Probing striatal microcircuitry to understand the functional role of cholinergic interneurons

Girasole, Allison E; Nelson, Alexandra

doi:10.1002/mds.26340

Cited by 21 publications

(22 citation statements)

References 177 publications

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“…These results are compatible with the observed changes in the brain of PD patients, where the cholinergic tone was not decreased but was instead increased in the striatum (Girasole & Nelson, 2015). Our results are also compatible with the effect provoked by acute DA SNpc intoxication with 6‐hydroxydopamine over the striatal modulatory circuit.…”

Section: Discussionsupporting

confidence: 90%

“…The relevance of these neuronal populations on striatal function is highlighted by the alteration of distinct neuronal types in several neurological disorders, including chorea (MSN), parkinsonism (DA SNpc), Tourette syndrome (ACh and FS), and dystonia (ACh). Although it is well known that acute alteration of a specific striatal component induces changes in the other elements of the circuit (Girasole & Nelson, 2015; Salin et al, 2009), knowledge on how chronic loss of a particular cell type disturbs the whole circuit's homeostasis is scarce.…”

Section: Introductionmentioning

confidence: 99%

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Substantia nigra dopaminergic neurons and striatal interneurons are engaged in three parallel but interdependent postnatal neurotrophic circuits

Sanchez-Garcia

Nieto-González

García-Junco-Clemente

et al. 2018

Aging Cell

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The striatum integrates motor behavior using a well‐defined microcircuit whose individual components are independently affected in several neurological diseases. The glial cell line‐derived neurotrophic factor (GDNF), synthesized by striatal interneurons, and Sonic hedgehog (Shh), produced by the dopaminergic neurons of the substantia nigra (DA SNpc), are both involved in the nigrostriatal maintenance but the reciprocal neurotrophic relationships among these neurons are only partially understood. To define the postnatal neurotrophic connections among fast‐spiking GABAergic interneurons (FS), cholinergic interneurons (ACh), and DA SNpc, we used a genetically induced mouse model of postnatal DA SNpc neurodegeneration and separately eliminated Smoothened (Smo), the obligatory transducer of Shh signaling, in striatal interneurons. We show that FS postnatal survival relies on DA SNpc and is independent of Shh signaling. On the contrary, Shh signaling but not dopaminergic striatal innervation is required to maintain ACh in the postnatal striatum. ACh are required for DA SNpc survival in a GDNF‐independent manner. These data demonstrate the existence of three parallel but interdependent neurotrophic relationships between SN and striatal interneurons, partially defined by Shh and GDNF. The definition of these new neurotrophic interactions opens the search for new molecules involved in the striatal modulatory circuit maintenance with potential therapeutic value.

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Section: Discussionsupporting

confidence: 90%

Section: Introductionmentioning

confidence: 99%

Substantia nigra dopaminergic neurons and striatal interneurons are engaged in three parallel but interdependent postnatal neurotrophic circuits

Sanchez-Garcia

Nieto-González

García-Junco-Clemente

et al. 2018

Aging Cell

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“…These findings reveal a divergence of task-related somatic and presynaptic activity in both associative and sensorimotor projections during early action learning that is consistent with the occurrence of learning-related in vivo potentiation of presynaptic Ca 2+ -related corticostriatal function. Although many mechanisms could mediate this effect, including learning-related changes in striatal microcircuits that impinge on presynaptic corticostriatal function (Lovinger, 2010; Kupferschmidt & Lovinger, 2015; Girasole & Nelson, 2015; Logie et al, 2013; Blomeley et al, 2015), one particularly intriguing mechanism may involve training- induced presynaptic corticostriatal NMDA receptor-mediated Ca 2+ influx and plasticity. Indeed, corticostriatal inputs exhibit forms of synaptic potentiation following learning-related patterns of activity (DeCoteau et al, 2007; Tort et al, 2008) that are mediated by enhanced presynaptic Ca 2+ influx via NMDA receptors (Park et al, 2014), and are altered in ex vivo brain slices from rodents in early phases of procedural training (Hawes et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Parallel, but Dissociable, Processing in Discrete Corticostriatal Inputs Encodes Skill Learning

Kupferschmidt

Juczewski

Cui

et al. 2017

Neuron

184

189

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SUMMARY Changes in cortical and striatal function underlie the transition from novel actions to refined motor skills. How discrete, anatomically defined corticostriatal projections function in vivo to encode skill learning remains unclear. Using novel fiber photometry approaches to assess real-time activity of associative inputs from medial prefrontal cortex to dorsomedial striatum and sensorimotor inputs from motor cortex to dorsolateral striatum, we show that associative and sensorimotor inputs co-engage early in action learning, and disengage in a dissociable manner as actions are refined. Disengagement of associative, but not sensorimotor, inputs predicts individual differences in subsequent skill learning. Divergent somatic and presynaptic engagement in both projections during early action learning suggests potential learning-related in vivo modulation of presynaptic corticostriatal function. These findings reveal parallel processing within associative and sensorimotor circuits that challenges and refines existing views of corticostriatal function, and expose neuronal projection- and compartment-specific activity dynamics that encode and predict action learning.

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“…In spite of the comparative small number of ChIs (Lehmann et al, 1979;Bolam et al, 1984a;Bennett & Wilson, 1999;Bennett et al, 2000;Kreitzer, 2009;Girasole & Nelson, 2015), their long and many branched axons allow a widespread release of ACh (Bolam et al, 1984a;Contant et al, 1996;Calabresi et al, 2000). Initially, ChIs were described as homogeneously dispersed; however, in mice, a greater concentration of ChIs in the dorsomedial compared to ventrolateral areas was observed following a stereological reconstruction (Matamales et al, 2016).…”

Section: Anatomicalmentioning

confidence: 99%

Cholinergic modulation of striatal microcircuits

Abudukeyoumu

Hernández-Flores

García‐Muñoz

et al. 2018

Eur J of Neuroscience

106

107

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The purpose of this review is to bridge the gap between earlier literature on striatal cholinergic interneurons and mechanisms of microcircuit interaction demonstrated with the use of newly available tools. It is well known that the main source of the high level of acetylcholine in the striatum, compared to other brain regions, is the cholinergic interneurons. These interneurons provide an extensive local innervation that suggests they may be a key modulator of striatal microcircuits. Supporting this idea requires the consideration of functional properties of these interneurons, their influence on medium spiny neurons, other interneurons, and interactions with other synaptic regulators. Here, we underline the effects of intrastriatal and extrastriatal afferents onto cholinergic interneurons and discuss the activation of pre- and postsynaptic muscarinic and nicotinic receptors that participate in the modulation of intrastriatal neuronal interactions. We further address recent findings about corelease of other transmitters in cholinergic interneurons and actions of these interneurons in striosome and matrix compartments. In addition, we summarize recent evidence on acetylcholine-mediated striatal synaptic plasticity and propose roles for cholinergic interneurons in normal striatal physiology. A short examination of their role in neurological disorders such as Parkinson's, Huntington's, and Tourette's pathologies and dystonia is also included.

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Probing striatal microcircuitry to understand the functional role of cholinergic interneurons

Cited by 21 publications

References 177 publications

Substantia nigra dopaminergic neurons and striatal interneurons are engaged in three parallel but interdependent postnatal neurotrophic circuits

Substantia nigra dopaminergic neurons and striatal interneurons are engaged in three parallel but interdependent postnatal neurotrophic circuits

Parallel, but Dissociable, Processing in Discrete Corticostriatal Inputs Encodes Skill Learning

Cholinergic modulation of striatal microcircuits

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