Serotonin Modulates Pallidal Neuronal Activity in the Awake Monkey

Kita, Hitoshi; Chiken, Satomi; Tachibana, Yoshihisa; Nambu, Atsushi

doi:10.1523/jneurosci.4058-06.2007

Cited by 41 publications

(37 citation statements)

References 49 publications

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“…Both modeling and experimental studies demonstrate that similar circuit function can result from a large variation in the synaptic and intrinsic conductances that contribute to circuit function (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11). This finding suggests that each individual could, during development, build a brain that differs significantly from all others and poses the question of whether circuits with diverse underlying structure, yet similar behavior, can respond reliably (12,13) to neuromodulatory substances that alter brain states (14)(15)(16)(17)(18)(19)(20)(21). Therefore, we used the dynamic clamp (22,23) to construct 2-cell circuits (24) from neurons of the crab stomatogastric ganglion (STG).…”

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confidence: 99%

Reliable neuromodulation from circuits with variable underlying structure

Grashow

Brookings

Marder

2009

Proc. Natl. Acad. Sci. U.S.A.

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Recent work argues that similar network performance can result from highly variable sets of network parameters, raising the question of whether neuromodulation can be reliable across individuals with networks with different sets of synaptic strengths and intrinsic membrane conductances. To address this question, we used the dynamic clamp to construct 2-cell reciprocally inhibitory networks from gastric mill (GM) neurons of the crab stomatogastric ganglion. When the strength of the artificial inhibitory synapses (gsyn) and the conductance of an artificial Ih (gh) were varied with the dynamic clamp, a variety of network behaviors resulted, including regions of stable alternating bursting. Maps of network output as a function of gsyn and gh were constructed in normal saline and again in the presence of serotonin or oxotremorine. Both serotonin and oxotremorine depolarize and excite isolated individual GM neurons, but by different cellular mechanisms. Serotonin and oxotremorine each increased the size of the parameter regions that supported alternating bursting, and, on average, increased burst frequency. Nonetheless, in both cases some parameter sets within the sample space deviated from the mean population response and decreased in frequency. These data provide insight into why pharmacological treatments that work in most individuals can generate anomalous actions in a few individuals, and they have implications for understanding the evolution of nervous systems. dynamic clamp ͉ evolution ͉ serotonin ͉ stomatogastric ganglion ͉ oscillator H ow different are the brains in a population of healthy individuals of the same species? Both modeling and experimental studies demonstrate that similar circuit function can result from a large variation in the synaptic and intrinsic conductances that contribute to circuit function (1-11). This finding suggests that each individual could, during development, build a brain that differs significantly from all others and poses the question of whether circuits with diverse underlying structure, yet similar behavior, can respond reliably (12, 13) to neuromodulatory substances that alter brain states (14-21). Therefore, we used the dynamic clamp (22, 23) to construct 2-cell circuits (24) from neurons of the crab stomatogastric ganglion (STG). The strength of the reciprocal inhibitory synapses (g syn ) and the conductance of an artificial I h (g h ) were varied (24), and the resulting activity patterns were recorded in control saline and in response to 2 neuromodulatory substances, serotonin and the muscarinic agonist, oxotremorine.In these hybrid experiments, the intrinsic properties of these 2 biological neurons vary between each other and across preparations while 2 of the important parameters for network performance are under experimental control. This method ensures that the variability intrinsic to biological systems is retained, while allowing access to some of the parameters controlling network performance. Results and DiscussionWe used gastric mill (GM) neurons of the STG of t...

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mentioning

confidence: 99%

Reliable neuromodulation from circuits with variable underlying structure

Grashow

Brookings

Marder

2009

Proc. Natl. Acad. Sci. U.S.A.

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“…5-HT suppressed GABAergic inhibitory responses to cortical stimulation in monkeys, through presynaptic 5-HT 1B receptors, densely expressed on axons and axon terminals in the pallidum (Kita et al, 2007). On the other hand, 5-HT 1A receptors are involved in the suppression of GLUergic excitations of the GP because local application of WAY 100635, a 5-HT 1A selective antagonist, blocked the effect of subsequent applications of 5-carboxamindotryptamine (5-CT) in suppressing cortical stimulation-induced excitations (Kita et al, 2007). Hence, 5-HT may reduce ionotropic GLUergic excitation, probably through 5-HT 1A receptors located at presynaptic and/or postsynaptic sites.…”

Section: -Ht Modulation Of Gp Activitymentioning

confidence: 98%

“…5-HT postsynaptic excitation of pallidal neurons occurs through activation of 5-HT 4 or 5-HT 7 receptors but not via 5-HT 2C and 5-HT 3 receptors (Bengtson et al, 2004;Kita et al, 2007;Chen et al, 2008;Hashimoto and Kita, 2008).…”

Section: -Ht Modulation Of Gp Activitymentioning

confidence: 98%

“…In reality, the effect of 5-HT is more complex because of the existence of various receptor subtypes on presynaptic and postsynaptic membranes in the pallidum. In fact, recent electrophysiological evidence has shown that 5-HT exerts strong modulation on inhibitory and excitatory responses to cortical stimulation in the GPe and the GPi (Kita et al, 2007;Hashimoto and Kita, 2008). 5-HT suppressed GABAergic inhibitory responses to cortical stimulation in monkeys, through presynaptic 5-HT 1B receptors, densely expressed on axons and axon terminals in the pallidum (Kita et al, 2007).…”

Section: -Ht Modulation Of Gp Activitymentioning

confidence: 99%

“…In fact, recent electrophysiological evidence has shown that 5-HT exerts strong modulation on inhibitory and excitatory responses to cortical stimulation in the GPe and the GPi (Kita et al, 2007;Hashimoto and Kita, 2008). 5-HT suppressed GABAergic inhibitory responses to cortical stimulation in monkeys, through presynaptic 5-HT 1B receptors, densely expressed on axons and axon terminals in the pallidum (Kita et al, 2007). On the other hand, 5-HT 1A receptors are involved in the suppression of GLUergic excitations of the GP because local application of WAY 100635, a 5-HT 1A selective antagonist, blocked the effect of subsequent applications of 5-carboxamindotryptamine (5-CT) in suppressing cortical stimulation-induced excitations (Kita et al, 2007).…”

Section: -Ht Modulation Of Gp Activitymentioning

confidence: 99%

See 2 more Smart Citations

Serotonin modulation of the basal ganglia circuitry: therapeutic implication for Parkinson's disease and other motor disorders

Matteo

Pierucci

Esposito

et al. 2008

Progress in Brain Research

133

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Several recent studies have emphasized a crucial role for the interactions between serotonergic and dopaminergic systems in movement control and the pathophysiology of basal ganglia. These observations are supported by anatomical evidence demonstrating large serotonergic innervation of all the basal ganglia nuclei. In fact, serotonergic terminals have been reported to make synaptic contacts with both substantia nigra dopamine-containing neurons and their terminal areas such as the striatum, the globus pallidus and the subthalamus. These brain areas contain a high concentration of serotonin (5-HT), with the substantia nigra pars reticulata receiving the greatest input. In this chapter, the distribution of different 5-HT receptor subtypes in the basal ganglia nuclei will be described. Furthermore, evidence demonstrating the serotonergic control of basal ganglia activity will be reviewed and the contribution of the different 5-HT receptor subtypes examined. The new avenues that the increasing knowledge of 5-HT in motor control has opened for exploring the pathophysiology and pharmacology of Parkinson's disease and other movement disorders will be discussed. It is clear that these avenues will be fruitful, despite the disappointing results so far obtained by clinical studies with selective 5-HT ligands. Nevertheless, these studies have led to a great increase in the attention given to the neurotransmitters of the basal ganglia and their connections.

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Non‐Dopaminergic Approaches to the Treatment of Parkinson's Disease

Fox

Brotchie

2011

Parkinson's Disease

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Serotonin Modulates Pallidal Neuronal Activity in the Awake Monkey

Cited by 41 publications

References 49 publications

Reliable neuromodulation from circuits with variable underlying structure

Reliable neuromodulation from circuits with variable underlying structure

Serotonin modulation of the basal ganglia circuitry: therapeutic implication for Parkinson's disease and other motor disorders

Non‐Dopaminergic Approaches to the Treatment of Parkinson's Disease

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