Possible glutamatergic/aspartatergic projections to the supramammillary nucleus and their origins in the rat studied by selective [3H]D-aspartate labelling and immunocytochemistry

Kiss, József Zoltán; Csáki, Ágnes; Bokor, Hajnalka; Kocsis, Krisztián; Kocsis, Bernát

doi:10.1016/s0306-4522(02)00037-4

Cited by 80 publications

(61 citation statements)

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“…Our results indicate that a separate population of LHb neurons also projects to histaminergic neurons in the hypothalamus. A projection from the LHb to the histaminergic tuberomammillary nucleus has also been demonstrated in rodents, but no direct projections to histaminergic neurons have been reported (58). In addition, anterogradely labeled fibers from the LHb have been shown to project to the hypothalamus in amphibians and mammals (58,59).…”

Section: Discussionmentioning

confidence: 99%

Evolutionary conservation of the habenular nuclei and their circuitry controlling the dopamine and 5-hydroxytryptophan (5-HT) systems

Stephenson-Jones

Floros

Robertson

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

129

153

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The medial (MHb) and lateral (LHb) habenulae are a small group of nuclei that regulate the activity of monoaminergic neurons. Disruptions to these nuclei lead to deficits in a range of cognitive and motor functions from sleep to decision making. Interestingly, the habenular nuclei are present in all vertebrates, suggesting that they provide a common neural mechanism to influence these diverse functions. To unravel conserved habenula circuitry and approach an understanding of their basic function, we investigated the organization of these nuclei in the lamprey, one of the phylogenetically oldest vertebrates. Based on connectivity and molecular expression, we show that the MHb and LHb circuitry is conserved in the lamprey. As in mammals, separate populations of neurons in the LHb homolog project directly or indirectly to dopamine and serotonin neurons through a nucleus homologous to the GABAergic rostromedial mesopontine tegmental nucleus and directly to histamine neurons. The pallidal and hypothalamic inputs to the LHb homolog are also conserved. In contrast to other species, the habenula projecting pallidal nucleus is topographically distinct from the dorsal pallidum, the homolog of the globus pallidus interna. The efferents of the MHb homolog selectively target the interpeduncular nucleus. The MHb afferents arise from sensory (medial olfactory bulb, parapineal, and pretectum) and not limbic areas, as they do in mammals; consequently, the "context" in which this circuitry is recruited may have changed during evolution. Our results indicate that the habenular nuclei provide a common vertebrate circuitry to adapt behavior in response to rewards, stress, and other motivating factors.basal ganglia | neuromodulator T he habenular complex, a small group of nuclei in the epithalamus, links the limbic forebrain to mid-and hind-brain regions involved in adapting the internal cerebral state (1-4). Lesion and genetic inactivation studies have implicated the habenula in a range of functions from control of the circadian rhythm to adapting the behavioral response to fear and reward, as well as to higher cognitive functions, such as attention and value-based decision making (5-8). The habenula is present in all classes of vertebrates, including those that seemingly lack highlevel cognitive functions (9). This suggests that it regulates processes crucial to survival through a basic neural mechanism common to all vertebrates. To unravel the neural basis for the habenula's basic and complex functions, it will be important to elucidate the basic circuitry and determine how this has evolved to regulate higher cognitive functions.In mammals, the habenula is subdivided into two nuclei: the medial habenula (MHb) and lateral habenula (LHb) (10). The LHb receives value-related signals from the basal ganglia [globus pallidus interna/entopeduncular nucleus (GPi/EP)] as well as inputs from the diagonal band of Broca and the lateral hypothalamus (1, 11). The LHb projects to the GABAergic rostromedial mesopontine tegmental nucleus (RMTg), a...

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Section: Discussionmentioning

confidence: 99%

Evolutionary conservation of the habenular nuclei and their circuitry controlling the dopamine and 5-hydroxytryptophan (5-HT) systems

Stephenson-Jones

Floros

Robertson

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

129

153

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“…Thus, 93% of the ChAT-positive neurons within the MS-DBB receive contacts from at least one vesicular glutamate transporter 2-containing bouton (Hajszan et al, 2004). This glutamatergic innervation has both extrinsic and intrinsic origins (Csaki et al, 2000Fremeau et al, 2001;Manns et al, 2001;Kiss et al, 2002;Lin et al, 2003;Hajszan et al, 2004). Because the projections of individual septohippocampal neurons are topographically organized with relatively small terminal fields (Ͻ1-1.5 mm in diameter) (Price and Stern, 1983), lateral interconnectivity within the MS-DBB mediated by glutamate could provide a mechanism for rapid radiation of excitation within the hippocampus.…”

Section: Discussionmentioning

confidence: 99%

Simultaneous Release of Glutamate and Acetylcholine from Single Magnocellular “Cholinergic” Basal Forebrain Neurons

2006

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Basal forebrain (BF) neurons provide the principal cholinergic drive to the hippocampus and cortex. Their degeneration is associated with the cognitive defects of Alzheimer's disease. Immunohistochemical studies suggest that some of these neurons contain glutamate, so might also release it. To test this, we made microisland cultures of single BF neurons from 12-to 14-d-old rats. Over 1-8 weeks in culture, neuronal processes made autaptic connections onto the neuron. In 34 of 36 cells tested, a somatically generated action potential was followed by a short-latency EPSC that was blocked by 1 mM kynurenic acid, showing that they released glutamate. To test whether the same neuron also released acetylcholine, we placed a voltage-clamped rat myoball expressing nicotinic receptors in contact with a neurite. In six of six neurons tested, the glutamatergic EPSC was accompanied by a nicotinic (hexamethonium-sensitive) myoball current. Stimulation of the M 2 -muscarinic presynaptic receptors (characterized using tripitramine and pirenzepine) produced a parallel inhibition of autaptic glutamatergic and myoball nicotinic responses; metabotropic glutamate receptor stimulation produced similar but less consistent and weaker effects. Atropine enhanced the glutamatergic EPSCs during repetitive stimulation by 25 Ϯ 6%; the anti-cholinesterase neostigmine reduced the train EPSCs by 37 Ϯ 6%. Hence, synaptically released acetylcholine exerted a negative-feedback inhibition of coreleased glutamate. We conclude that most cholinergic basal forebrain neurons are capable of releasing glutamate as a cotransmitter and that the release of both transmitters is subject to simultaneous feedback inhibition by synaptically released acetylcholine. This has implications for BF neuron function and for the use of cholinesterase inhibitors in Alzheimer's disease.

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Section: Nih Public Accessmentioning

confidence: 99%

“…Experiments combining retrograde tracing with serotonin (5-HT) immunostaining have established that many nonserotonergic DRN neurons project extrinsically (Beitz et al, 1986;Ma et al, 1991;Petrov et al, 1992Petrov et al, , 1994 Van Bockstaele et al, 1993;Kirifides et al, 2001;Kim et al, 2004;Halberstadt and Balaban, 2006a). Nonserotonergic DRN projections are neurochemically heterogeneous, and may contain a number of transmitter substances, including glutamate (Schwarz and Schwarz, 1992;Kiss et al, 2002), dopamine (Pohle et al, 1984;Descarries et al, 1986;Yoshida et al, 1989;Stratford and Wirtshafter, 1990;Hasue and Shammah-Lagnado, 2002), GABA (Nanopoulos et al, 1982;Stamp and Semba, 1995;Ford et al, 1995;Jankowski and Sesack, 2002), nitric oxide (Xu and Hokfelt, 1997;Simpson et al, 2003), and neuropeptides such as vasoactive intestinal polypeptide (VIP) (Petit et al, 1995;Kozicz et al, 1998) and cholecystokinin Seroogy and Fallon, 1989).Although it is likely that non-5-HT DRN projections influence processing in target regions (Weiss and Pellet, 1982;Hajés-Korcsok and Sharp, 2002), very little is known about the anatomical organization of this pathway. Anterograde tracing studies with Phaseolus vulgaris leucoagglutinin (PHA-L) or biotinylated dextran amine (BDA) have demonstrated that regions of the basal forebrain are heavily targeted by DRN projections (Vertes, 1991;Sim and Joseph, 1993;Morin and Meyer-Bernstein, 1999), and retrograde tracing has confirmed that this projection arises, in part, from nonserotonergic neurons (Descarries et al, 1986;Semba et al, 1988;Stratford and Wirtshafter, 1990;…”

mentioning

confidence: 99%

Selective anterograde tracing of nonserotonergic projections from dorsal raphe nucleus to the basal forebrain and extended amygdala

Halberstadt

Balaban

2008

Journal of Chemical Neuroanatomy

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The dorsal raphe nucleus (DRN) contains both serotonergic and non-serotonergic projection neurons. Retrograde tracing studies have demonstrated that components of the basal forebrain and extended amygdala are targeted heavily by input from nonserotonergic DRN neurons. The object of this investigation was to examine the terminal distribution of nonserotonergic DRN projections in the basal forebrain and extended amygdala, using a technique that allows selective anterograde tracing of nonserotonergic DRN projections. To trace nonserotonergic DRN projections, animals were pretreated with nomifensine, desipramine and the serotonergic neurotoxin 5,7-dihydroxytryptamine (5,7-DHT), 7 days prior to placing an iontophoretic injection of biotinylated dextran amine (BDA) into the DRN. In animals treated with 5,7-DHT, numerous nonserotonergic BDA-labeled fibers ascended to the basal forebrain in the medial forebrain bundle system. Some of these labeled fibers crossed through the lateral hypothalamus, bed nucleus of the stria terminalis, and substantial innominata. These fibers entered the amygdala through the ansa peduncularis and ramified within the central and basolateral amygdaloid nuclei. Other fibers entered the diagonal band of Broca and formed a dense plexus of labeled fibers in the dorsal half of the intermediate portion of the lateral septal nucleus and the septohippocampal nucleus. These findings demonstrate that the basal forebrain and extended amygdala receive a dense projection from nonserotonergic DRN neurons. Given that the basal forebrain plays a critical role in processes such as motivation, affect, and behavioral control, these findings support the hypothesis that nonserotonergic DRN projections may exert substantial modulatory control over emotional and motivational functions. Keywords amygdala; bed nucleus; 5,7-dihydroxytryptamine; septal nuclei; biotinylated dextran amine; tyrosine hydroxylase It is well known that the dorsal raphe nucleus contains more than half of all the serotonergic neurons in the brain (Leger and Wiklund, 1982) and is a source of projections that terminate extensively throughout the central nervous system (Vertes, 1991;Sim and Joseph, 1993;Vertes and Kocsis, 1994;Morin and Meyer-Bernstein, 1999 Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. within dorsomedial (DRNdm), ventromedial (DRNvm), and lateral (DRNl) cell groups . It has been proposed that the activity of serotonergic DRN neurons plays an important role in the coordination of sensory processing and motor output with the sleep-wake-arousal cycle (Jacobs and Azmitia, 1992; Forn...

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Possible glutamatergic/aspartatergic projections to the supramammillary nucleus and their origins in the rat studied by selective [3H]D-aspartate labelling and immunocytochemistry

Cited by 80 publications

References 90 publications

Evolutionary conservation of the habenular nuclei and their circuitry controlling the dopamine and 5-hydroxytryptophan (5-HT) systems

Evolutionary conservation of the habenular nuclei and their circuitry controlling the dopamine and 5-hydroxytryptophan (5-HT) systems

Simultaneous Release of Glutamate and Acetylcholine from Single Magnocellular “Cholinergic” Basal Forebrain Neurons

Selective anterograde tracing of nonserotonergic projections from dorsal raphe nucleus to the basal forebrain and extended amygdala

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