Excessive Activation of Serotonin (5-HT) 1B Receptors Disrupts the Formation of Sensory Maps in Monoamine Oxidase A and 5-HT Transporter Knock-Out Mice

Salichon, Nathalie; Gaspar, Patrícia; Upton, Amy L.; Picaud, Sandrine; Hanoun, Naı̈ma; Hamon, Michel; Maeyer, Edward De; Murphy, Dennis L.; Mößner, Rainald; Lesch, Klaus‐Peter; Hen, René; Seif, Isabelle

doi:10.1523/jneurosci.21-03-00884.2001

Cited by 248 publications

(261 citation statements)

References 66 publications

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“…Therefore, it would be of interest to examine whether the thalamic feedback loop undergoes a critical period of plasticity as found in the S1 cortex (Crair and Malenka, 1995). We also found that the release of glutamate at the nVPM-to-nRT synapses is controlled by the 5-HT 1B Rs of the newborn mice, raising the possibility that the abnormal barrel field found with excessive levels of 5-HT (Cases et al, 1996;Salichon et al, 2001) may be associated with abnormal spindles in the newborn mice and anatomical changes in the thalamic neuronal circuits.…”

mentioning

confidence: 75%

“…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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mentioning

confidence: 75%

Section: Introductionmentioning

confidence: 99%

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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“…The MAOA KO mouse was selected as a model in which barrels are lacking in the cerebral cortex, despite a normal patterning of the subcortical sensory relays (Cases et al, 1995). In addition, MAOA KO mice in which 5-HT 1B receptors were genetically removed resulted in a normal segregation of somatosensory projections that results in a normal barrel field in the cortex (Salichon et al, 2001). As illustrated in Figure 6, cytochrome oxidase staining performed at P10 indicated that barrels could clearly be observed in wild-type C3H/HE and in double KO mice, whereas they were lacking in the MAOA KO mice (Fig.…”

Section: Shaping Of Astrocytic Network In Transgenic Mice With Modifmentioning

confidence: 99%

Gap Junction-Mediated Astrocytic Networks in the Mouse Barrel Cortex

Houades¹,

Koulakoff²,

Ezan³

et al. 2008

J. Neurosci.

184

161

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The barrel field of the somatosensory cortex constitutes a well documented example of anatomofunctional compartmentalization and activity-dependent interaction between neurons and astrocytes. In astrocytes, intercellular communication through gap junction channels composed by connexin 43 and 30 underlies a network organization. Immunohistochemical and electrophysiological experiments were undertaken to determine the coupling properties of astrocyte networks in layer IV of the developing barrel cortex. The expression of both connexins was found to be enriched within barrels compared with septa and other cortical layers. Combination of dye-coupling experiments performed with biocytin and immunostaining with specific cell markers demonstrated that astrocytic networks do not involve neurons, oligodendrocytes or NG2 cells. The shape of dye coupling was oval in the barrel cortex whereas it was circular in layer IV outside the barrel field. Two-dimensional analysis of these coupling areas indicated that gap junctional communication was restricted from a barrel to its neighbor. Such enrichment of connexin expression and transversal restriction were not observed in a transgenic mouse lacking the barrel organization, whereas they were both observed in a double-transgenic mouse with restored barrels. Direct observation of sulforhodamine B spread indicated that astrocytes located between two barrels were either weakly or not coupled, whereas coupling within a barrel was oriented toward its center. These observations indicated a preferential orientation of coupling inside the barrels resulting from subpopulations of astrocytes with different coupling properties that contribute to shaping astrocytic networks. Such properties confine intercellular communication in astrocytes within a defined barrel as previously reported for excitatory neuronal circuits.

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“…In rat, neonatal systemic depletion of the cortical serotonergic innervation delays thalamocortical patterning (Blue et al, 1991) and diminishes the size of the barrel field area during the first postnatal week (Bennett-Clarke et al, 1994). Interestingly, increased serotonin neurotransmission during the critical period also alters barrel field development (Vitalis et al, 1998;Boylan et al, 2000b;Salichon et al, 2001). The importance of serotonin in thalamocortical maturation is underscored by the transient expression of the high affinity serotonin uptake sites (SERTs), and the 5-HT1B receptor in thalamocortical afferents in the barrel field area during the first postnatal weeks (Bennett-Clarke et al, 1991;Bennett-Clarke et al, 1993;Bruning and Liangos, 1997;Hansson et al, 1998;Lebrand et al, 1998;Mansour-Robaey et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

Neonatal serotonin depletion alters behavioral responses to spatial change and novelty

et al. 2007

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Multiple brain disorders that show serotonergic imbalances have a developmental onset. Experimental models indicate a role for serotonin as a morphogen in brain development. To selectively study the effects of serotonin depletions on cortical structural development and subsequent behavior, we developed a mouse model in which a serotonin neurotoxin, 5,7-dihydroxytryptamine (5,7-DHT), is injected into the medial forebrain bundle (mfb) on the day of birth. Littermates with saline injections into the mfb and age matched mice served as controls. This study characterized the extent and duration of serotonergic denervation after the selective neonatal lesion and investigated effects on exploratory behavior, spatial learning and anxiety in mice of both sexes. We report significant decreases in the serotonergic (5-HT) innervation to cortex and hippocampus, but not to subcortical forebrain structures in 5,7-DHT-lesioned mice. The depletion of 5-HT fibers in cortical areas was long lasting in lesioned mice but autoradiographic binding to high affinity 5-HT transporters was only transiently reduced. Male but not female lesioned mice reduced their exploration significantly in response to spatial rearrangement and object novelty, suggesting increased anxiety in response to change but normal spatial cognition. Our data show that developmental disruptions in the serotonergic innervation of cortex and hippocampus are sufficient to induce permanent, sex specific, behavioral alterations. These results may have significant implications for understanding brain disorders presenting with cortical morphogenetic abnormalities and altered serotonin neurotransmission, such as autism, schizophrenia and affective disorders.

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Excessive Activation of Serotonin (5-HT) 1B Receptors Disrupts the Formation of Sensory Maps in Monoamine Oxidase A and 5-HT Transporter Knock-Out Mice

Cited by 248 publications

References 66 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

Gap Junction-Mediated Astrocytic Networks in the Mouse Barrel Cortex

Neonatal serotonin depletion alters behavioral responses to spatial change and novelty

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