Effects of substantia nigra and pallidum stimulation on hippocampal interictal activity in the cat

doi:10.1016/0304-3940(86)90344-7

Neuroscience Letters

Volume 64, Issue 3, 14 March 1986, Pages 293-298

https://doi.org/10.1016/0304-3940(86)90344-7 Get rights and content

Abstract

In the present work the role played by substantia nigra pars compacta and globus pallidus pars interna on hippocampal bioelectrical activity is studied. Injections of sodium penicillin (i.v.) produce steady interictal spikes in the hippocampus. Substantia nigra stimulation induces regular theta rhythm and inhibits the spikes. Pallidal stimulation, on the contrary, appears to strongly enhance epileptiform activity, proceeding to generalized seizure activity. The results are discussed in the light of the interrelationships between basal ganglia and hippocampus, hypothesizing a putative feedback loop from striatal to limbic centers.

References (18)

L.C.A. Conrad et al.
Autoradiographic tracing of nucleus accumbens efferents in the rat
Brain Res.
(1976)
J.C. Garland et al.
An electrophysiological study of convergence of entopeduncular and lateral preoptic inputs on lateral habenular neurons projecting to the midbrain
Brain Res.
(1983)
W.R. Klemm
Physiological and behavioural significance of hippocampal rhythmic slow activity (‘theta rhythm’)
Progr. Neurobiol.
(1976)
W.R. Klemm et al.
Septal- and caudate-induced behavioral inhibition in relation to hippocampal EEG of rabbits
Physiol. Behav.
(1975)
V. La Grutta et al.
The importance of the caudate nucleus in the control of convulsive activity in the amygdaloid complex and the temporal cortex of the cat
Electroenceph. Clin. Neurophysiol.
(1971)
V. La Grutta et al.
Effects of caudate nucleus on paroxysmal activity in hippocampus of cat
Electroenceph. Clin. Neurophysiol.
(1985)
G. Le Gal La Salle et al.
Role of the hippocampus, amygdala and the substantia nigra in the evolution of status epilepticus induced by sistemic injection of kainic acid in rats
Rev. E.E.G. Neurophysiol.
(1984)
J.I. Nagy et al.
Evidence for a GABA-containing projection from the entopeduncular nucleus to the lateral habenula in the rat
Brain Res.
(1978)
W.J.H. Nauta et al.
Projections of the lentiform nucleus in the monkey
Brain Res.
(1966)

There are more references available in the full text version of this article.

Cited by (17)

A supramodal role of the basal ganglia in memory and motor inhibition: Meta-analytic evidence
2018, Neuropsychologia
Citation Excerpt :
For example, Sabatino and colleagues found evidence that basal ganglia activity influences hippocampal oscillations. Specifically, whereas caudate stimulation appeared to influence the hippocampal theta rhythm by inhibiting the hippocampal spikes (La Grutta et al., 1985; Sabatino et al., 1985), pallidal stimulation triggered enhanced epileptiform activity, inducing generalised seizure activity (Sabatino et al., 1986). Berke et al. (2004) also found entrainment of ventral/medial striatal neurons to the hippocampal theta in rats.
The ability to stop actions and thoughts is essential for goal-directed behaviour. Neuroimaging research has revealed that stopping actions and thoughts engage similar cortical mechanisms, including the ventro- and dorso-lateral prefrontal cortex. However, whether and how these abilities require similar subcortical mechanisms remains unexplored. Specifically of interest are the basal ganglia, subcortical structures long-known for their motor functions, but less so for their role in cognition. To investigate the potential common mechanisms in the basal ganglia underlying action and thought stopping, we conducted meta-analyses using fMRI data from the Go/No-Go, Stop-signal, and Think/No-Think tasks. All three tasks require active stopping of prepotent actions or thoughts. To localise basal ganglia activations, we performed high-resolution manual segmentations of striatal subregions. We found that all three tasks recovered clusters in the basal ganglia, although the specific localisation of these clusters differed. Although the Go/No-Go and Stop-signal tasks are often interchangeably used for measuring action stopping, their cluster locations in the basal ganglia did not significantly overlap. These different localised clusters suggest that the Go/No-Go and Stop-signal tasks may recruit distinct basal ganglia stopping processes, and therefore should not be treated equivalently. More importantly, the basal ganglia cluster recovered from the Think/No-Think task largely co-localised with that from the Stop-signal task, but not the Go/No-Go task, possibly indicating that the Think/No-Think and Stop-signal tasks share a common striatal circuitry involved in the cancellation of unwanted thoughts and actions. The greater similarity of the Think/No-Think task to the Stop-Signal rather than Go/No-Go task also was echoed at the cortical level, which revealed highly overlapping and largely right lateralized set of regions including the anterior DLPFC, VLPFC, Pre-SMA and ACC. Overall, we provide novel evidence suggesting not only that the basal ganglia are critical for thought stopping, but also that they are involved in specific stopping subprocesses that can be engaged by tasks in different domains. These findings raise the possibility that the basal ganglia may be part of a supramodal network responsible for stopping unwanted processes more broadly.
Induction of hippocampal theta rhythm by electrical stimulation of the ventral tegmental area and its loss after septum inactivation
2012, Brain Research
Citation Excerpt :
Many places have been found in the mesencephalon that produce theta rhythm when stimulated (Dypvik and Bland, 2004; Klemm, 1972; Kramis and Vanderwolf, 1980; Macadar et al., 1974; McNaughton and Sedgwick, 1978; Oswald and Emmerich, 1980; Robinson and Vanderwolf, 1978; Vertes, 1980; Vorobev et al., 1988), however, the vast majority of these places occupy more posterior areas of the brainstem in comparison to our stimulation site. In our study, the control stimulation sites outside of the VTA but in the same part of the anterior–posterior axis (mainly in the zona incerta, which contains the A13 group of dopaminergic cells exhibiting projections to hypothalamus (Dahlstrom and Fuxe, 1964)) were not capable of inducing theta rhythm, with the exception of the substantia nigra pars compacta: this structure, however, is expected to produce theta rhythm when stimulated, as described by Sabatino et al. (1986) and Hallworth and Bland (2004). Procaine administered into the medial septum resulted in temporary ineffectiveness of theta induction by VTA stimulation.
The ventral tegmental area (VTA), which may be one of the structures involved in regulation of hippocampal theta rhythm, sends direct projections to the hippocampus and also to the forebrain septum, the key centres involved in theta generation. In the present study we aimed at assessing which projections from the VTA (direct or through the septum) participate in regulation of hippocampal electric activity. Experiments were conducted on 3 groups of urethanised male Wistar rats. In the first group (n = 6) electrical stimulation of the VTA was used to evoke theta rhythm episodes in hippocampus. Stimulation was repeatedly applied in control conditions and after procainic blockade of the septum. The second group (n = 6), subjected to unilateral electrical stimulation of the VTA (30-s stimulation at 10-min intervals during 2 h) and to subsequent detection of Fos expression, served to measure neuronal activation of the target mesolimbic structures. Activation levels of selected structures were compared to data from analogous stimulation of the zona incerta (ZI, the third group, n = 6). Stimulation of the VTA immediately generated regular theta rhythm in both hippocampi. Inactivation of the septum with procaine temporarily abolished this effect. VTA stimulation increased the density of Fos in the ipsilateral nucleus accumbens. Stimulation of the ZI never generated theta but evoked significant induction of Fos expression in the hippocampus. Our data suggest that the projection through which the VTA enhances theta rhythm is not direct but is incorporated into the main route of theta generation, which involves septum as the main relay node.
Basal ganglia-hippocampal interactions support the role of the hippocampal formation in sensorimotor integration
2004, Experimental Neurology
Experiments were carried out to evaluate whether neural activity in the basal ganglia is functionally related to the neural activity underlying mechanisms of theta band oscillation and synchrony in the hippocampal formation. Experiment 1 demonstrated that electrical stimulation administered to the substantia nigra, globus pallidus (GP) and caudate-putamen (CPu) in urethane anesthetized rats elicited theta field activity in the hippocampal formation. Subsequent microinfusion of the local anesthetic procaine hydrochloride into the medial septum reversibly abolished this effect. In Experiment 2, single cell discharge profiles established for 152 cells recorded in nuclei of the basal ganglia resulted in 101 (66%) being classified as theta-related and 51 (34%) classified as nonrelated. Theta-related cells were further subclassified as tonic theta-ON cells (n = 79) and tonic theta-OFF (n = 22). Tonic theta-ON and tonic theta-OFF cells displayed irregular or regular (tonic) discharge patterns. Rhythmic discharge patterns did not occur in any theta-related cells in the nuclei of the basal ganglia. However, analyses using Kaneoke and Vitek's [J. Neurosci. Methods 68, (1996) 211] algorithms revealed that 51/101 (50%) theta-related cells displayed periodicity in their discharge patterns whereas 27/51 (53%) of the nonrelated cells displayed periodicity in their discharge patterns. The periodicities in the majority of cells were in frequency ranges above that of theta band oscillation and synchrony. The results support the following conclusions: (1) the cellular activity of the basal ganglia, composed of nuclei traditionally associated with motor functions, is functionally connected with the neural circuitry involved in the generation of theta band oscillation and synchrony in the hippocampal formation; (2) the observed functional connectivity provides support for the role of the hippocampal formation in sensorimotor integration.
Excitatory neurotransmitters in the lateral habenula and pedunculopontine nucleus of rat modulate limbic seizures induced by pilocarpine
1992, Brain Research
The involvement of the excitatory neurotransmitter system in the lateral habenula and pedunculopontine nucleus in the initiation and propagation of limbic seizures induced by pilocarpine has been investigated in the rat. Limbic seizures occur in animals following bilateral microinjection into the lateral habenula of $N- methyl- d -aspartate$ (NMDA) (5 and 12.5 nmol) or kainate (100 and 200 pmol), 15 min prior to a subconvulsant dose of pilocarpine (150 mg/kg, i.p.). In the absence of pilocarpine NMDA (5 and 12.5 nmol) or kainate (100 and 200 pmol), injected focally into the lateral habenula or pedunculopontine nucleus, produced sniffing, grooming and tremor but no electrographic or behavioural seizures. Limbic seizures also occur after a subconvulsant dose of pilocarpine when it is preceded by injection of NMDA (5 and 12.5 nmol) or kainate (50, 100 and 200 pmol) into the pedunculopontine nucleus. Behavioural and electrographic signs of limbic seizures following pilocarpine (380 mg/kg, i.p.) were attenuated or completely antagonized by focal injection into the lateral habenula of the NMDA antagonist, 2-amino-7-phosphonoheptanoate (AP7) (10 and 50 pmol) or kainate antagonist, γ-d-glutamylaminomethylsulphonate (GAMS) (20 nmol). In addition, AP7 (0.05, 0.1 and 1.0 nmol) or GAMS (40 nmol) injected into the pedunculopontine nucleus suppressed limbic seizures induced by i.p. administration of pilocarpine (380 mg/kg). The relative efficacy of NMDA and non-NMDA receptor antagonists revealed that the selective NMDA antagonist, AP7, was more potent in its anticonvulsant activity in comparison to GAMS, a non-NMDA receptor antagonist.
Relay stations and neurotransmitters between the pallidal region and the hippocampus
1991, Electroencephalography and Clinical Neurophysiology
The effects of internal pallidum and lateral habenula stimulation on epileptiform activity of cat's hippocampus were studied. A steady interictal activity was induced by locally applied sodium penicillin (PCN) solution. Both pallidal and habenular electrical stimulation caused an increase in spike frequency and amplitude. Intraperitobeally injected atropine sulphate failed to modify pallidal and habenular influences. Intraperitoneal methysergide bimaleate (5-HT antagonist) suppressed the effects of habenular stimulation. In contrast to the effects of pallidal and habenular stimulation, raphe electrical stimulation inhibited hippocampal spiking and intra-raphal muscimol (a GABA receptor agonist) enhanced hippocampal-based epilepsy. After muscimol, raphe stimulation at the same threshold parameters failed to affect hippocampal activity. In cats with habenular lesions hippocampal spike frequency and amplitude were reduced and intra-raphal muscimol did not affect the hippocampus. The results are discussed in the light of a complex interrelationship between basal ganglia and hippocampus. The role of the lateral habenula and of the medial raphe as relay stations between the two regions is emphasized.
Nigral influence on focal epilepsy
1990, Neurophysiologie Clinique / Clinical Neurophysiology
The substantia nigra (SN) has been proposed as a structure involved in epileptiform phenomena. Previous investigations demonstrated that SN is able to elicit hippocampal rhythmic slow activity (RSA) as well as to inhibit hippocampal interictal spikes induced by parenteral administration of penicillin. The present series of experiments was carried out in order to characterize the action of SN on a focal model of hippocampal epilepsy. Experiments were performed on encéphale isolé cats in which steady epileptiform activity was induced by locally applied penicillin. Electrical stimulation of SN pars reticulata (pr) caused a statistically significant decrease of hippocampal spike frequency and amplitude in 30% of the total number of stimulation sessions. Stimulation of SN pars compacta (pc) was even more effective. It induced inhibitory effects on hippocampal spikes in 91% of the cases. In 30% of the cats, RSA was noted on hippocampal recordings in correspondence to nigral activation. Experimental data support the hypothesis that the SNpc influences hippocampal excitability: a differential role may be played by SNpc and SNpr in the control of seizure processes.
La substantia nigra (SN) est une structure probablement active dans les phénomènes épileptiformes. Des recherches antérieures ont démontré que la SN peut déclencher une activité rythmique lente (ARL) de l'hippocampe ainsi qu'inhiber les spikes interictaux de l'hippocampe provoqués par l'administration parentérale de pénicilline. Le protocole suivant a été élaboré afin de caractériser l'action exercée par la SN sur un modèle d'épilepsie hippocampale. Les expériences ont été conduites sur des chats à encéphale isolé chez lesquels on provoquait l'activité épileptiforme par des applications locales de pénicilline. La stimulation électrique de la pars reticulata (pr) de la SN causait une réduction statistiquement significante de la fréquence et de l'amplitude des spikes hippocampaux dans 30% du nombre total des sessions de stimulation. La stimulation de la pars compacta (pc) de la SN était encore plus efficace et provoquait des effets d'inhibition sur les spikes hippocampaux dans 91% des cas. Chez 30% des chats, on observait une ARL en enregistrant l'activité hippocampale correspondant à l'activation de la SN. Les données expérimentales confirment l'hypothèse que la pc de la SN exerce une influence sur l'excitabilité de l'hippocampe. La pc et la pr de la SN jouent probablement un rôle différentiel dans le contrôle des attaques épileptiques.

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Effects of substantia nigra and pallidum stimulation on hippocampal interictal activity in the cat

Abstract

Brain Res.

Brain Res.

Progr. Neurobiol.

Physiol. Behav.

Electroenceph. Clin. Neurophysiol.

Electroenceph. Clin. Neurophysiol.

Rev. E.E.G. Neurophysiol.

Brain Res.

Brain Res.