Three Types of Neurochemical Projection from the Bed Nucleus of the Stria Terminalis to the Ventral Tegmental Area in Adult Mice

Kudo, Takeaki; Uchigashima, Motokazu; Miyazaki, Toru; Konno, Kohtarou; Yamasaki, Miwako; Yanagawa, Yuchio; Minami, Masabumi; Watanabe, Masahiko

doi:10.1523/jneurosci.4057-12.2012

Cited by 164 publications

(175 citation statements)

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“…Indeed, BNST-A contains a small group of glutamatergic cells interspersed among a dominant population of GABAergic neurons (Day et al 1999;Esclapez et al 1993;Hur and Zaborszky 2005;Kudo et al 2012;Poulin et al 2009;Sun and Cassell 1993). Moreover, BNST-A neurons express numerous peptides than can coexist in various combinations (Woodhams et al 1983).…”

Section: Morphological Correlates Of Electroresponsive Propertiesmentioning

confidence: 99%

Contrasting distribution of physiological cell types in different regions of the bed nucleus of the stria terminalis

Rodríguez-Sierra

Turesson

Paré

2013

Journal of Neurophysiology

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Rodríguez-Sierra OE, Turesson HK, Pare D. Contrasting distribution of physiological cell types in different regions of the bed nucleus of the stria terminalis. J Neurophysiol 110: 2037-2049. First published August 7, 2013 doi:10.1152/jn.00408.2013.-We characterized the electroresponsive and morphological properties of neurons in the bed nucleus of the stria terminalis (BNST). Previously, Rainnie and colleagues distinguished three cell types in the anterolateral region of BNST (BNST-AL): low-threshold bursting cells (LTB; type II) and regular spiking neurons that display time-dependent (RS; type I) or fast (fIR; type III) inward rectification in the hyperpolarizing direction (Hammack SE, Mania I, Rainnie DG. J Neurophysiol 98: 638 -56, 2007). We report that the same neuronal types exist in the anteromedial (AM) and anteroventral (AV) regions of BNST. In addition, we observed two hitherto unreported cell types: late-firing (LF) cells, only seen in BNST-AL, that display a conspicuous delay to firing, and spontaneously active (SA) neurons, only present in BNST-AV, firing continuously at rest. However, the feature that most clearly distinguished the three BNST regions was the incidence of LTB cells (approximately 40 -70%) and the strength of their bursting behavior (both higher in BNST-AM and AV relative to AL). The incidence of RS cells was similar in the three regions (ϳ25%), whereas that of fIR cells was higher in BNST-AL (ϳ25%) than AV or AM (Յ8%). With the use of biocytin, two dominant morphological cell classes were identified but they were not consistently related to particular physiological phenotypes. One neuronal class had highly branched and spiny dendrites; the second had longer but poorly branched and sparsely spiny dendrites. Both often exhibited dendritic varicosities. Since LTB cells prevail in BNST, it will be important to determine what inputs set their firing mode (tonic vs. bursting) and in what behavioral states.bed nucleus of the stria terminalis; anxiety; fear; intrinsic properties; morphology DESPITE ANATOMICAL SIMILARITIES (Alheid and Heimer 1988; deOlmos and Heimer 1999;McDonald 2003), dense interconnections (Krettek and Price 1978a,b; Dong et al. 2001a), and functional kinship (Walker et al. 2003) between the amygdala and bed nucleus of the stria terminalis (BNST), there is a stark contrast between our understanding of these two structures. For instance, numerous in vitro studies have examined the physiological properties of amygdala neurons, mechanisms of synaptic transmission, neuromodulation, and activity-dependent plasticity (reviewed in Sah et al. 2003;Pape and Pare 2010). In contrast, relatively few reports on these themes are available for the BNST (reviewed in McElligott and Winder 2009; Hammack et al. 2009). As a result, the operations carried out by the BNST remain poorly understood.

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Section: Morphological Correlates Of Electroresponsive Propertiesmentioning

confidence: 99%

Contrasting distribution of physiological cell types in different regions of the bed nucleus of the stria terminalis

Rodríguez-Sierra

Turesson

Paré

2013

Journal of Neurophysiology

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confidence: 99%

“…A majority of BNST cells are GABAergic/peptidergic and a minority (Day et al 1999;Poulin et al 2009;Kudo et al 2012). Given the pattern of results obtained in retrograde tracing studies (Day et al 1999;Herman et al 2004;Kudo et al 2012), it is likely that a large proportion of the GABAergic cells and at least some of the glutamatergic neurons are projection cells. Similarly, although electrophysiological studies have distinguished three main cell types in BNST-AL (Hammack et al 2007;Hazra et al 2011;Rodríguez-Sierra et al 2013), it remains unclear whether all or a subset of each class correspond to projection cells or interneurons.…”

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confidence: 99%

Neuronal correlates of fear conditioning in the bed nucleus of the stria terminalis

2013

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Lesion and inactivation studies indicate that the central amygdala (CeA) participates in the expression of cued and contextual fear, whereas the bed nucleus of the stria terminalis (BNST) is only involved in the latter. The basis for this functional dissociation is unclear because CeA and BNST form similar connections with the amygdala and brainstem fear effectors. To address this question, we recorded neurons in the anterolateral (AL) and anteromedial (AM) regions of BNST in rats subjected to auditory fear conditioning. During habituation, few neurons were responsive to the conditioned stimulus (CS). After fear conditioning, 20% of BNST-AL neurons developed inhibitory responses to the CS. In BNST-AM, 26% of neurons developed positive CS responses. The behavior of BNST-AM and -AL neurons during contextual fear paralleled their CS responsiveness: More BNST-AM neurons fired at higher rates during contextual freezing than movement, whereas the opposite was seen in BNST-AL cells. These findings point to regional differences in the activity of BNST-AL and -AM in relation to learned fear, raising the possibility that they exert opposite influences on fear output networks. However, given the similar behavior of BNST-AM and -AL neurons in relation to cued and contextual fear, it remains unclear why lesion and inactivation of BNST differentially affect these two types of fear. Either neurons in a different BNST sector, not explored here, show a different activity profile in relation to the two forms of fear or inactivation/ lesion studies inadvertently affected a structure adjacent to BNST, which is involved in contextual fear.

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“…Since, pharmacological inhibition of the BNST (but not the amygdala) by the GABA-A receptor agonist muscimol was shown to disrupt fear responses to TMT [32] [54], and since, increased anxiety levels were reported after inactivation of GABA synthesis within the BNST [59], it can be assumed that GABAergic mechanisms in the BNST are involved in TMT-induced innate fear responses. It was already shown that GABAergic BNST neurons can inhibit the HPA axis via direct projections to the PVN [58], and by the way of GABA-GABA disinhibitory connections [60], the amygdala is in a position to cause a stress-induced activation of the HPA axis. Since, stressful events, like the exposure to a predator odor, are able to activate GABAergic neurons within the BNST [61] a delivering of the BNST from the inhibitory GABAergic influence of the amygdala can be supposed.…”

Section: Discussionmentioning

confidence: 99%

2,5-Dihydro-2,4,5-Trimethylthiazoline (TMT)-Induced Neuronal Activation Pattern and Behavioral Fear Response in GAD67 Mice

Janitzky

Prellwitz²,

Schwegler

et al. 2015

JBBS

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The synthetic predator odor 2,5-dihydro-2,4,5-trimethylthiazoline (TMT) was used to induce innate fear in male GAD67 mice and behavioral changes were correlated with c-fos mRNA levels as marker for neuronal activation to reveal underlying activated fear circuits. Results show the same amount of increased freezing and decreased rearing and grooming behavior of TMT-exposed GAD67 mice and wild type littermates, and therefore suggest that heterozygous knock-in of GFP in the GAD67 gene that is associated with a fifty percent decreased GAD67 protein level in the brain, has no impact on TMT-induced behavioral effects. Exposure to TMT significantly increased the number of c-fos mRNA positive cells in the main olfactory bulb (MOB), the lateral septum (LS), the bed nucleus of the stria terminalis (BNST), the central amygdala (CeA), the anterior-ventral (MeAav), the anterior-dorsal (MeAad) and the posterior-ventral (MeApv) part of the medial amygdala in GAD67 mice. Thus, to further investigate the role of GABAergic neurons in TMT-induced uncontrollable stress responses GAD67 mice that provide the advantage of prelabeled GABAergic neurons through the GABA neuron specific expression of GFP could be a suitable model organism.

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Three Types of Neurochemical Projection from the Bed Nucleus of the Stria Terminalis to the Ventral Tegmental Area in Adult Mice

Cited by 164 publications

References 59 publications

Contrasting distribution of physiological cell types in different regions of the bed nucleus of the stria terminalis

Contrasting distribution of physiological cell types in different regions of the bed nucleus of the stria terminalis

Neuronal correlates of fear conditioning in the bed nucleus of the stria terminalis

2,5-Dihydro-2,4,5-Trimethylthiazoline (TMT)-Induced Neuronal Activation Pattern and Behavioral Fear Response in GAD67 Mice

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