on the interactions and dynamics of GABAergic and glutamatergic afferents. Importantly, these inputs are subject to differential short-term depression when stimulated at high, DBS-like frequencies, shifting the balance of excitation and inhibition toward inhibition. Thus, we present a mechanism for fast yet transient decoupling of the STN from synchronizing afferent control. Together, our study provides new insights into the microcircuit organization of the STN by identifying its neurons as parallel processing units and thus sets new constraints for future computational models of the basal ganglia. The observed differential short-term plasticity of afferent inputs further offers a basis to better understand and optimize DBS algorithms.

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Sensorimotor processing in the basal ganglia leads to transient beta oscillations during behavior

Cited by 13 publications

References 84 publications

The globus pallidus orchestrates abnormal network dynamics in a model of Parkinsonism

The globus pallidus orchestrates abnormal network dynamics in a model of Parkinsonism

Beta Oscillations in Working Memory, Executive Control of Movement and Thought, and Sensorimotor Function

Connectivity and dynamics underlying synaptic control of the Subthalamic Nucleus

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