The globus pallidus receives a projection from the parafascicular nucleus in the rat

doi:10.1016/0006-8993(91)90224-J

Brain Research

Volume 553, Issue 1, 5 July 1991, Pages 18-26

https://doi.org/10.1016/0006-8993(91)90224-J Get rights and content

Abstract

Study of the afferents of the rat globus pallidus (GP) with Fluoro-gold, a retrograde tracer, revealed retrogradely labeled neurons in the ipsilateral parafascicular nucleus of the thalamus (PF), a previously undescribed afferent of the rat GP. We used the anterograde tracer,Phaseolus vulgaris-leucoagglutinin (PHA-L), to confirm and extend our findings. After injections of PHA-L in the PF, labeled fibers with varicosities and terminal specializations were observed in the ipsilateral GP. The topographical organization of the projection is such that lateral and ventral PF neurons project preferentially to respective parts of the GP, and medial PF neurons project primarily to the ventral GP. There were very few labeled fibers seen in the dorsal or medial GP. The presently described projection from the PF to the GP provides an additional route for the PF to influence basal ganglia circuitry.

References (54)

AlbinR.L. et al.
The functional anatomy of basal ganglia disorders
Trends Neurosci.
(1989)
BecksteadR.M. et al.
Efferent connections of the substantia nigra and ventral tegmental area in the rat
Brain Research
(1979)
CornwallJ. et al.
Afferent projections to the parafascicular thalamic nucleus of the rat, as shown by the retrograde transport of wheat germ agglutinin
Brain Res. Rev.
(1988)
FrancoisC. et al.
A topographic study of the course of nigral axons and of the distribution of pallidal axonal endings in the centre median-parafascicular complex of macaques
Brain Research
(1988)
GerfenC.R. et al.
An anterograde neuroanatomical tracing method that shows detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin,phaseolus-vulgaris-leucoagglutinin (PHA-L)
Brain Research
(1984)
HaberS.N. et al.
Ramifications of the globus pallidus in the rat as indicated by patterns of immunohistochemistry
Neuroscience
(1983)
HaringJ.H. et al.
The identification of some sources of afferent input to the rat nucleus basalis magnocellularis by retrograde transport of horseradish peroxidase
Brain Research
(1986)
HeimerL. et al.
Ventral striatum and ventral pallidum. Components of the motor system?
Trends Neurosci.
(1982)
JacksonA. et al.
Nucleus tegmenti pedunculopontinus: efferent connections with special reference to the basal ganglia, studied in the rat by anterograde and retrograde transport of horseradish peroxidase
Neuroscience
(1983)
LindvallO. et al.
Dopaminergic innervation of the globus pallidus by collaterals from the nigrostriatal pathway
Brain Research
(1979)

NagyJ.I. et al.

Anterior striatal projections to the globus pallidus, entopeduncular nucleus and substantia nigra in the rat: the GABA connection

Brain Research

(1978)

NautaH.J.W.

Projections of the pallidal complex: an autoradiographic study in the cat

Neuroscience

(1979)

NautaW.J.H. et al.

Projections of the lentiform nucleus in the monkey

Brain Research

(1966)

ParentA.

Extrinsic connections of the basal ganglia

Trends Neurosci.

(1990)

ParentA. et al.

Organization of ascending serotonin systems in the adult rat brain. A radioautographic study after intraventricular administration of (³H)-5-hydroxytryptamine

Neuroscience

(1981)

PieriboneV.A. et al.

The iontophoretic appliation of fluoro-gold for the study of afferents to deep brain nuclei

Brain Research

(1988)

SadikotA.F. et al.

The centre median and parafascicular thalamic nuclei project respectively to the sensorimotor and associative-limbic striatal territories in the squirrel monkey

Brain Research

(1990)

SaperC.B. et al.

Projections of the pedunculopontine tegmental nucleus in the rat: evidence for additional extrapyramidal circuitry

Brain Research

(1982)

SawchenkoP.E. et al.

A method for tracing biochemically defined pathways in the central nervous system using combined fluorescence retrograde transport and immunohistochemical techniques

Brain Research

(1981)

SchmuedL.C. et al.

Fluoro-gold: a new fluorescent retrograde axonal tracer with numerous unique properties

Brain Research

(1986)

StainesW.A. et al.

Demonstration of a pallidostriatal pathway by retrograde transport of HRP-labeled lectin

Brain Research

(1981)

SwitzerR.C. et al.

The globus pallidus and its rostroventral extension into the olfactory tubercle of the rat: a cyto- and chemoarchitectural study

Neuroscience

(1982)

Van Der KooyD. et al.

Non-cholinergic globus pallidus cells that project to the cortex but not to the subthalamic nucleus in rat

Neurosci. Lett.

(1985)

Van Der KooyD. et al.

The pallido-subthalamic projection in rat: anatomical and biochemical studies

Brain Research

(1981)

WouterloodF.G. et al.

Neuroanatomical tracing by use ofPhaseolus vulgaris-leucoagglutinin (PHA-L): electron microscopy of PHA-L-filled neuronal somata, dendrites, axons and axon terminals

Brain Research

(1985)

Albe-FessardD. et al.

Convergent thalamic and cortical projections—The non-specific system

AlexanderG.E. et al.

Parallel organization of functionally segregated circuits linking basal ganglia and cortex

Annu. Rev. Neurosci.

(1986)

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Although GP and STN neurons pattern each other’s activity, the GP is considered as a structure controlling the electrical activity of STN neurons by means of its GABAergic projections (Hallworth and Bevan, 2005; Baufreton et al., 2009). In addition to massive GABAergic axon terminals from the striatum and glutamatergic afferents from the STN and the parafascicular nucleus of the thalamus (Kincaid et al., 1991; Mouroux et al., 1997), GP receives dopaminergic afferents from the SNc. These dopaminergic afferents are considered as collaterals of the nigrostriatal projections (François et al., 1999; Smith and Kieval, 2000; Bouali-Benazzouz et al., 2009) and specific nigro-pallidal projections (Jan et al., 2000; Smith and Kieval, 2000; Rommelfanger and Wichmann, 2010).
In addition to GABA and glutamate innervations, the globus pallidus (GP) receives dopamine afferents from the pars compacta of the substantia nigra (SNc), and in turn, sends inhibitory GABAergic efferents to the subthalamic nucleus (STN) and the pars reticulata of the substantia nigra (SNr). Nevertheless, the role of dopamine in the modulation of these pallido-subthalamic and pallido-nigral projections is not known. The present study aimed to investigate the effects of intrapallidal injection of 6-hydroxydopamine (6-OHDA) on the electrical activity of STN and SNr neurons using in vivo extracellular single unit recordings in the rat and on motor behaviors, using the “open field” actimeter and the stepping test. We show that intrapallidal injection of 6-OHDA significantly decreased locomotor activity and contralateral paw use. Electrophysiological recordings show that 6-OHDA injection into GP significantly increased the number of bursty cells in the STN without changing the firing rate, while in the SNr neuronal firing rate decreased and the proportion of irregular cells increased. Our data provide evidence that intrapallidal injection of 6-OHDA resulted in motor deficits paralleled by changes in the firing activity of STN and SNr neurons, which mimic in large part those obtained after major dopamine depletion in the classical rat model of Parkinson’s disease. They support the assumption that in addition to its action in the striatum, dopamine mediates its regulatory function at various levels of the basal ganglia circuitry, including the GP.
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Striatopallidal neurons expressing D2 receptors send inhibitory projections to the external segment of the globus pallidus (GPe). The GPe sends focussed inhibitory projections to GPi/SNr (Bolam et al., 2000; Kincaid et al., 1991; Smith and Bolam, 1989, 1990). Due to this additional inhibitory projection, activity in the indirect pathway ultimately results in inhibition of the thalamus and thus suppression of frontal action plans.
We review the contributions of biologically constrained computational models to our understanding of motor and cognitive deficits in Parkinson’s disease (PD). The loss of dopaminergic neurons innervating the striatum in PD, and the well-established role of dopamine (DA) in reinforcement learning (RL), enable neural network models of the basal ganglia (BG) to derive concrete and testable predictions. We focus in this review on one simple underlying principle – the notion that reduced DA increases activity and causes long-term potentiation in the indirect pathway of the BG. We show how this theory can provide a unified account of diverse and seemingly unrelated phenomena in PD including progressive motor degeneration as well as cognitive deficits in RL, decision making and working memory. DA replacement therapy and deep brain stimulation can alleviate some aspects of these impairments, but can actually introduce negative effects such as motor dyskinesias and cognitive impulsivity. We discuss these treatment effects in terms of modulation of specific mechanisms within the computational framework. In addition, we review neurocomputational interpretations of increased impulsivity in the face of response conflict in patients with deep-brain-stimulation.
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The globus pallidus (GP) plays an important role in basal ganglia circuitry. In contrast to the well-characterized actions of dopamine on striatal neurons, the functional role of the dopamine innervation of GP is still not clearly determined. The present study aimed to investigate the effects of intrapallidal injection of 6-hydroxydopamine (6-OHDA) on rotational behavior induced by apomorphine, on the loss of dopamine cell bodies in the substantia nigra pars compacta (SNc) and fibers in the GP and striatum and on in vivo extracellularly-recorded GP neurons in the rat. Injection of 6-OHDA into GP induced severe loss of tyrosine hydroxylase–immunoreactive (TH-IR) fibers in GP (−85%) with a reduction in the number of TH-IR cell bodies in the SNc (−52%) and fibers in the striatum (−50%). S.c. injection of apomorphine in these rats induced a moderate number of turns (26±6 turns/5 min). Electrophysiological recordings show that 6-OHDA injection in GP induced a significant decrease of the firing rate of GP neurons (16.02±1.11 versus 24.14±1.58 spikes/sec in control animals and 22.83±1.28 in sham animals, one-way ANOVA, P<0.0001) without any change in the firing pattern (χ²=1.03, df=4, P=0.90). Our results support the premise of the existence of collaterals of SNc dopaminergic axons projecting to the striatum and GP and that dopamine plays a role in the modulation of the firing rate but not the firing pattern of GP neurons. Our data provide important insights into the functional role of the SNc–GP dopaminergic pathway suggesting that dopamine depletion in GP may participate in the development of motor disabilities.
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The MCh-sensitive inward current was relatively linear and had an average reversal potential of −101±29 mV (Fig. 8Biii, n=6), which is near the K+ equilibrium potential and indicative of Kleak. Considering lPf neurons project to the neocortex and/or the basal ganglia (Jones and Leavitt, 1974; Berendse and Groenewegen, 1990, 1991; Kincaid et al., 1991; Feger et al., 1994; Deschenes et al., 1996), we next investigated whether bushy and diffuse neuronal subtypes project to distinct brain regions. Fluorescent microspheres were injected into the dorsal lateral striatum or the frontal neocortex (see Experimental Procedures).
The lateral parafascicular nucleus (lPf) is a member of the intralaminar thalamic nuclei, a collection of nuclei that characteristically provides widespread projections to the neocortex and basal ganglia and is associated with arousal, sensory, and motor functions. Recently, lPf neurons have been shown to possess different characteristics than other cortical-projecting thalamic relay neurons. We performed whole cell recordings from lPf neurons using an in vitro rat slice preparation and found two distinct neuronal subtypes that were differentiated by distinct morphological and physiological characteristics: diffuse and bushy. Diffuse neurons, which had been previously described, were the predominant neuronal subtype (66%). These neurons had few, poorly-branching, extended dendrites, and rarely displayed burst-like action potential discharge, a ubiquitous feature of thalamocortical relay neurons. Interestingly, we discovered a smaller population of bushy neurons (34%) that shared similar morphological and physiological characteristics with thalamocortical relay neurons of primary sensory thalamic nuclei. In contrast to other thalamocortical relay neurons, activation of muscarinic cholinergic receptors produced a membrane hyperpolarization via activation of M₂ receptors in most lPf neurons (60%). In a minority of lPf neurons (33%), muscarinic agonists produced a membrane depolarization via activation of predominantly M₃ receptors. The muscarinic receptor-mediated actions were independent of lPf neuronal subtype (i.e. diffuse or bushy neurons); however the cholinergic actions were correlated with lPf neurons with different efferent targets. Retrogradely-labeled lPf neurons from frontal cortical fluorescent bead injections primarily consisted of bushy type lPf neurons (78%), but more importantly, all of these neurons were depolarized by muscarinic agonists. On the other hand, lPf neurons labeled by striatal injections were predominantly hyperpolarized by muscarinic agonists (63%). Our results indicate two distinct subpopulations of lPf projection neurons, and interestingly lPf neurons respond differentially to muscarinic receptor activation based on their axonal target.
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In addition to the cerebral cortex, the striatum receives excitatory input from the thalamus. The centromedian (centre median, CM) and parafascicular (Pf) nuclei are an important source of thalamostriatal projections. Anterograde tract-tracing indicates the CM–Pf complex provides dense afferents to the matrix compartment of the striatum. Whereas CM projects to the entire sensorimotor territory of the striatum, the Pf provides complementary input to the entire associative sector. The Pf also provides lighter input to the nucleus accumbens. Both CM and Pf provide light to moderately dense inputs to other components of the basal ganglia in a largely complementary manner, covering motor or associative-limbic territories of the subthalamic nucleus, globus pallidus and ventral midbrain. In turn, the CM and Pf receive mainly segregated input from parallel motor and associative-limbic circuits of the basal ganglia. The CM and Pf may therefore be considered important participants in parallel processing of motor and associative-limbic information in the basal ganglia. Connections of the CM and Pf with other thalamic nuclei suggest they also participate in integrative functions within the thalamus. In addition, inputs from the brainstem reticular core, reciprocal connections with the cerebral cortex and reticular thalamic nucleus suggest a role in state-dependant information processing. Consideration of the differential connections of the CM and Pf, and better understanding of their role in pathophysiology, may eventually lead to development of an important new target for relief of a variety of neurological and psychiatric disorders.
The neuronal activity of thalamic parafascicular nucleus is conversely regulated by nigrostriatal pathway and pedunculopontine nucleus in the rat
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The PF has reciprocal connections with the basal ganglia and associated structures, and consequently plays an important role in motor control (Kilpatrick and Phillipson, 1986; Cornwall and Phillipson, 1988; Sadikot et al., 1990; Mouroux and Feger, 1993). The PF receives mainly inputs from the entopeduncular nucleus (EP), the substantia nigra pars reticulata (SNr), the neostriatum and the pedunculopontine nucleus (PPN) (Sofroniew et al., 1985; Cornwall and Phillipson, 1988; Steriade et al., 1988; Lavoie and Parent, 1994a) and projects broadly to the neostriatum, the globus pallidus and the subthalamic nucleus (STN) (Sugimoto and Hattori, 1983; Kincaid et al., 1991; Feger et al., 1994; Castle et al., 2005; Lanciego et al., 2004). Several studies have suggested that the PF is implicated in the pathophysiology of Parkinson's disease (PD) and especially in the tremor at rest.
The aim of the present study was to investigate changes in the firing activity of thalamic parafascicular nucleus (PF) neurons at different time periods after 6-hydroxydopamine (6-OHDA) lesions of the substantia nigra pars compacta (SNc) and the role of the pedunculopontine nucleus (PPN) in these changes. In normal rats, the firing rate of PF neurons was 3.66 ± 0.37 spikes/s. In rats with 6-OHDA lesions of the SNc, the firing rate of PF neurons slightly decreased to 3.19 ± 0.35 spikes/s during the third week compared to normal rats, unexpectedly, as moving on to fifth week, the firing rate increased significantly to 4.82 ± 0.31 spikes/s. In rats with ibotenic acid lesions of the PPN, the firing rate decreased significantly to 1.98 ± 0.19 spikes/s compared to normal rats. When the SNc and PPN were double lesioned, the firing rate of PF neurons decreased significantly to 2.36 ± 0.23 spikes/s during the third week and 2.16 ± 0.16 spikes/s during the fifth week post-lesions. The separate lesions of the PPN, SNc, and double lesion of both in the rats did not change the firing pattern of PF neurons compared to normal rats. These findings demonstrate that PF neurons are hyperactive in the 6-OHDA-lesioned rats suggesting the implication of this nucleus in the pathophysiology of parkinsonism. Furthermore, the fact that the PPN lesions induced a decrease in the firing rate of PF neurons in normal and SNc-lesioned rats suggests that the PF is under major control of the PPN.

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The globus pallidus receives a projection from the parafascicular nucleus in the rat

Abstract

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