Role of Ionotropic Glutamatergic and GABAergic Inputs on the Firing Activity of Neurons in the External Pallidum in Awake Monkeys

Kita, Hitoshi; Nambu, Atsushi; Kaneda, Katsuyuki; Tachibana, Yoshihisa; Takada, Masahiko

doi:10.1152/jn.00346.2004

Cited by 156 publications

(243 citation statements)

References 56 publications

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“…We investigated how experimentally observed changes induced by dopamine depletion might alter the model behavior, in particular considering the effects of (1) enhanced synaptic connections between STN and GPe neurons (Cragg et al, 2004;Shen and Johnson, 2005;Kita, 2007;Fan et al, 2012;Wilson, 2013), including the STN-to-GPe excitation mediated by NMDA receptors (Bernard and Bolam, 1998;Kita et al, 2004), and (2) enhanced efficacy of the striatal GABAergic projection to the GPe (Kish et al, 1999;Obeso et al, 2000;Kita, 2007).…”

Section: Impact Of Relative Weights Of the Direct And Indirect Pathwaysmentioning

confidence: 99%

Role of the Indirect Pathway of the Basal Ganglia in Perceptual Decision Making

2015

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The basal ganglia (BG) play an important role in motor control, reinforcement learning, and perceptual decision making. Modeling and experimental evidence suggest that, in a speed-accuracy tradeoff, the corticostriatal pathway can adaptively adjust a decision threshold (the amount of information needed to make a choice). In this study, we go beyond the focus of previous works on the direct and hyperdirect pathways to examine the contribution of the indirect pathway of the BG system to decision making in a biophysically based spiking network model. We find that the mechanism of adjusting the decision threshold by plasticity of the corticostriatal connections is effective, provided that the indirect pathway counterbalances the direct pathway in their projections to the output nucleus. Furthermore, in our model, changes within basal ganglia connections similar to those that arise in parkinsonism give rise to strong beta oscillations. Specifically, beta oscillations are produced by an abnormal enhancement of the interactions between the subthalamic nucleus (STN) and the external segment of globus pallidus (GPe) in the indirect pathway, with an oscillation frequency that depends on the excitatory cortical input to the STN and the inhibitory input to the GPe from the striatum. In a parkinsonian state characterized by pronounced beta oscillations, the mean reaction time and range of threshold variation (a measure of behavioral flexibility) are significantly reduced compared with the normal state. Our work thus reveals a specific circuit mechanism for impairments of perceptual decision making associated with Parkinson's disease.

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Section: Impact Of Relative Weights Of the Direct And Indirect Pathwaysmentioning

confidence: 99%

Role of the Indirect Pathway of the Basal Ganglia in Perceptual Decision Making

2015

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“…A tungsten electrode (5-8 8 MΩ, FHC Inc., Bowdoin, ME, USA) attached with a silica capillary tube (40-µm inner diameter, 104-µm outer diameter; Polymicro Technologies Inc., Phoenix, AZ, USA) connected to a 1-µL Hamilton microsyringe was used for extracellular recording with local drug injections (modified from Kita et al, 2004;Kaneda et al, 2005;Tachibana et al, 2008).…”

Section: Visual Stimulation and Single-unit Recordingsmentioning

confidence: 99%

“…After consistent and stable visual responses to at least 15 repeated stimuli, a total volume of 0.06-0.2 µL of each drug solution or vehicle (0.1 M PBS, 0.2 µL) was locally injected in the vicinity of recorded neurons at a rate of 0.04 µL/min using a micropump (ESP-32, EICOM, Kyoto, Japan) connected to a Hamilton microsyringe and a silica tube as described above. Drug doses were selected to be in the range of those used in previous studies using local administration of these compounds in vivo, where the antagonists effectively and selectively antagonized GABA receptor-mediated responses (Galvan et al, 2005;Kita et al, 2004Kita et al, , 2006Tachibana et al, 2008Tachibana et al, , 2011. Because the effects of drugs appeared within 5 min in all cases, we presented PSTHs created just before and 5 min after the drug injections from 10-20 trials.…”

Section: Local Drug Injection During Unit Recordingsmentioning

confidence: 99%

GABAergic mechanisms for shaping transient visual responses in the mouse superior colliculus

Kaneda

Isa

2013

Neuroscience

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An object that suddenly appears in the visual field should be quickly detected and responded to because it could be beneficial or harmful. The superficial layer of the superior colliculus (sSC) is a brain structure capable of such functions, as sSC neurons exhibit sharp transient spike discharges with short latency in response to the appearance of a visual stimulus.However, how transient activity is generated in the sSC is poorly understood. Here, we show that inhibitory inputs actively shape transient activity in the sSC. Juxtacellular recordings from anesthetized mice demonstrate that almost all types of sSC neurons, which were identified by post hoc histochemistry, show transient spike discharges, i.e., ON activity, immediately after visual stimulus onset. ON activity was followed by a pause before the visual stimulus was turned off. To determine whether the pause reflected the absence of excitatory drive or inhibitory conductance, we injected depolarizing currents juxtasomally, which enabled us to observe inhibition as decreased discharges. The pause was observed even under this condition, suggesting that inhibitory input caused the pause. We further found that local application of a mixture of gamma aminobutyric acid (GABA) A and GABA B receptor antagonists additively diminished the pause. These results indicate that GABAergic inputs produce transient ON responses by attenuating excitatory activity through the cooperative activation of GABA A and GABA B receptors, allowing sSC neurons to act as a saliency detector. Detecting an object that suddenly appears in the visual field is crucial for animals because their survival may depend on whether the object is beneficial or harmful. Transient, but not persistent, spike discharges in the sensory systems should encode the detection of the appearance. One of the candidate nuclei for this function is the superior colliculus (SC), a midbrain structure that is critical for visuomotor information processing (Sparks, 1986;Isa and Sparks, 2006). The superficial layer of the SC (sSC) receives visual inputs from the retina and the primary visual cortex (V1) in a retinotopically organized manner (Dräger and Hubel, 1976;May, 2006). sSC neurons exhibit transient spike discharges, called ON responses, immediately after the appearance of a visual stimulus (Schiller and Koerner, 1971; Cynader, 1972, 1975;Cynader and Berman, 1972;Goldberg and Wurtz, 1972;Dräger and Hubel, 1975;Rhoades and Chalupa, 1977;Marrocco and Li, 1977;Moors and Vendrik, 1979;Wang et al., 2010), implying that the sSC could detect the appearance of the object. Indeed, lesions or inactivation of the SC cause a detection deficit of visual stimuli (Butter et al., 1978;Overton and Dean, 1988;Fitzmaurice et al., 2003).The sSC consists of several cell types, including excitatory and inhibitory neurons (Mize, 1992;Endo et al., 2003Endo et al., , 2005May, 2006;Kaneda et al., 2008). Previous intracellular recording and labeling studies elucidated that some sSC neurons responded to moving or static visual stim...

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“…However, in most brain circuits, EPSP-IPSP sequences are more commonly observed than IPSP-EPSP sequences (Pouille and Scanziani, 2004). Indeed, this sequence also occurs when cortical excitation of STN neurons is relayed to the reciprocally connected GP, which in turn generates a feedback IPSP Maurice et al, 1998;Nambu et al, 2000;Kita et al, 2004). Because feedforward and/or feedback GABAergic inhibition are critical for the synchronization of neuronal network activity at a variety of functionally and pathologically relevant frequencies (Cobb et al, 1995;McCormick and Bal, 1997;McCormick, 1999;Beierlein et al, 2000;Tamas et al, 2000;Whittington et al, 2000;Klausberger et al, 2003;Pouille and Scanziani, 2004;Mann et al, 2005), the influence of feedback inhibition on the entrainment of STN neuronal activity neurons by rhythmic sequences of excitation was assessed.…”

Section: Ipsps Enhance Epsp-ap Couplingmentioning

confidence: 99%

Enhancement of Excitatory Synaptic Integration by GABAergic Inhibition in the Subthalamic Nucleus

Baufreton¹,

Atherton²,

Surmeier³

et al. 2005

J. Neurosci.

155

143

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The activity patterns of subthalamic nucleus (STN) neurons, which are intimately related to normal movement and abnormal movement in Parkinson's disease (PD), are sculpted by feedback GABAergic inhibition from the reciprocally connected globus pallidus (GP). To understand the principles underlying the integration of GABAergic inputs, we used gramicidin-based patch-clamp recording of STN neurons in rat brain slices. Voltage-dependent Na ϩ (Na v ) channels actively truncated synthetic IPSPs and were required for autonomous activity. In contrast, hyperpolarization-activated cyclic nucleotide-gated and class 3 voltage-dependent Ca 2ϩ channels contributed minimally to the integration of single or low-frequency trains of IPSPs and autonomous activity. Interestingly, IPSPs modified action potentials (APs) in a manner that suggested IPSPs enhanced postsynaptic Na v channel availability. This possibility was confirmed in acutely isolated STN neurons using current-clamp recordings containing IPSPs as voltage-clamp waveforms. Tetrodotoxin-sensitive subthreshold and spike-associated Na ϩ currents declined during autonomous spiking but were indeed transiently boosted after IPSPs. A functional consequence of inhibition-dependent augmentation of postsynaptic excitability was that EPSP-AP coupling was dramatically improved when IPSPs preceded EPSPs.Because STN neuronal activity exhibits coherence with cortical ␤-oscillations in PD, we tested how rhythmic sequences of cortical EPSPs were integrated in the absence and presence of feedback inhibition. STN neuronal activity was consistently entrained by EPSPs only in the presence of feedback inhibition. These observations suggest that feedback inhibition from the GP is critical for the emergence of coherent ␤-oscillations between the cortex and STN in PD.

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Role of Ionotropic Glutamatergic and GABAergic Inputs on the Firing Activity of Neurons in the External Pallidum in Awake Monkeys

Cited by 156 publications

References 56 publications

Role of the Indirect Pathway of the Basal Ganglia in Perceptual Decision Making

Role of the Indirect Pathway of the Basal Ganglia in Perceptual Decision Making

GABAergic mechanisms for shaping transient visual responses in the mouse superior colliculus

Enhancement of Excitatory Synaptic Integration by GABAergic Inhibition in the Subthalamic Nucleus

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