Dendritic and axonal targeting of the vesicular acetylcholine transporter to membranous cytoplasmic organelles in laterodorsal and pedunculopontine tegmental nuclei

Garzón, Miguel; Pickel, Virginia M.

doi:10.1002/(sici)1096-9861(20000327)419:1<32::aid-cne2>3.0.co;2-o

Cited by 27 publications

(18 citation statements)

References 132 publications

(144 reference statements)

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“…However, the present observation of 25% symmetric synapses is inconsistent with prior reports within the ventral midbrain (Bolam et al, 1991;Garzon et al, 1999). Although some part of this discrepancy may reflect variation in the criteria used to identify synapse type, it is important to note that cholinergic axons forming symmetric synapses have been described in other targets of the brainstem tegmentum (Hallanger et al, 1990;Garzon and Pickel, 2000).…”

Section: Cholinergic Terminals Within the Vtacontrasting

confidence: 99%

“…Our finding of numerous VAChT-labeled unmyelinated axons and axon terminals forming predominantly asymmetric axo-dendritic synapses within the VTA supports previous reports of cholinergic innervation to this and adjacent brain regions (Hallanger et al, 1990;Bolam et al, 1991;Garzon et al, 1999;Garzon and Pickel, 2000). However, the present observation of 25% symmetric synapses is inconsistent with prior reports within the ventral midbrain (Bolam et al, 1991;Garzon et al, 1999).…”

Section: Cholinergic Terminals Within the Vtacontrasting

confidence: 70%

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Cholinergic axons in the rat ventral tegmental area synapse preferentially onto mesoaccumbens dopamine neurons

Omelchenko

Sesack

2005

J of Comparative Neurology

117

112

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Cholinergic afferents to the ventral tegmental area (VTA) contribute substantially to the regulation of motivated behaviors and the rewarding properties of nicotine. These actions are believed to involve connections with dopamine (DA) neurons projecting to the nucleus accumbens (NAc). However, this direct synaptic link has never been investigated, nor is it known whether cholinergic inputs innervate other populations of DA and GABA neurons, including those projecting to the prefrontal cortex (PFC). We addressed these questions using electron microscopic analysis of retrograde tract-tracing and immunocytochemistry for the vesicular acetylcholine transporter (VAChT) and for tyrosine hydroxylase (TH) and GABA. In tissue labeled for TH, VAChT+ terminals frequently synapsed onto DA mesoaccumbens neurons but only seldom contacted DA mesoprefrontal cells. In tissue labeled for GABA, one third of VAChT+ terminals innervated GABA-labeled dendrites, including both mesoaccumbens and mesoprefrontal populations. VAChT+ synapses onto DA and mesoaccumbens neurons were more commonly of the asymmetric (presumed excitatory) morphological type, whereas VAChT+ synapses onto GABA cells were more frequently symmetric (presumed inhibitory or modulatory). These findings suggest that cholinergic inputs to the VTA mediate complex synaptic actions, with a major portion of this effect likely to involve an excitatory influence on DA mesoaccumbens neurons. As such, the results suggest that natural and drug rewards operating through cholinergic afferents to the VTA have a direct synaptic link to the mesoaccumbens DA neurons that modulate approach behaviors. Keywordsdopamine; GABA; acetylcholine; nucleus accumbens; prefrontal cortex; ultrastructure Cholinergic projections to the substantia nigra and ventral tegmental area (VTA) derive mainly from the pedunculopontine (PPT) and laterodorsal (LDT) tegmentum (Woolf and Butcher, 1986;Hallanger and Wainer, 1988;Lavoie and Parent, 1994;Oakman et al., 1995;Forster and Blaha, 2000) and provide an important substrate for the reinforcing properties of nicotine and the pathophysiology of addiction as well as mental disorders such as schizophrenia (Nisell et al., 1994;Yeomans, 1995;Nestler, 2001;Corrigall et al., 2002;Mansvelder and McGehee, 2002;Dani, 2003). Within the VTA, acetylcholine and agonists of nicotinic and muscarinic receptors typically increase the activity of dopamine (DA) and GABA cells, promote bursting, and phasically increase efflux in terminal regions (Corrigall et al., 1994;Nisell et al., 1994;Westerink et al., 1996;Westerink et al., 1998;Forster and Blaha, 2000;Gronier et al., 2000;Yin and French, 2000 Burst firing in DA neurons provides an important physiological mechanism for signaling behaviorally relevant events and enhancing DA release in target areas (Suaud-Chagny et al., 1992;Schultz et al., 1997;Paladini and Tepper, 1999;Redgrave et al., 1999). Hence, cholinergic inputs from the mesopontine tegmentum may provide an important source of salience information for DA neuron...

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Section: Cholinergic Terminals Within the Vtacontrasting

confidence: 99%

Section: Cholinergic Terminals Within the Vtacontrasting

confidence: 70%

Cholinergic axons in the rat ventral tegmental area synapse preferentially onto mesoaccumbens dopamine neurons

Omelchenko

Sesack

2005

J of Comparative Neurology

117

112

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“…The analysis of the roundness and area of the synaptic vesicles in the terminals indicated that VNTB‐labeled buttons were clearly distinguishable from other types of endings that were found unlabeled with BDA. Furthermore, they shared similar ultrastructural characteristics with cholinergic endings in the cochlear nucleus (Yao and Godfrey,1999), and in nuclei involved in the mediation of the PPI, such as the pedunculopontine and laterodorsal tegmental nuclei (Garzón and Pickel,2000; Fendt et al,2001). We distinguished two types of unlabeled endings on the cell body of CRNs that differed from the VNTB endings.…”

Section: Discussionmentioning

confidence: 83%

Cholinergic input from the ventral nucleus of the trapezoid body to cochlear root neurons in rats

Gómez-Nieto

Rubio

López

2007

J of Comparative Neurology

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Brain stem pathways are essential for the modulation of the acoustic startle reflex by sounds; nevertheless, the neural circuits that convey fast auditory information to the primary acoustic startle circuit are still unclear. In the rat, cochlear root neurons (CRNs) comprise the first component of the primary acoustic startle circuit and are critical in the initiation and full expression of the acoustic startle reflex. To determine whether CRNs receive auditory descending inputs, we developed tract-tracing studies combined with immunohistochemistry, electron microscopy, morphometry, and confocal microscopy. Either FluoroGold or biotinylated dextran amine (BDA) injections in CRNs showed retrogradely labeled neurons in the ventral nucleus of the trapezoid body (VNTB). We verified the projection to CRNs by injecting BDA into the VNTB. Our results showed that neurons from VNTB project bilaterally and directly to CRNs, giving off numerous endings onto cell bodies and preferentially dendrites of CRNs. Electron microscopy analysis of labeled VNTB terminals demonstrated that they made multiple symmetric synapses and contained small round vesicles. Colocalization of the vesicular acetylcholine transporter and fluorescein dextran after injection in the VNTB indicated that these terminals use acetylcholine as neurotransmitter. We also revealed that the inferior colliculus, an important nucleus mediating the auditory prepulse inhibition, projects to VNTB neurons that innervate CRNs. Our data show a novel and short descending auditory pathway from the VNTB to the first nucleus of the primary acoustic startle circuit that might play an important role in the auditory prepulse inhibition of the startle reflex elicited by sounds.

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“…This antiserum shows a specific band at the predicted 70 kDa molecular weight in Western blots of tissue (Brunelli et al, 2005). The VAChT antiserum has been used extensively in electron microscopy studies in the rat to identify cholinergic processes (Garzón and Pickel, 2000, Pickel et al, 2000, Svingos et al, 2001, Towart et al, 2003, Kaplan et al, 2004). …”

Section: Methodsmentioning

confidence: 99%

Spatial and intracellular relationships between the α7 nicotinic acetylcholine receptor and the vesicular acetylcholine transporter in the prefrontal cortex of rat and mouse

et al. 2009

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The alpha-7 subunit of the nicotinic acetylcholine receptor (α7nAChR) is expressed in the prefrontal cortex (PFC), a brain region where these receptors are implicated in cognitive function and in the pathophysiology of schizophrenia. Activation of this receptor is dependent on release of acetylcholine (ACh) from axon terminals that contain the vesicular acetylcholine transporter (VAChT). Since rat and mouse models are widely used for studies of specific abnormalities in schizophrenia, we sought to determine the subcellular location of the α7nAChR with respect to VAChT storage vesicles in axon terminals in the PFC in both species. For this, we used dual electron microscopic immunogold and immunoperoxidase labeling of antisera raised against the α7nAChR and VAChT. In both species, the α7nAChR-immunoreactivity (-ir) was principally identified within dendrites and dendritic spines, receptive to axon terminals forming asymmetric excitatory-type synapses, but lacking detectable α7nAChR or VAChT-ir. Quantitative analysis of the rat PFC revealed that of α7nAChR labeled neuronal profiles, 65% (299/463) were postsynaptic structures (dendrites and dendritic spine) and only 22% (104/463) were axon terminals or small unmyelinated axons. In contrast, VAChT was principally localized to varicose vesicle-filled axonal profiles, without recognized synaptic specializations (n = 240). Of the α7nAChR-labeled axons, 47% (37/79) also contained VAChT, suggesting that ACh release is autoregulated through the presynaptic α7nAChR. The VAChT-labeled terminals rarely formed synapses, but frequently apposed α7nAChR-containing neuronal profiles. These results suggest that in rodent PFC, the α7nAChR plays a major role in modulation of the postsynaptic excitation in spiny dendrites in contact with VAChT containing axons.

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Dendritic and axonal targeting of the vesicular acetylcholine transporter to membranous cytoplasmic organelles in laterodorsal and pedunculopontine tegmental nuclei

Cited by 27 publications

References 132 publications

Cholinergic axons in the rat ventral tegmental area synapse preferentially onto mesoaccumbens dopamine neurons

Cholinergic axons in the rat ventral tegmental area synapse preferentially onto mesoaccumbens dopamine neurons

Cholinergic input from the ventral nucleus of the trapezoid body to cochlear root neurons in rats

Spatial and intracellular relationships between the α7 nicotinic acetylcholine receptor and the vesicular acetylcholine transporter in the prefrontal cortex of rat and mouse

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