Hemispheric asymmetries in spontaneous firing characteristics of substantia nigra pars reticulata neurons following a unilateral 6-hydroxydopamine lesion of the rat nigrostriatal pathway

Rohlfs, Anke; Nikkhah, Guido; Rosenthal, Christoph; Rundfeldt, Chris; Brandis, Almuth; Samii, Madjid; Löscher, Wolfgang

doi:10.1016/s0006-8993(97)00475-7

Cited by 51 publications

(49 citation statements)

References 25 publications

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“…Firing rates of neurons recorded in the SNpr of the two preparations were not significantly different (Table 1), despite the marked difference in firing pattern after dopamine loss. These observations are consistent with a number of studies showing increased burstiness or oscillatory activity in the SNpr 2-8 weeks after dopamine cell lesion in anesthetized rats (Sanderson et al, 1986;MacLeod et al, 1990;Burbaud et al, 1995;Murer et al, 1997;Rohlfs et al, 1997;Tseng et al, 2000Tseng et al, ,2001aBelluscio et al, 2003).…”

Section: Snpr Spike Train Firing Patterns and Spike-lfp Phase Relatiosupporting

confidence: 92%

“…Mean firing rates were significantly increased in the STN and the striatum but not significantly altered in the GP and SNpr at this post lesion time point. In general, the firing pattern changes observed are consistent with previous reports of alterations in individual basal ganglia nuclei in anesthetized, dopamine-depleted preparations at time periods 1-10 weeks after lesion (Sanderson et al, 1986;MacLeod et al, 1990;Hollerman and Grace, 1992;Burbaud et al, 1995;Hassani et al, 1996;Murer et al, 1997;Rohlfs et al, 1997;Magill et al, 2000Magill et al, , 2001Ni et al, 2000aNi et al, , 2001Tseng et al, 2000Tseng et al, , 2001aVila et al, 2000;Belluscio et al, 2003;Tai et al, 2003). It is interesting to note that dopamine receptor antagonist-induced reductions in dopamine receptor stimulation also induce changes in firing pattern in basal ganglia output nuclei in anesthetized rats (Degos et al, 2005).…”

Section: Firing Patterns In the Basal Ganglia Network After Dopamine supporting

confidence: 90%

“…In the context of the familiar dual circuit model of the basal ganglia (Albin et al, 1989;Alexander and Crutcher, 1990;DeLong, 1990), the present results argue that activity in the indirect pathway from the striatum to the SNpr via the GP and STN plays a more prominent role than the direct pathway in establishing slow oscillatory activity in the basal ganglia output nuclei after loss of dopamine. On the other hand, only 30-50% of the SNpr neurons are showing significant oscillations in the present study, a proportion consistent with other studies examining SNpr activity in the anesthetized dopamine cell lesioned preparation (Sanderson et al, 1986;Burbaud et al, 1995;Murer et al, 1997;Rohlfs et al, 1997;Tseng et al, 2000Tseng et al, , 2001aBelluscio et al, 2003). The observation that this proportion is considerably smaller than the proportion showing oscillatory activity in other areas of the basal ganglia suggests that the direct pathway is exerting a relatively greater influence, and counteracting the effect of the indirect pathway, on those SNpr neurons that fail to show oscillatory activity in the lesioned rats.…”

supporting

confidence: 93%

“…In addition, they provide an opportunity to examine relationships between interconnected nuclei to gain insight into the extent to which firing pattern changes in individual nuclei are linked to broader changes engaging the entire basal ganglia network. In one commonly used animal model of PD, the anesthetized rodent with a unilateral 6-hydroxydopamine (6-OHDA)-induced medial forebrain bundle lesion, a number of studies have found that firing patterns in STN and SNpr become more bursty (Sanderson et al, 1986;MacLeod et al, 1990;Hollerman and Grace, 1992;Burbaud et al, 1995;Hassani et al, 1996;Murer et al, 1997;Rohlfs et al, 1997;Tseng et al, 2000Tseng et al, , 2001aVila et al, 2000;Magill et al, 2001;Ni et al, 2001;Belluscio et al, 2003;Tai et al, 2003). This bursty activity has been shown to be correlated with slow oscillations in cortical EEG (Magill et al, 2001;Tseng et al, 2001b;Belluscio et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

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Phase relationships support a role for coordinated activity in the indirect pathway in organizing slow oscillations in basal ganglia output after loss of dopamine

et al. 2007

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The goal of the present study was to determine the phase relationships of the slow oscillatory activity that emerges in basal ganglia nuclei in anesthetized rats after dopamine cell lesion in order to gain insight into the passage of this oscillatory activity through the basal ganglia network. Spike train recordings from striatum, subthalamic nucleus (STN), globus pallidus (GP), and substantia nigra pars reticulata (SNpr) were paired with simultaneous local field potential (LFP) recordings from SNpr or motor cortex ipsilateral to a unilateral lesion of substantia nigra dopamine neurons in urethane anesthetized rats. Dopamine cell lesion induced a striking increase in incidence of slow oscillations (0.3-2.5 Hz) in firing rate in all nuclei. Phase relationships assessed through paired recordings using SNpr LFP as a temporal reference showed that slow oscillatory activity in GP spike trains is predominantly antiphase with oscillations in striatum, and slow oscillatory activity in STN spike trains is in-phase with oscillatory activity in cortex but predominantly antiphase with GP oscillatory activity. Taken together, these results imply that after dopamine cell lesion in urethane anesthetized rats, increased oscillatory activity in GP spike trains is shaped more by increased phasic inhibitory input from the striatum than by phasic excitatory input from STN. In addition, results show that oscillatory activity in SNpr spike trains is typically antiphase with GP oscillatory activity and in-phase with STN oscillatory activity. While these observations do not rule out additional mechanisms contributing to the emergence of slow oscillations in the basal ganglia after dopamine cell lesion in the anesthetized preparation, they are compatible with 1) increased oscillatory activity in the GP facilitated by an effect of dopamine loss on striatal 'filtering' of slow components of oscillatory cortical input, 2) increased oscillatory activity in STN spike trains supported by convergent antiphase inhibitory and excitatory oscillatory input from GP and cortex, respectively, and 3) increased oscillatory activity in SNpr spike trains organized by convergent antiphase inhibitory and excitatory oscillatory input from GP and STN, respectively. 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 errorsmaybe discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. NIH Public Access Author ManuscriptNeuroscience. Author manuscript; available in PMC 2012 May 17. NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript KeywordsParkinson's disease; subthalamic nucleus; substantia nigra; globus pallidus; striatum; bursting; local field potentials Dopa...

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Section: Snpr Spike Train Firing Patterns and Spike-lfp Phase Relatiosupporting

confidence: 92%

Section: Firing Patterns In the Basal Ganglia Network After Dopamine supporting

confidence: 90%

supporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

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Phase relationships support a role for coordinated activity in the indirect pathway in organizing slow oscillations in basal ganglia output after loss of dopamine

et al. 2007

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“…Cortical activity in the urethane-anesthetised rat is highly synchronized, characteristically oscillates at ∼1Hz, and is relatively stable over time (Steriade et al, 1993;Steriade, 1995, 1997;Amzica and Steriade, 1998). Many studies have shown changes in firing pattern and increased oscillatory activity in the basal ganglia following dopamine cell lesion in the anesthetized rat (Sanderson et al, 1986;MacLeod et al, 1990;Hollerman and Grace, 1992;Burbaud et al, 1995;Hassani et al, 1996;Murer et al, 1997;Rohlfs et al, 1997;Tseng et al, 2000Tseng et al, , 2001aTseng et al, , 2001bPerier et al, 2000;Vila et al, 2000;Magill et al, 2001;Ni et al, 2001;Belluscio et al, 2003;Tai et al, 2003;Walters et al, 2005Walters et al, , 2007Parr-Brownlie et al, 2007;Zold et al, 2007). Recently, this cortical oscillatory activity has been used as a probe signal in the urethane-anesthetized rat to investigate the effects of dopamine loss on the phase relationships between oscillatory activity in the external segment of the globus pallidus (GPe), the substantia nigra pars reticulata (SNpr), the subthalamic nucleus (STN), and the striatum .…”

Section: Introductionmentioning

confidence: 99%

Altered neuronal activity relationships between the pedunculopontine nucleus and motor cortex in a rodent model of Parkinson's disease

Aravamuthan

Bergstrom

French

et al. 2008

Experimental Neurology

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The pedunculopontine nucleus (PPN) is a new deep brain stimulation (DBS) target for Parkinson's disease (PD), but little is known about PPN firing pattern alterations in PD. The anesthetized rat is a useful model for investigating the effects of dopamine loss on the transmission of oscillatory cortical activity through basal ganglia structures. After dopamine loss, synchronous oscillatory activity emerges in the subthalamic nucleus and substantia nigra pars reticulata in phase with cortical slow oscillations. To investigate the impact of dopamine cell lesion-induced changes in basal ganglia output on activity in the PPN, this study examines PPN spike timing with reference to motor cortex (MCx) local field potential (LFP) activity in urethane-and ketamine-anesthetized rats. Seven -ten days after unilateral 6-hydroxydopamine lesion of the medial forebrain bundle, spectral power in PPN spike trains and coherence between PPN spiking and PPN LFP activity increased in the ∼1 Hz range in urethane-anesthetized rats. PPN spike timing also changed from firing predominantly in-phase with MCx slow oscillations in the intact urethane-anesthetized rat to firing predominantly antiphase to MCx oscillations in the hemi-parkinsonian rat. These changes were not observed in the ketamine-anesthetized preparation. These observations suggest that dopamine loss alters PPN spike timing by increasing inhibitory oscillatory input to the PPN from basal ganglia output nuclei, a phenomenon that may be relevant to motor dysfunction and PPN DBS efficacy in PD patients.

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Extracellular single-unit recordings of piriform cortex neurons in rats: Influence of different types of anesthesia and characterization of neurons by pharmacological manipulation of serotonin receptors

et al. 1999

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In epilepsy research, there is a growing interest in the role of the piriform cortex (PC) in the development and maintenance of limbic kindling and other types of limbic epileptogenesis leading to complex partial seizures. Neurophysiological studies on PC or amygdala-PC slice preparations from kindled rats showed that kindling of the amygdala induces long-lasting changes in synaptic efficacy in the ipsilateral PC, including spontaneous discharges and enhanced susceptibility of PC neurons to evoked burst responses. These long-lasting electrophysiological changes in the PC during kindling appear to be due, at least in part, to impaired function of gamma-aminobutyric acid (GABA)ergic interneurons. The aim of the present study was to develop an anesthetic protocol allowing electrophysiological single-unit recordings from inhibitory, presumably GABAergic PC interneurons in vivo. In addition to recording of spontaneously active PC neurons, microiontophoretic application of glutamate was used to activate silent neurons. Anesthesia of rats with ketamine/xylazine was not suited for single-unit recordings in the PC because of marked cardiovascular depression. Anesthesia with chloral hydrate allowed recording of spontaneous or glutamate-driven single-unit activity in approximately 40% of all animals. A similar percentage was obtained when recordings were done with the narcotic opioid fentanyl (plus gallamine), after all surgical preparations were performed under anesthesia with repeated administration of the barbiturate methohexital. To avoid brain accumulation of methohexital by repeated applications, we modified the anesthetic protocol in that methohexital was only injected once for initiation of surgical anesthesia, followed by the short-acting anesthetic propofol which does not accumulate upon repeated application. Again, after surgical preparation, electrophysiological recordings were done under fentanyl (plus gallamine). By this procedure, spontaneous or glutamate-driven single-unit activity could be measured in all rats in either layer II or III of the PC. Based on shape and frequency of action potentials, two types of neurons were recorded. The predominant type was similar in its firing characteristics to GABAergic neurons in other brain regions, was mainly located in layer III, and could be suppressed by the serotonin2A receptor antagonist MDL 100,907, suggesting that this type of PC neuron represents inhibitory, putative GABAergic interneurons. This new in vivo preparation may be useful for evaluation of PC neurons in kindled rats.

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Hemispheric asymmetries in spontaneous firing characteristics of substantia nigra pars reticulata neurons following a unilateral 6-hydroxydopamine lesion of the rat nigrostriatal pathway

Cited by 51 publications

References 25 publications

Phase relationships support a role for coordinated activity in the indirect pathway in organizing slow oscillations in basal ganglia output after loss of dopamine

Phase relationships support a role for coordinated activity in the indirect pathway in organizing slow oscillations in basal ganglia output after loss of dopamine

Altered neuronal activity relationships between the pedunculopontine nucleus and motor cortex in a rodent model of Parkinson's disease

Extracellular single-unit recordings of piriform cortex neurons in rats: Influence of different types of anesthesia and characterization of neurons by pharmacological manipulation of serotonin receptors

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