Activity-Dependent Presynaptic Effect of Serotonin 1B Receptors on the Somatosensory Thalamocortical Transmission in Neonatal Mice

Laurent, Alban; Goaillard, Jean-Marc; Cases, Olivier; Lebrand, Cécile; Gaspar, Patrícia; Ropert, Nicole

doi:10.1523/jneurosci.22-03-00886.2002

Cited by 111 publications

(118 citation statements)

References 78 publications

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“…Conversely, the agonist CP93129 (100 nM, 4 min), which was tested on large (Ͼ200 pA) nVPMevoked minimal EPSCs, systematically (in five of five) mimicked the inhibitory effect of 5-HT, reducing the amplitude of the EPSCs by 31.9 Ϯ 4.9%, and changing significantly the PPR from 0.96 Ϯ 0.08 in control to 1.25 Ϯ 0.13 in CP93129 ( p Ͻ 0.05) (data not shown). In agreement with the previous demonstration of a lack of expression of 5-HT 1B Rs in the nVPM of older mice (Laurent et al, 2002), we found no effect of 5-HT (20 M, 4 min) on the large (Ͼ200 pA; n ϭ 5) nVPM-evoked EPSCs recorded in the nRT between P18 and P24 (Fig. 5C).…”

Section: Nvpm-to-nrt Excitatory Synapses Express Functional 5-ht 1b Rsupporting

confidence: 93%

“…The lack of effect of 20 M 5-HT could not simply be attributed to our inability to detect an effect on smaller-amplitude EPSCs for two reasons. First, we also already demonstrated an inhibitory effect of 5-HT on small (ϳ50 pA) TC EPSCs recorded in the S1 cortex (Laurent et al, 2002). Second, a significant inhibitory effect of 5-HT was also seen on smaller (195.1 Ϯ 47.9; n ϭ 27) nVPM-to-nRT EPSCs recorded in younger (P1-P6) mice (Fig.…”

Section: Nvpm-to-nrt Excitatory Synapses Express Functional 5-ht 1b Rsupporting

confidence: 64%

“…We have shown earlier that during the first postnatal week the nVPM neurons express transiently 5-HT 1B R mRNA and that 5-HT 1B R activation reduces the release of glutamate at the TC synapse in the L4 barrel cortex (Laurent et al, 2002). We decided to study the effect of 5-HT on the nVPM-evoked EPSCs for two reasons.…”

Section: Nvpm-to-nrt Excitatory Synapses Express Functional 5-ht 1b Rmentioning

confidence: 99%

“…The cortical NMDARs that mediate Hebbian plasticity at the thalamocortical (TC) synapses (Crair and Malenka, 1995;Feldman et al, 1998;Lu et al, 2001) control the differentiation of cortical spiny stellate neurons and the clustering of the TC axonal arbors (Iwasato et al, 2000;Datwani et al, 2002b;Lee et al, 2005). The presynaptic 5-HT 1B receptors (5-HT 1B Rs) that inhibit glutamate release at the TC synapse (Laurent et al, 2002) control also barrel development (Cases et al, 1996;Salichon et al, 2001). However, several cortex-specific genetic modifications have no effect on the closure of the critical period (Lu et al, 2001;Datwani et al, 2002a;Rebsam et al, 2005;Inan et al, 2006;Iwasato et al, 2008) and the TC axon clustering (Iwasato et al, 2000;Hannan et al, 2001;Inan et al, 2006;Watson et al, 2006), suggesting that still unknown changes occur in the thalamus.…”

Section: Introductionmentioning

confidence: 99%

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Early Development of the Thalamic Inhibitory Feedback Loop in the Primary Somatosensory System of the Newborn Mice

Evrard¹,

Ropert²

2009

J. Neurosci.

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Spontaneous neuronal activity plays an important role during the final development of the brain circuits and the formation of the primary sensory maps. In young rats, spindle bursts have been recorded in the primary somatosensory cortex. They are correlated with spontaneous muscle twitches and occur before active whisking. They bear similarities with the spindles recorded in adult brain that occur during early stages of sleep and rely on a thalamic feedback loop between the glutamatergic nucleus ventroposterior medialis (nVPM) and the GABAergic nucleus reticularis thalami (nRT). However, whether a functional nVPM-nRT loop exists in newborn rodents is unknown. We studied the reciprocal synaptic connections between nVPM and nRT in thalamic acute slices from mice from birth [postnatal day 0 (P0)] until P9. We first demonstrated that nVPM-to-nRT EPSCs could be distinguished from corticothalamic EPSCs by their inhibition by 5-HT attributable to the transient expression of functional presynaptic serotonin 1B receptors. The nVPM-to-nRT EPSCs and nRT-to-nVPMIPSCs were both detected the first day after birth; their amplitude near 2 nS was relatively stable until P5. At P6 -P7, there was a rapid and simultaneous increase of both nVPM-to-nRT EPSCs and nRT-to-nVPM IPSCs that reached 8 and 9 nS, respectively. Our results show that the thalamic synapses implicated in spindle activity are functional shortly after birth, suggesting that they could already generate spindles during the first postnatal week. Our results also suggest an inhibitory action of 5-HT on the spindle bursts of the newborn mice.

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Section: Nvpm-to-nrt Excitatory Synapses Express Functional 5-ht 1b Rsupporting

confidence: 93%

Section: Nvpm-to-nrt Excitatory Synapses Express Functional 5-ht 1b Rsupporting

confidence: 64%

Section: Nvpm-to-nrt Excitatory Synapses Express Functional 5-ht 1b Rmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Early Development of the Thalamic Inhibitory Feedback Loop in the Primary Somatosensory System of the Newborn Mice

Evrard¹,

Ropert²

2009

J. Neurosci.

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“…In recent years, several mutant mouse models lacking cortical barrels have began to unveil the cellular and molecular mechanisms by which these patterns emerge. Neural activity plays a crucial role in conferring presynaptic patterns to postsynaptic cells via neurotransmitter receptor-mediated intracellular signals (Erzurumlu and Kind, 2001;Laurent et al, 2002). MAOA KO have an excess level of brain serotonin, causing a lack of segregation of both thalamocortical and cortical neurons (Cases et al, 1996).…”

Section: Cux-1 and Cux-2 Expression In Mutants With An Altered Barrelmentioning

confidence: 99%

Expression of Cux‐1 and Cux‐2 in the developing somatosensory cortex of normal and barrel‐defective mice

et al. 2006

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Recently, two orthologues of the Drosophila homeobox Cut gene, Cux-1 and Cux-2, have been identified as restricted molecular markers of upper layer (II-IV) neurons in the murine cerebral cortex. We show that during early postnatal life, from P0 to P10, Cux-1 and Cux-2 mRNA are coexpressed in all primary sensory cortices. Antisera to Cux-1 and Cux-2 immunoreactivities preferentially label neurons in the barrel walls of the primary somatosensory cortex (S1). Subsequently, Cux-1 remains enriched in sensory cortices, whereas Cux-2 expression enlarges to comprise the frontal and insular areas. The laminar distribution of Cux-1 and Cux-2 differs: Cux-1 follows a layer IV to layer II decreasing gradient of expression, whereas Cux-2 expression is homogeneous across layers IV-II. No colocalization was found with GABA and birth dating experiments showed that Cux-1-positive neurons in layer IV are born during a restricted period, E13.5-E14.5, suggesting that Cux-1 is a useful molecular marker of the glutamatergic neurons of layer IV. We examined Cux-1 and Cux-2 in barrel-defective mouse strains, the VMAT2 KO, the MAOA KO, and the Adcyl 1 brl strain. A normal expression level of Cux-1 and Cux-2 was found in layer IV, despite the lack of segregation of the neurons as barrels. Conversely, in Reeler mice, Cux-1 and Cux-2 had a distinct laminar distribution: the Cux-1-positive neurons had an inverted deep localization, whereas the Cux-2-positive neurons were distributed throughout the cortical thickness, suggesting that Cux-2 expression is more widely expressed in the inverted cortex of reeler mutants. Our results indicate that Cux-1 is a useful marker of the layer IV neurons in S1, and that Cux-1 and Cux-2 are differently regulated in the upper layers of the cerebral cortex.

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Changing distribution of monoaminergic markers in the developing human cerebral cortex with special emphasis on the serotonin transporter

2002

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This article reviews the current knowledge of the early onset of the monoaminergic innervation in the developing cerebral cortex in humans and of changes in the distribution of tyrosine hydroxylase (TH) immunoreactivity in different neuronal populations of the developing telencephalon. The early genesis of the central monoaminergic neurons in mammals has led to postulations of a trophic role of monoamines in brain morphogenesis-especially in the cerebral cortex. The developmental effects of amines can be linked to the transient expression of different molecules linked to dopamine or serotonin neurotransmission. We present novel data on the immunocytochemistry of the vesicular monoamine transporter (VMAT2) and of the high-affinity serotonin transporter (SERT) in human fetuses. SERT is a marker of the serotoninergic axons and allows visualization of the serotonin afferents of the raphe in the human telencephalon. In addition, during a restricted time period corresponding to 12-14 postovulatory weeks, we found SERT-immunolabeled fibers in the rostral and caudal limbs of the internal capsule that do not correspond to serotoninergic fibers, but do coincide with the calbindin D28k-labeled thalamocortical fiber tracts. The present observations are correlated with findings in rodents, in which a transient expression of SERT is visible in the thalamocortical axons during early postnatal life. The function of this transporter has been shown to be important for the fine-tuning of cortical sensory maps during the critical period of development of these maps. Although the present observation does not allow ascertainment of which neurons transiently express SERT, it lends support to the notion that serotonin and serotonin uptake could have important developmental roles, during the formation of brain connections in humans, as they have in rodents. Anat The early genesis of the central monoaminergic neurons in mammals has repeatedly led to postulations of a trophic role of monoamines on brain morphogenesis-especially in the cerebral cortex. Recent studies in rodents have allowed substantiation of these assumptions and have demonstrated that such an effect does occur in vivo. Indeed, modifying the levels of amines in the brain-in particular that of serotonin (5HT)-during critical periods affects the normal development of the somatosensory and visual maps (Rhoades et al., 1993;Bennett-Clarke et al.,

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Activity-Dependent Presynaptic Effect of Serotonin 1B Receptors on the Somatosensory Thalamocortical Transmission in Neonatal Mice

Cited by 111 publications

References 78 publications

Early Development of the Thalamic Inhibitory Feedback Loop in the Primary Somatosensory System of the Newborn Mice

Early Development of the Thalamic Inhibitory Feedback Loop in the Primary Somatosensory System of the Newborn Mice

Expression of Cux‐1 and Cux‐2 in the developing somatosensory cortex of normal and barrel‐defective mice

Changing distribution of monoaminergic markers in the developing human cerebral cortex with special emphasis on the serotonin transporter

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