Statistical Properties of Pauses of the High-Frequency Discharge Neurons in the External Segment of the Globus Pallidus

Elias, Shlomo; Joshua, Mati; Goldberg, Joshua A.; Heimer, Gali; Arkadir, David; Morris, Genela; Bergman, Hagai

doi:10.1523/jneurosci.4156-06.2007

Cited by 88 publications

(105 citation statements)

References 65 publications

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“…The classification of each recorded cell as belonging to either the external or internal pallidum was determined as follows: Neurons located at a depth of Ͻ1.5 mm from the striatopallidal border, or neurons that exhibited pauses in their firing pattern were categorized as GPe neurons (DeLong, 1971;Elias et al, 2007). Candidates to GPi were neurons with a highfrequency discharge rate with no pauses, 2.5 mm from the striatopallidal border or farther in the ventromedial direction.…”

Section: Methodsmentioning

confidence: 99%

Low-Pass Filter Properties of Basal Ganglia–Cortical–Muscle Loops in the Normal and MPTP Primate Model of Parkinsonism

Rivlin‐Etzion¹,

Marmor²,

Saban³

et al. 2008

J. Neurosci.

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Oscillatory bursting activity is commonly found in the basal ganglia (BG) and the thalamus of the parkinsonian brain. The frequency of these oscillations is often similar to or higher than that of the parkinsonian tremor, but their relationship to the tremor and other parkinsonian symptoms is still under debate. We studied the frequency dependency of information transmission in the cortex-BG and cortex-periphery loops by recording simultaneously from multiple electrodes located in the arm-related primary motor cortex (MI) and in the globus pallidus (GP) of two vervet monkeys before and after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) treatment and induction of parkinsonian symptoms. We mimicked the parkinsonian bursting oscillations by stimulating with 35 ms bursts given at different frequencies through microelectrodes located in MI or GP while recording the evoked neuronal and motor responses. In the normal state, microstimulation of MI or GP does not modulate the discharge rate in the other structure. However, the functionalconnectivity between MI and GP is greatly enhanced after MPTP treatment. In the frequency domain, GP neurons usually responded equally to 1-15 Hz stimulation bursts in both states. In contrast, MI neurons demonstrated low-pass filter properties, with a cutoff frequency above 5 Hz for the MI stimulations, and below 5 Hz for the GP stimulations. Finally, muscle activation evoked by MI microstimulation was markedly attenuated at frequencies higher than 5 Hz. The low-pass properties of the pathways connecting GP to MI to muscles suggest that parkinsonian tremor is not directly driven by the BG 5-10 Hz burst oscillations despite their similar frequencies.

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Section: Methodsmentioning

confidence: 99%

Low-Pass Filter Properties of Basal Ganglia–Cortical–Muscle Loops in the Normal and MPTP Primate Model of Parkinsonism

Rivlin‐Etzion¹,

Marmor²,

Saban³

et al. 2008

J. Neurosci.

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“…These include the majority (85%; DeLong 1971) of GPe (external segment of globus pallidus) neurons, which play a central role in the internal stages of the basal ganglia circuitry (Arkadir et al 2004;Bolam et al 2000;Kita 2007) and almost all GPi (internal segment of globus pallidus) and SNr (substantia nigra pars reticulata) neurons, which compose the output stage of the basal ganglia network (Gerfen 2004;Haber and Gdowski 2004;Schultz 1986). The high-frequency discharge of many of the GPe neurons is also interrupted by long intervals of total silence or pauses (DeLong 1971;Elias et al 2007).…”

Section: Introductionmentioning

confidence: 99%

“…Details of the surgery and data recording methods are given elsewhere Heimer et al 2006). Neurons in all structures were identified according to their stereotaxic coordinates (based on the MRI and the primate atlas data) and their real-time physiological identification (for example, typical spike shape and firing characteristics of neighboring neurons; for details see Elias et al 2007). …”

Section: Introductionmentioning

confidence: 99%

Balance of Increases and Decreases in Firing Rate of the Spontaneous Activity of Basal Ganglia High-Frequency Discharge Neurons

Elias¹,

Ritov

Bergman

2008

Journal of Neurophysiology

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of increases and decreases in firing rate of the spontaneous activity of basal ganglia high-frequency discharge neurons. J Neurophysiol 100: 3086 -3104, 2008. First published October 8, 2008 doi:10.1152/jn.90714.2008. Most neurons in the external and internal segments of the globus pallidus and the substantia nigra pars reticulata (GPe, GPi, and SNr) are characterized by a high-frequency discharge (HFD) rate (50 -80 Hz) that, in most GPe neurons, is also interrupted by pauses. Almost all (ϳ90%) of the synaptic inputs to these HFD neurons are GABAergic and inhibitory. Nevertheless, their responses to behavioral events are usually dominated by increases in discharge rate. Additionally, there are no reports of prolonged bursts in the spontaneous activity of these cells that could reflect their disinhibition by GPe pauses. We recorded the spontaneous activity of 385 GPe, GPi, and SNr HFD neurons during a quiet-wakeful state from two monkeys. We developed three complementary methods to quantify the balance of increases and decreases in the spontaneous discharge of HFD neurons and validated them by simulations. Unlike the behavioral evoked responses, the spontaneous activity of pallidal and SNr neurons is not dominated by increases. Moreover, the activity of basal ganglia neurons does not include bursts that could reflect disinhibition by the spontaneous pauses of GPe neurons. These findings suggest that the discharge increase/decrease balance during a quiet-wakeful state better reflects the inhibitory input of the HFD basal ganglia neurons than during responses to behavioral events; however, the GPe pauses are not echoed by comparable bursts either in the GPe or in the output nuclei. Changes in the excitatory drive of these structures (e.g., during behavioral activity) thus may lead to a remarkable change in this balance.

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“…We have suspected that Str inputs generate the pauses and that the increased pause and burst activity of GPe neurons observed after DA depletion is due, in part, to the increased gain of the cortico-Str-GPe projection (Elias et al 2007;Kita and Kita 2011a, b). Str-GPe synapses are known to generate weak (Ͻ10 pA), unitary inhibitory postsynaptic currents/inhibitory postsynaptic potentials (IPSCs/IPSPs) in GPe (Kita 2007;Tecuapetla et al 2009), implying that a synchronous activation of a large number of Str projection neurons is required to induce pauses in GPe.…”

mentioning

confidence: 99%

Short-term plasticity shapes activity pattern-dependent striato-pallidal synaptic transmission

Kim

Kita

2013

Journal of Neurophysiology

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Kim J, Kita H. Short-term plasticity shapes activity pattern-dependent striato-pallidal synaptic transmission. J Neurophysiol 109: 932-939, 2013. First published November 28, 2012 doi:10.1152/jn.00459.2012.-The cortico-striato (Str)-globus pallidus external segment (GPe) projection plays major roles in the control of neuronal activity in the basal ganglia under both normal and pathological conditions. The present study used rat brain-slice preparations to address our hypothesis that the gain of this disynaptic projection is dynamically controlled by activations of short-term plasticity mechanisms of Str-GPe synapses. The Str-GPe projection neurons fire with very different frequency and firing patterns in vivo depending on the condition of the animal. The results show that the Str-GPe synapses have very strong short-term enhancement mechanisms and that repetitive burst activation of the Str-GPe synapses, which mimic oscillatory burst firing of Str neurons, can sustain enhanced states of synaptic transmission for tens of seconds. The results reveal that the short-term enhancement of StrGPe synapses contributes to the generation of pauses in the firing of GPe neurons and that signal transfer function in the Str-GPe projection is highly dependent on the firing pattern of Str neurons.

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Statistical Properties of Pauses of the High-Frequency Discharge Neurons in the External Segment of the Globus Pallidus

Cited by 88 publications

References 65 publications

Low-Pass Filter Properties of Basal Ganglia–Cortical–Muscle Loops in the Normal and MPTP Primate Model of Parkinsonism

Low-Pass Filter Properties of Basal Ganglia–Cortical–Muscle Loops in the Normal and MPTP Primate Model of Parkinsonism

Balance of Increases and Decreases in Firing Rate of the Spontaneous Activity of Basal Ganglia High-Frequency Discharge Neurons

Short-term plasticity shapes activity pattern-dependent striato-pallidal synaptic transmission

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