scholarly journals Conservation of the direct and indirect pathways dichotomy in mouse caudal striatum with uneven distribution of dopamine receptor D1- and D2-expressing neurons

2021 ◽  
Author(s):  
Kumiko Ogata ◽  
Fuko Kadono ◽  
Yasuharu Hirai ◽  
Ken-ichi Inoue ◽  
Masahiko Takada ◽  
...  
Keyword(s):  
Substantia Nigra ◽  
Dopamine Receptor ◽  
Common Marmoset ◽  
Projection Neuron ◽  
Membrane Properties ◽  
Electrophysiological Recording ◽  
Projection Neurons ◽  
The Poor ◽  
Neural Tracing

The striatum is one of the key nuclei for adequate control of voluntary behaviors and reinforcement learning. Two striatal projection neuron types, expressing either dopamine receptor D1 (D1R) or dopamine receptor D2 (D2R) constitute two independent output routes: the direct or indirect pathways, respectively. These pathways co-work in balance to achieve coordinated behavior. Two projection neuron types are equivalently intermingled in most striatal space. However, recent studies revealed two atypical zones in the caudal striatum: the zone in which D1R-neurons are the minor population (D1R-poor zone) and that in which D2R-neurons are the minority (D2R-poor zone). It remains obscure as to whether these imbalanced zones have similar properties on axonal projections and electrophysiology to other striatal regions. Based on morphological experiments in mice using immunofluorescence, in situ hybridization, and neural tracing, here, we revealed the poor zones densely projected to the globus pallidus and substantia nigra pars lateralis, with a few collaterals in substantia nigra pars reticulata and compacta. As other striatal regions, D1R-neurons were the direct pathway neurons, while projection neurons in the poor zones possessed similar electrophysiological membrane properties to those in the conventional striatum using in vitro electrophysiological recording. In addition, the poor zones existed irrespective of the age of mice. We also identified the poor zones in the common marmoset as well as other rodents. These results suggest that the poor zones in the caudal striatum follow the conventional projection patterns irrespective of imbalanced distribution of projection neurons. The poor zones could be an innate structure and common in mammals and relate to specific functions via highly restricted projections.

Bursting in Substantia Nigra Pars Reticulata Neurons In Vitro: Possible Relevance for Parkinson Disease

2007 ◽  
Vol 98 (4) ◽  
pp. 2311-2323 ◽  
Author(s):  
Osvaldo Ibáñez-Sandoval ◽  
Luis Carrillo-Reid ◽  
Elvira Galarraga ◽  
Dagoberto Tapia ◽  
Ernesto Mendoza ◽  
...  
Keyword(s):  
Substantia Nigra ◽  
Parkinson Disease ◽  
Temporal Structure ◽  
Projection Neurons ◽  
Rate Model ◽  
Indirect Pathway ◽  
Bath Application ◽  
Pattern Generators ◽  
Oscillatory Model

Projection neurons of the substantia nigra reticulata (SNr) convey basal ganglia (BG) processing to thalamocortical and brain stem circuits responsible for movement. Two models try to explain pathological BG performance during Parkinson disease (PD): the rate model, which posits an overexcitation of SNr neurons due to hyperactivity in the indirect pathway and hypoactivity of the direct pathway, and the oscillatory model, which explains PD as the product of pathological pattern generators disclosed by dopamine reduction. These models are, apparently, incompatible. We tested the predictions of the rate model by increasing the excitatory drive and reducing the inhibition on SNr neurons in vitro. This was done pharmacologically with bath application of glutamate agonist N-methyl-d-aspartate and GABAA receptor blockers, respectively. Both maneuvers induced bursting behavior in SNr neurons. Therefore synaptic changes forecasted by the rate model induce the electrical behavior predicted by the oscillatory model. In addition, we found evidence that CaV3.2 Ca2+ channels are a critical step in generating the bursting firing pattern in SNr neurons. Other ion channels involved are: hyperpolarization-activated cation channels, high-voltage-activated Ca2+ channels, and Ca2+-activated K+ channels. However, although these channels shape the temporal structure of bursting, only CaV3.2 Ca2+ channels are indispensable for the initiation of the bursting pattern.

Opposite Functions of Histamine H1 and H2 Receptors and H3 Receptor in Substantia Nigra Pars Reticulata

2006 ◽  
Vol 96 (3) ◽  
pp. 1581-1591 ◽  
Author(s):  
Fu-Wen Zhou ◽  
Jian-Jun Xu ◽  
Yu Zhao ◽  
Mark S. LeDoux ◽  
Fu-Ming Zhou
Keyword(s):  
Basal Ganglia ◽  
Substantia Nigra ◽  
Inhibitory Neuron ◽  
Projection Neuron ◽  
Receptor Activation ◽  
Histamine Receptors ◽  
Receptor Expression ◽  
Substantia Nigra Pars Reticulata ◽  
Projection Neurons ◽  
Neuron Firing

The substantia nigra pars reticulata (SNr) is a key basal ganglia output nucleus. Inhibitory outputs from SNr are encoded in spike frequency and pattern of the inhibitory SNr projection neurons. SNr output intensity and pattern are often abnormal in movement disorders of basal ganglia origin. In Parkinson’s disease, histamine innervation and histamine H3 receptor expression in SNr may be increased. However, the functional consequences of these alterations are not known. In this study, whole cell patch-clamp recordings were used to elucidate the function of different histamine receptors in SNr. Histamine increased SNr inhibitory projection neuron firing frequency and thus inhibitory output. This effect was mediated by activation of histamine H1 and H2 receptors that induced inward currents and depolarization. In contrast, histamine H3 receptor activation hyperpolarized and inhibited SNr inhibitory projection neurons, thus decreasing the intensity of basal ganglia output. By the hyperpolarization, H3 receptor activation also increased the irregularity of the interspike intervals or changed the pattern of SNr inhibitory neuron firing. H3 receptor–mediated effects were normally dominated by those mediated by H1 and H2 receptors. Furthermore, endogenously released histamine provided a tonic, H1 and H2 receptor–mediated excitation that helped keep SNr inhibitory projection neurons sufficiently depolarized and spiking regularly. These results suggest that H1 and H2 receptors and H3 receptor exert opposite effects on SNr inhibitory projection neurons. Functional balance of these different histamine receptors may contribute to the proper intensity and pattern of basal ganglia output and, as a consequence, exert important effects on motor control.

scholarly journals Regulation of Action Potential Size and Excitability in Substantia Nigra Compacta Neurons: Sensitivity to 4-Aminopyridine

1999 ◽  
Vol 82 (6) ◽  
pp. 2903-2913 ◽  
Author(s):  
S. Nedergaard
Keyword(s):  
Substantia Nigra ◽  
Time Window ◽  
Slow Component ◽  
Brain Slices ◽  
Membrane Properties ◽  
Initial Time ◽  
Direct Excitation ◽  
Spontaneous Action ◽  
Intrinsic Membrane Properties

Slow, pacemaker-like firing is due to intrinsic membrane properties in substantia nigra compacta (SNc) neurons in vitro. How these properties interact with afferent synaptic inputs is not fully understood. In this study, intracellular recordings from SNc neurons in brain slices showed that spontaneous action potentials (APs) were attenuated when generated from lower than normal threshold. Such APs were blocked by 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) and could be related to non– N-methyl-d-aspartate (NMDA) receptor–mediated spontaneous excitatory postsynaptic potentials (EPSPs). The AP attenuation was reproduced by stimulus-evoked EPSPs and by current injections to the soma. APs evoked from holding potentials between −40 and −60 mV were reduced in width by Cd2+ (0.2 mM). Tetraethylammonium chloride (TEA, 10 mM) or 4-aminopyridine (4-AP, 5 mM) increased the AP width. However, at more negative holding potentials, Cd2+ and TEA were inefficacious, whereas 4-AP enlarged the AP, partly via induction of a Cd2+-sensitive component. A monophasic afterhyperpolarization (AHP), following attenuated APs, was little affected by either Cd2+ or TEA, but inhibited by 4-AP, which induced an additional, slow component, sensitive to Cd2+ or apamin (100 nM). The AP delay showed a discontinuous relation to the amplitude or slope of the injected current (delay shift), which was sensitive to low doses of 4-AP (0.05 mM). The initial time window before the delay shift was longer than the rise time of EPSPs. It is suggested that a 4-AP–sensitive current prevents or postpones discharge during slow depolarization's, but allows direct excitation by fast EPSPs. Fast excitation leads to AP attenuation, primarily due to strong activation of 4-AP–sensitive current. This seems to cause inhibition of the Ca2+ current during the AP and reduction of Ca2+-dependent K+ currents. Together, these properties are likely to influence the excitability and the local, somatodendritic effects of the AP, in a manner that discriminates between firing induced by the intrinsic pacemaker mechanism and fast synaptic potentials.

scholarly journals Developmental regulation of membrane excitability in rat spinal lamina I projection neurons

2012 ◽  
Vol 107 (10) ◽  
pp. 2604-2614 ◽  
Author(s):  
Jie Li ◽  
Mark L. Baccei
Keyword(s):  
Developmental Regulation ◽  
Retrograde Transport ◽  
Firing Frequency ◽  
Membrane Properties ◽  
Projection Neurons ◽  
Membrane Excitability ◽  
Lamina I ◽  
Age Dependent ◽  
Spinal Lamina

It is now universally recognized that neonates can experience considerable pain. While spinal lamina I neurons projecting to the brain contribute to the generation of hyperalgesia, nothing is known about their electrophysiological properties during early life. Here we have used in vitro whole cell patch-clamp recordings in rat spinal cord slices to determine whether the intrinsic membrane properties of lamina I projection neurons, as well as their synaptic inputs, are developmentally regulated during the early postnatal period. Projection neurons were identified via retrograde transport of DiI injected into the parabrachial nucleus (PB) or periaqueductal gray (PAG) and characterized at postnatal days (P)2–5, P10–12, P19–23, and P30–32. Both spino-PB and spino-PAG neurons demonstrated an age-dependent reduction in spike threshold and duration at room temperature, which was accompanied by a developmental increase in the frequency of miniature excitatory and inhibitory postsynaptic currents. Notably, in both groups, age-dependent changes in the passive membrane properties or rheobase only occurred after the third postnatal week. However, spontaneous activity was significantly more prevalent within the developing spino-PB population and was dominated by an irregular pattern of discharge. In addition, while the instantaneous firing frequency remained unaltered in spino-PB neurons during the first weeks of life, spino-PAG cells fired at a higher rate at P19–23 compared with younger groups, suggesting that the gain of parallel ascending nociceptive pathways may be independently regulated during development. Overall, these results demonstrate that intrinsic membrane excitability is modulated in a cell type-specific manner within developing spinal nociceptive circuits.

scholarly journals Gastric and pyloric motor pattern control by a modulatory projection neuron in the intact crab Cancer pagurus

2011 ◽  
Vol 105 (4) ◽  
pp. 1671-1680 ◽  
Author(s):  
Ulrike B. S. Hedrich ◽  
Florian Diehl ◽  
Wolfgang Stein
Keyword(s):  
Motor Activity ◽  
Motor Pattern ◽  
Central Pattern Generators ◽  
Projection Neuron ◽  
Firing Frequency ◽  
Projection Neurons ◽  
Cycle Period ◽  
Gastric Mill

Neuronal release of modulatory substances provides motor pattern generating circuits with a high degree of flexibility. In vitro studies have characterized the actions of modulatory projection neurons in great detail in the stomatogastric nervous system, a model system for neuromodulatory influences on central pattern generators. Less is known about the activities and actions of modulatory neurons in fully functional and richly modulated network settings, i.e., in intact animals. It is also unknown whether their activities contribute to the motor patterns in different behavioral conditions. Here, we show for the first time the activity and effects of the well-characterized modulatory projection neuron 1 (MCN1) in vivo and compare them to in vitro conditions. MCN1 was always spontaneously active, typically in a rhythmic fashion with its firing being interrupted by ascending inhibitions from the pyloric motor circuit. Its activity contributed to pyloric motor activity, because 1) the cycle period of the motor pattern correlated with MCN1 firing frequency and 2) stimulating MCN1 shortened the cycle period while 3) lesioning of the MCN1 axon reduced motor activity. In addition, gastric mill motor activity was elicited for the duration of the stimulation. Chemosensory stimulation of the antennae moved MCN1 away from baseline activity by increasing its firing frequency. Following this increase, a gastric mill rhythm was elicited and the pyloric cycle period decreased. Lesioning the MCN1 axon prevented these effects. Thus modulatory projection neurons such as MCN1 can control the motor output in vivo, and they participate in the processing of exteroceptive sensory information in behaviorally relevant conditions.

Activation of a Lobster Motor Rhythm-Generating Network by Disinhibition of Permissive Modulatory Inputs

1998 ◽  
Vol 80 (5) ◽  
pp. 2776-2780 ◽  
Author(s):  
Serge Faumont ◽  
John Simmers ◽  
Pierre Meyrand
Keyword(s):  
Nervous System ◽  
Projection Neuron ◽  
Projection Neurons ◽  
Synaptic Inhibition ◽  
Rhythm Generation ◽  
Stomatogastric Nervous System ◽  
Motor Network ◽  
Motor Rhythm ◽  
Chemical Synapses

Faumont, Serge, John Simmers, and Pierre Meyrand. Activation of a lobster motor rhythm-generating network by disinhibition of permissive modulatory inputs. J. Neurophysiol. 80: 2776–2780, 1998. Rhythm generation by the gastric motor network in the stomatogastric ganglion (STG) of the lobster Homarus gammarus is controlled by modulatory projection neurons from rostral commissural ganglia (CoGs); blocking action potential conduction in these inputs to the STG of a stomatogastric nervous system in vitro rapidly renders the gastric network silent. However, exposure of the CoGs to low Ca2+ saline to block chemical synapses activates a spontaneously silent gastric network or enhances an ongoing gastric rhythm. A similar permissive effect was observed when picrotoxin was also superfused on these ganglia. We conclude that in the CoGs continuous synaptic inhibition is exerted on modulatory projection neuron(s) and that release from this inhibition allows strong activation of the gastric network.

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