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Weakly correlated activity of pallidal neurons in behaving monkeys.

ABSTRACT: The basal ganglia play a crucial role in the control of voluntary movements. Neurons in both the external and internal segments of the globus pallidus, the connecting and output nuclei of the basal ganglia, respectively, change their firing rates in relation to movements. Firing rate changes of movement-related neurons seem to convey signals for motor control. On the other hand, coincident spikes among neurons, that is, correlated activity, may also contribute to motor control. To address this issue, we first identified multiple pallidal neurons receiving inputs from the forelimb regions of the primary motor cortex and supplementary motor area, recorded neuronal activity of these neurons simultaneously, and analyzed their spike correlations while monkeys performed a hand-reaching task. Most (79%) pallidal neurons exhibited task-related firing rate changes, whereas only a small fraction (20%) showed significant but small and short correlated activity during the task performance. These results suggest that motor control signals are conveyed primarily by firing rate changes in the external and internal segments of the globus pallidus and that the contribution of correlated activity may play only a minor role in the healthy state.

SUBMITTER: Wongmassang W

PROVIDER: S-EPMC8247335 | biostudies-literature | 2021 Apr

REPOSITORIES: biostudies-literature

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Weakly correlated activity of pallidal neurons in behaving monkeys.

Wongmassang Woranan W Hasegawa Taku T Chiken Satomi S Nambu Atsushi A

The European journal of neuroscience 20200727 7

The basal ganglia play a crucial role in the control of voluntary movements. Neurons in both the external and internal segments of the globus pallidus, the connecting and output nuclei of the basal ganglia, respectively, change their firing rates in relation to movements. Firing rate changes of movement-related neurons seem to convey signals for motor control. On the other hand, coincident spikes among neurons, that is, correlated activity, may also contribute to motor control. To address this i ...[more]

PMID: 32649021

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Project description:BACKGROUND:The ability to appropriately integrate and respond to rewarding and aversive stimuli is essential for survival. The ventral pallidum (VP) plays a critical role in processing both rewarding and aversive stimuli. However, the VP is a heterogeneous structure, and how VP subpopulations integrate into larger reward networks to ultimately modulate these behaviors is not known. We identify a noncanonical population of glutamatergic VP neurons that play a unique role in responding to aversive stimuli and constraining inappropriate reward seeking. METHODS:Using neurochemical, genetic, and electrophysiological approaches, we characterized glutamatergic VP neurons (n = 4-8 mice/group). We performed patch clamp and in vivo electrophysiology recordings in the lateral habenula, rostromedial tegmental nucleus, and ventral tegmental area to determine the effect of glutamatergic VP neuron activation in these target regions (n = 6-10 mice/group). Finally, we selectively optogenetically stimulated glutamatergic VP neurons in a real-time place preference task and ablated these neurons using a virally expressed caspase to determine their necessity for reward seeking. RESULTS:Glutamatergic VP neurons exhibit little overlap with cholinergic or gamma-aminobutyric acidergic markers, the canonical VP subtypes, and exhibit distinct membrane properties. Glutamatergic VP neurons innervate and increase firing activity of the lateral habenula, rostromedial tegmental nucleus, and gamma-aminobutyric acidergic ventral tegmental area neurons. While nonselective optogenetic stimulation of the VP induced a robust place preference, selective activation of glutamatergic VP neurons induced a place avoidance. Viral ablation of glutamatergic VP neurons increased reward responding and abolished taste aversion to sucrose. CONCLUSIONS:Glutamatergic VP neurons constitute a noncanonical subpopulation of VP neurons. These glutamatergic VP neurons increase activity of the lateral habenula, rostromedial tegmental nucleus, and gamma-aminobutyric acidergic ventral tegmental area neurons and adaptively constrain reward seeking.

Project description:The external (GPe) and internal (GPi) segments of the primate globus pallidus receive dopamine (DA) axonal projections arising mainly from the substantia nigra pars compacta and this innervation is here described based on tyrosine hydroxylase (TH) immunohistochemical observations gathered in the squirrel monkey (Saimiri sciureus). At the light microscopic level, unbiased stereological quantification of TH positive (+) axon varicosities reveals a similar density of innervation in the GPe (0.19 ± 0.02 × 10(6) axon varicosities/mm(3) of tissue) and GPi (0.17 ± 0.01 × 10(6)), but regional variations occur in the anteroposterior and dorsoventral axes in both GPe and GPi and along the mediolateral plane in the GPe. Estimation of the neuronal population in the GPe (3.47 ± 0.15 × 10(3) neurons/mm(3)) and GPi (2.69 ± 0.18 × 10(6)) yields a mean ratio of, respectively, 28 ± 3 and 68 ± 15 TH+ axon varicosities/pallidal neuron. At the electron microscopic level, TH+ axon varicosities in the GPe appear significantly smaller than those in the GPi and very few TH+ axon varicosities are engaged in synaptic contacts in the GPe (17 ± 3%) and the GPi (15 ± 4%) compared to their unlabeled counterparts (77 ± 6 and 50 ± 12%, respectively). Genuine synaptic contacts made by TH+ axon varicosities in the GPe and GPi are of the symmetrical and asymmetrical type. Such synaptic contacts together with the presence of numerous synaptic vesicles in all TH+ axon varicosities observed in the GPe and GPi support the functionality of the DA pallidal innervation. By virtue of its predominantly volumic mode of action, DA appears to exert a key modulatory effect upon pallidal neurons in concert with the more direct GABAergic inhibitory and glutamatergic excitatory actions of the striatum and subthalamic nucleus. We argue that the DA pallidal innervation plays a major role in the functional organization of the primate basal ganglia under both normal and pathological conditions.

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Weakly correlated activity of pallidal neurons in behaving monkeys.

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Weakly correlated activity of pallidal neurons in behaving monkeys.

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