On the origin of the dopaminergic innervation of the paraventricular thalamic nucleus

doi:10.1016/0304-3940(90)90513-9

Neuroscience Letters

Volume 115, Issue 1, 17 July 1990, Pages 33-36

https://doi.org/10.1016/0304-3940(90)90513-9 Get rights and content

Abstract

The origin of the dopaminergic innervation of the paraventricular thalamic nucleus was examined in the rat. Employing a combination of fluorescent retrograde tracing and immunofluorescence histochemistry for tyrosine hydroxylase, we found that this innervation predominantly takes origin from the mesencephalic A8 and A10 catecholamine cell groups.

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The paraventricular thalamic nucleus: A key hub of neural circuits underlying drug addiction
2019, Pharmacological Research
Drug addiction is a chronic relapsing brain disease characterized by compulsive, out-of-control drug use and the appearance of negative somatic and emotional consequences when drug access is prevented. The limited efficacy of treatment urges researchers toward a deeper understanding of the neural mechanism of drug addiction. Brain circuits that regulate reward and motivation are considered to be the neural substrate of drug addiction. An increasing body of literature indicates that the paraventricular thalamic nucleus (PVT) could serve as a key node in the neurocircuits that control goal-directed behaviors. In this review, we summarize the anatomical and functional evidence that the PVT regulates drug-related behaviors. The PVT receives extensive inputs from the brainstem and hypothalamus, and is reciprocally connected with the limbic system. Neurons in the PVT are recruited by drug exposure as well as cues and context associated with drug taking. Pathway-specific perturbation studies have begun to decipher the precise role of PVT circuits in drug-related behaviors. We also highlight recent findings about the involvement of neural plasticity of the PVT pathways in drug addiction and provide perspectives on future studies.
Pharmacological modulation of lateral habenular dopamine D2 receptors alters the anxiogenic response to cocaine in a runway model of drug self-administration
2016, Behavioural Brain Research
Cocaine has long been known to produce an initial “high” followed by an aversive/anxiogenic “crash”. While much is known about the neurobiology of cocaine’s positive/rewarding effects, the mechanisms that give rise to the drug’s negative/anxiogenic actions remain unclear. Recent research has implicated the lateral habenula (LHb) in the encoding of aversive events including the anxiogenic response to cocaine. Of particular interest in this regard are the reciprocal connections between the LHb and the ventral tegmental area (VTA). VTA-DA neurons innervate different subsets of LHb cells that in turn feedback upon and modulate VTA neuronal activity. Here we examined the impact of D2 receptor activation and inhibition on the anxiogenic response to cocaine using a runway model of self-administration that is sensitive to the dual and opposing effects of the drug. Male rats ran a straight alley for IV cocaine (1.0 mg/kg) following bilateral intra-LHb infusions of the D2 receptor antagonist, cis-flupenthixol (0, 7.5 or 15 μg/side) or the D2 agonist, sumanirole (0, 5 or 10 μg/side). Vehicle-pretreated controls developed approach-avoidance conflict behaviors about goal-box entry reflective of the dual positive and negative effects of cocaine. These behaviors were significantly diminished during LHb-D2 receptor antagonism and increased by the LHb D2 receptor agonist. These results demonstrate that activity at the D2 receptor in the lateral habenula serves to modulate the anxiogenic response to cocaine.
Limbic thalamus and state-dependent behavior: The paraventricular nucleus of the thalamic midline as a node in circadian timing and sleep/wake-regulatory networks
2015, Neuroscience and Biobehavioral Reviews
Citation Excerpt :
A distinctive feature of the subcortical input to the thalamic midline, and in particular to PVT, is also the large variety of chemically characterized fibers, documented in many species including non-human primates and humans. Thus, PVT receives a dense aminergic innervation from the brain stem: adrenergic innervation from the medulla oblongata (Otake and Ruggiero, 1995; Phillipson and Bohn, 1994), noradrenergic fibers from the locus coeruleus (Jones and Yang, 1985; Krout et al., 2002; Vogt et al., 2008), serotonergic innervation from the median and dorsal raphe (Cropper et al., 1984; de Medeiros Silva et al., 2014; Hsu and Price, 2009; Otake and Ruggiero, 1995; Vertes et al., 2010), dopaminergic fibers which derive primarily from cells of the periventricular and posterior hypothalamic areas (García-Cabezas et al., 2007, 2009; Hökfelt et al., 1976; Otake and Ruggiero, 1995; Takada et al., 1990). The aminergic innervation of PVT includes histaminergic fibers deriving from the tuberomammillary nucleus of the posterior hypothalamus (Airaksinen and Panula, 1988; Airaksinen et al., 1989; Jin et al., 2002; Panula et al., 1989).
The paraventricular thalamic nucleus (PVT), the main component of the dorsal thalamic midline, receives multiple inputs from the brain stem and hypothalamus, and targets the medial prefrontal cortex, nucleus accumbens and amygdala. PVT has been implicated in several functions, especially adaptation to chronic stress, addiction behaviors and reward, mood, emotion. We here focus on the wiring and neuronal properties linking PVT with circadian timing and sleep/wake regulation, and their behavioral implications. PVT is interconnected with the master circadian pacemaker, the hypothalamic suprachiasmatic nucleus, receives direct and indirect photic input, is densely innervated by orexinergic neurons which play a key role in arousal and state transitions. Endowed with prominent wake-related Fos expression which is suppressed by sleep, and with intrinsic neuronal properties showing a diurnal oscillation unique in the thalamus, PVT could represent a station of interaction of thalamic and hypothalamic sleep/wake-regulatory mechanisms. PVT could thus play a strategic task by funneling into limbic and limbic-related targets circadian timing and state-dependent behavior information, tailoring it for cognitive performance and motivated behaviors.
Neural mechanism underlying hyperalgesic response to orofacial pain in Parkinson's disease model rats
2015, Neuroscience Research
To investigate the neural mechanism of pain originating from the orofacial region in PD patients, we used PD model rats produced by unilateral injection of 6-hydroxydopamine (6-OHDA) into the medial forebrain bundle. We investigated effects of nigrostriatal lesions on the behavioral response (face rubbing) to formalin injection into the upper lip. We also examined expression of c-Fos and phosphorylated extracellular signal-regulated kinase (pERK) in the trigeminal spinal subnucleus caudalis (Vc) and expression of c-Fos in the periaqueductal gray matter (PAG).
Face rubbings following formalin injection showed a biphasic profile, with the first phase for the first 5 min and the second phase from 10 to 90 min. Rats with 6-OHDA lesions showed increased face rubbings in the second phase when formalin was injected ipsilaterally to the lesion, and c-Fos expression in the Vc increased. When formalin was injected contralaterally, face rubbings were reduced in the first phase, however, expression levels of c-Fos and pERK in the Vc were unchanged. No significant difference was found in c-Fos expression in the PAG between 6-OHDA- and saline-injected rats.
These results suggest that unilateral dopamine depletion in the nigrostriatal pathway may be involved in hypersensitivity to noxious stimulation delivered to the orofacial region.
Limbic circuitry of the midline thalamus
2015, Neuroscience and Biobehavioral Reviews
Citation Excerpt :
In addition, PV is essentially unique among the midline nuclei in that it receives afferents from the suprachiasmatic nucleus and the intergeniculate leaflet (Moore et al., 2000; Kawano et al., 2001). While varying in density, brainstem projections to PV derive from VTA, the pontomesencephalic RF, nucleus cuneiformis, nucleus of Darkschewitsch, the dorsal and median raphe nuclei, regions of the PAG, parabrachial nucleus, LDT and PPT, LC, and the solitary nucleus (Chen and Su, 1990; Takada et al., 1990; Bester et al., 1999; Krout and Loewy, 2000a,b; Krout et al., 2002; Li and Kirouac, 2012). The paratenial nucleus (PT) is a slender, elongated nucleus located in the anterior thalamus.
The thalamus was subdivided into three major groups: sensorimotor nuclei (or principal/relay nuclei), limbic nuclei and nuclei bridging these two domains. Limbic nuclei of thalamus (or ‘limbic thalamus’) consist of the anterior nuclei, midline nuclei, medial division of the mediodorsal nucleus (MDm) and central medial nucleus (CM) of the intralaminar complex. The midline nuclei include the paraventricular (PV) and paratenial (PT) nuclei, dorsally, and the reuniens (RE) and rhomboid (RH) nuclei, ventrally. The ‘limbic’ thalamic nuclei predominantly connect with limbic-related structures and serve a direct role in limbic-associated functions. Regarding the midline nuclei, RE/RH mainly target limbic cortical structures, particularly the hippocampus and the medial prefrontal cortex. Accordingly, RE/RH participate in functions involving interactions of the HF and mPFC. By contrast, PV/PT mainly project to limbic subcortical structures, particularly the amygdala and nucleus accumbens, and hence are critically involved in affective behaviors such as stress/anxiety, feeding behavior, and drug seeking activities. The anatomical/functional characteristics of MDm and CM are very similar to those of the midline nuclei and hence the collection of nuclei extending dorsoventrally along the midline/paramidline of the thalamus constitute the core of the ‘limbic thalamus’.
Dynorphin activation of kappa opioid receptor reduces neuronal excitability in the paraventricular nucleus of mouse thalamus
2015, Neuropharmacology
Citation Excerpt :
The efferent projections of PVT differ from those of the mediodorsal thalamic nucleus by sending glutamatergic projections to the nucleus accumbens (NAC), amygdala, and subiculum (Berendse and Groenewegen, 1990; Bubser and Deutch, 1998; Moga et al., 1995; Su and Bentivoglio, 1990; Turner and Herkenham, 1991). In addition, PVT receives dopamine innervation (Groenewegen, 1988; Otake and Ruggiero, 1995; Takada et al., 1990) and a dense peptidergic innervation from hypothalamus (Freedman and Cassell, 1994; Kirouac et al., 2005, 2006; Otake, 2005; Parsons et al., 2006). Increasing evidences indicate that PVT is involved in drug-seeking behavior (Martin-Fardon and Boutrel, 2012) and stress response (Heydendael et al., 2014, 2011).
It has been reported that kappa opioid receptor (KOR) is expressed in the paraventricular nucleus of thalamus (PVT), a brain region associated with arousal, drug reward and stress. Although intra-PVT infusion of KOR agonist was found to inhibit drug-seeking behavior, it is still unclear whether endogenous KOR agonists directly regulate PVT neuron activity. Here, we investigated the effect of the endogenous KOR agonist dynorphin-A (Dyn-A) on the excitability of mouse PVT neurons at different developmental ages. We found Dyn-A strongly inhibited PVT neurons through a direct postsynaptic hyperpolarization. Under voltage-clamp configuration, Dyn-A evoked an obvious outward current in majority of neurons tested in anterior PVT (aPVT) but only in minority of neurons in posterior PVT (pPVT). The Dyn-A current was abolished by KOR antagonist nor-BNI, Ba²⁺ and non-hydrolyzable GDP analogue GDP-β-s, indicating that Dyn-A activates KOR and opens G-protein-coupled inwardly rectifying potassium channels in PVT neurons. More interestingly, by comparing Dyn-A currents in aPVT neurons of mice at various ages, we found Dyn-A evoked significant larger current in aPVT neurons from mice around prepuberty and early puberty stage. In addition, KOR activation by Dyn-A didn't produce obvious desensitization, while mu opioid receptor (MOR) activation induced obvious desensitization of mu receptor itself and also heterologous desensitization of KOR in PVT neurons. Together, our findings indicate that Dyn-A activates KOR and inhibits aPVT neurons in mice at various ages especially around puberty, suggesting a possible role of KOR in regulating aPVT-related brain function including stress response and drug-seeking behavior during adolescence.

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On the origin of the dopaminergic innervation of the paraventricular thalamic nucleus

Abstract

Brain Res.

Neuroscience

Brain Res.

Brain Res.

Neuroscience

Brain Res. Bull.

Brain Res.

Brain Res.

Brain Res.

Neurosci. Lett.