Substance P-Containing terminals in synaptic contact with cholinergic neurons in the neostriatum and basal forebrain: a double immunocytochemical study in the rat

Bolam, J. Paul; Ingham, C.A.; Izzo, P. N.; Levey, Aĺlan I.; Rye, David B.; Smith, A.D.; Wainer, Bruce H.

doi:10.1016/0006-8993(86)90629-3

Cited by 257 publications

(102 citation statements)

References 39 publications

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“…Reliance of striatal cholinergic survival on non-cell autonomous processes, involving for instance sonic hedgehog signaling from dopaminergic projections, was recently demonstrated in the adult brain (Gonzalez-Reyes et al, 2012). In our case, SP released by striatonigral MSNs might be a good candidate to support such pro-survival function as: (i) the presence of numerous SP positive axonal terminals making synaptic contact with dendrites of cholinergic neurons suggests an intimate relationship between these two populations (Bolam et al, 1986), (ii) SP biological functions are mediated by the NK1 receptor, which is almost exclusively expressed by cholinergic interneurons in the striatum (Elde et al, 1990;Gerfen, 1991), and (iii) NK1 receptor activation triggers pro-survival pathways crucial for the maintenance of some neuronal populations (Chu et al, 2011). The differential effects of DT in the striatum and nucleus accumbens open interesting questions and suggest that the cholinergic interneurons have distinct properties in each territory.…”

Section: Discussionmentioning

confidence: 83%

Cellular and Behavioral Outcomes of Dorsal Striatonigral Neuron Ablation: New Insights into Striatal Functions

Révy

Jaouen

Salin

et al. 2014

Neuropsychopharmacol

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The striatum is the input structure of the basal ganglia network that contains heterogeneous neuronal populations, including two populations of projecting neurons called the medium spiny neurons (MSNs), and different types of interneurons. We developed a transgenic mouse model enabling inducible ablation of the striatonigral MSNs constituting the direct pathway by expressing the human diphtheria toxin (DT) receptor under the control of the Slc35d3 gene promoter, a gene enriched in striatonigral MSNs. DT injection into the striatum triggered selective elimination of the majority of striatonigral MSNs. DT-mediated ablation of striatonigral MSNs caused selective loss of cholinergic interneurons in the dorsal striatum but not in the ventral striatum (nucleus accumbens), suggesting a regionspecific critical role of the direct pathway in striatal cholinergic neuron homeostasis. Mice with DT injection into the dorsal striatum showed altered basal and cocaine-induced locomotion and dramatic reduction of L-DOPA-induced dyskinesia in the parkinsonian condition. In addition, these mice exhibited reduced anxiety, revealing a role of the dorsal striatum in the modulation of behaviors involving an emotional component, behaviors generally associated with limbic structures. Altogether, these results highlight the implication of the direct striatonigral pathway in the regulation of heterogeneous functions from cell survival to regulation of motor and emotion-associated behaviors.

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Section: Discussionmentioning

confidence: 83%

Cellular and Behavioral Outcomes of Dorsal Striatonigral Neuron Ablation: New Insights into Striatal Functions

Révy

Jaouen

Salin

et al. 2014

Neuropsychopharmacol

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“…As for the GABA neurons that send inhibitory inputs to the cholinergic interneurons, a potential candidate is the medium spiny projection neuron, of which local axon collaterals were demonstrated by anatomical studies to make synaptic contacts with the cholinergic interneurons (Bolam et al, 1986;Kita, 1993). In addition, it has been extensively reported that this neuron type produces LTP under certain conditions (Calabresi et al, 1992(Calabresi et al, , 1996Wickens et al, 1996;Charpier and Deniau, 1997).…”

Section: Discussionmentioning

confidence: 99%

Dopamine-Dependent Synaptic Plasticity in the Striatal Cholinergic Interneurons

et al. 2001

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The striatum, the input stage of the basal ganglia, is a critical brain structure for the learning of stimulus-response habits as well as motor, perceptual, and cognitive skills. Roles of dopamine (DA) and acetylcholine (ACh) in this form of implicit memory have long been considered essential, but the underlying cellular mechanism is still unclear. By means of patch-clamp recordings from corticostriatal slices of the mouse, we studied whether the identified striatal cholinergic interneurons undergo long-term synaptic changes after tetanic stimulation of corticoand thalamostriatal fibers. Electrical stimulation of the fibers revealed a depolarizing and hyperpolarizing postsynaptic potential in the striatal cholinergic interneurons. The early depolarizing phase was considered to be a cortico/thalamostriatal glutamatergic EPSP, and the hyperpolarizing component was considered to be an intrastriatally evoked GABAergic IPSP. Tetanic stimulation of cortico/thalamostriatal fibers was found to induce simultaneously occurring long-term potentiation (LTP) of the EPSPs as well as the disynaptically mediated IPSPs. The induction of LTP of EPSP required a rise in intracellular Ca 2ϩ concentration and dopamine D 5 , but not D 2 receptor activation. Ca 2ϩ -permeable AMPA receptors might also play a part in the LTP induction. Blockade of NMDA receptors, metabotropic glutamate receptors, or serotonin receptors had no significant effects. The long-term enhancement of the disynaptic IPSPs was caused by a long-term increase in the occurrence rate but not the amplitude of disynaptically mediated IPSP in the striatal cholinergic interneurons. This dual mechanism of synaptic plasticity may be responsible for the long-term modulation of the cortico/thalamostriatal synaptic transmission.

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“…However, among these three, the major source of SP terminals is probably the striatonigral medium spiny neurons (Bolam et al, 1986). Although the striatal cholinergic neurons receive massive synaptic inputs from the thalamus (Lapper and Bolam, 1992), the SP-containing thalamostriatal projections may be very weak because it has been reported that all SP-immunoreactive axonal boutons form symmetrical synaptic specializations, whereas the striatal afferents from the cm-pf form synaptic contacts with asymmetrical membrane specializations (Bolam et al, 1983;Bolam and Izzo, 1988).…”

Section: Discussionmentioning

confidence: 99%

Actions of Substance P on Rat Neostriatal NeuronsIn Vitro

Aosaki

Kawaguchi

1996

J. Neurosci.

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Actions of substance P (SP) on the neostriatal neurons in in vitro rat slice preparations were studied via whole-cell patch-clamp recording. Almost all large aspiny neurons (cholinergic cells) and half of the low-threshold spike (LTS) cells (somatostatin/ NOS-positive cells) showed depolarization or an inward shift of the holding currents in response to bath-applied SP in a dosedependent manner. In contrast, no responses were observed in fast-spiking (FS) cells (parvalbumin-positive cells) and medium spiny cells. Spike discharges followed by slow EPSPs/EPSCs were evoked by intrastriatal electrical stimulation in the large aspiny neurons. Pretreatment with [D-Arg 1 ,D-Pro 2 ,DTrp 7,9 ,Leu 11 ]-SP, an antagonist of the SP receptor, reversibly suppressed the induction of the slow EPSPs/EPSCs and unmasked slow IPSCs. The SP-induced inward current, although almost unchanged even after the blockade of I h channels and voltage-dependent Na ϩ , Ca 2ϩ , and K ϩ channels, changed its amplitude according to the Na ϩ concentration used in both the large aspiny neurons and LTS cells. Thus, the cation current could account for virtually all of the inward current at resting levels in both neurons. These results suggest that the firing of afferent neurons such as striatonigral medium spiny neurons, one of the possible sources of SP, would increase the firing probability of the two types of interneurons of the neostriatum by SP-receptor-mediated opening of tetrodotoxin-insensitive cation channels.Key words: striatum; basal ganglia; cholinergic; somatostatin; interneurons; substance P; tachykinin; neuropeptide; cations; slice preparations; patch clampThe undecapeptide substance P (SP), one of the neuropeptides known as tachykinins, is thought to play an important role as a neurotransmitter/neuromodulator in the CNS (Otsuka and Yoshioka, 1993). Evidence suggests that SP-containing fiber terminals in the striatum originate from thalamocaudate neurons in the center median-parafascicular complex (Sugimoto et al., 1984). There are two distinct populations of SP-containing medium-sized neurons in the striatum: the striatonigral medium-sized spiny projection neurons (Hong et al., 1977; Brownstein et al., 1983;Gerfen and Young, 1988) and the medium-sized aspiny interneurons with indented nuclei (Bolam et al., 1983). The striatum has also been shown to contain three G-protein-coupled neurokinin receptor subtypes: NK1, NK2, and NK3, among which SP preferentially binds to the first. The NK1 receptor is not expressed, however, in the medium spiny neurons but, rather, in the somatostatinergic and large cholinergic interneurons of the striatum of the rat (Gerfen, 1991;Kaneko et al., 1993), as well as nonhuman primates and human (Aubry et al., 1994;Parent et al., 1995). Both cell types have been reported to have synapses on their somatodendritic trees at the SP-containing terminals (Bolam and Izzo, 1988). However, the cholinergic neurons are especially important because, although they represent only a small population in the striatum, their wi...

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Substance P-Containing terminals in synaptic contact with cholinergic neurons in the neostriatum and basal forebrain: a double immunocytochemical study in the rat

Cited by 257 publications

References 39 publications

Cellular and Behavioral Outcomes of Dorsal Striatonigral Neuron Ablation: New Insights into Striatal Functions

Cellular and Behavioral Outcomes of Dorsal Striatonigral Neuron Ablation: New Insights into Striatal Functions

Dopamine-Dependent Synaptic Plasticity in the Striatal Cholinergic Interneurons

Actions of Substance P on Rat Neostriatal NeuronsIn Vitro

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