Deep brain stimulation of the pedunculopontine tegmental nucleus modulates neuronal hyperactivity and enhanced beta oscillatory activity of the subthalamic nucleus in the rat 6-hydroxydopamine model

Alam, Mesbah; Heissler, Hans E.; Schwabe, Kerstin; Krauss, Joachim K.

doi:10.1016/j.expneurol.2011.10.006

Cited by 42 publications

(24 citation statements)

References 70 publications

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“…Recent studies showed that a bursting state is combined with a decrease in entropy (Cruz et al, 2009;Alam et al, 2012), which is in line with our present finding that a lower maxApEn value is primarily found in cells with a bursty spike pattern compared with regular and irregular firing cells. Accordingly, lesioned rats showed lower entropy and higher burst activity compared to controls.…”

Section: Discussionsupporting

confidence: 93%

Neuronal activity in the medial associative‐limbic and lateral motor part of the rat subthalamic nucleus and the effect of 6‐hydroxydopamine‐induced lesions of the dorsolateral striatum

Lindemann

Alam

Krauss

et al. 2013

J of Comparative Neurology

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Lesions of the rat nigrostriatal dopamine system by injection of 6-hydroxydopamine (6-OHDA) lead to abnormal neuronal activity in the basal ganglia (BG) motor loop similar to that found in Parkinson's disease (PD). In the BG motor loop the subthalamic nucleus (STN) represents an important structure, which, however, also comprises areas of the BG associative and limbic loops. We were interested whether neuronal activity would differ between the STN medial associative-limbic and lateral motor part, and whether selective 6-OHDA-induced lesions of the dorsolateral striatum, the entrance region of the BG motor loop, would differently affect these subregions. In male Sprague-Dawley rats 6-OHDA (n = 12) or vehicle (n = 10) was bilaterally injected in the dorsolateral striatum. Four weeks later extracellular single-unit activity and local field potentials were recorded in medial and lateral STN neurons of urethane-anesthetized rats. In sham-lesioned rats the discharge rate and burst activity were higher in the lateral compared to the medial STN. Similar differences were found for other neuronal activity measures (coefficient of variation of interspike interval, skewness, kurtosis, approximate entropy). After 6-OHDA injection neuronal burst activity was enhanced, while the discharge rate was not affected. In addition, in 6-OHDA-lesioned rats β-band oscillatory activity was enhanced, with no difference between STN subregions. We found important differences of neuronal activity between STN subregions, indicating functional segregation. However, selective 6-OHDA lesions of the dorsolateral striatum also had a pronounced effect on the medial STN subregion, indicating interaction between BG loops.

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Section: Discussionsupporting

confidence: 93%

Neuronal activity in the medial associative‐limbic and lateral motor part of the rat subthalamic nucleus and the effect of 6‐hydroxydopamine‐induced lesions of the dorsolateral striatum

Lindemann

Alam

Krauss

et al. 2013

J of Comparative Neurology

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“…Neuronal information transmission is bounded by neuronal firing pattern entropy, and computational studies have suggested that increased entropy in the globus pallidus, upstream from the SNr, induces errors in information transmission through the thalamus (Rubin and Terman, 2004 ; Guo et al, 2008 ; Dorval et al, 2010 ). While some previous work has focused on the covariance of entropy with PD symptoms (Alam et al, 2012 ; Lindemann et al, 2013 ), the reported entropy changes between conditions have been small, especially in the SNr or GPi (Dorval et al, 2008 ; Dorval and Grill, 2014 ). In the present study, entropy changes were not significant, although the general trends in SNr entropy were consistent with the reports cited above.…”

Section: Discussionmentioning

confidence: 96%

Subthalamic deep brain stimulation reduces pathological information transmission to the thalamus in a rat model of parkinsonism

Anderson

Sheppard

Huynh

et al. 2015

Front. Neural Circuits

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The degeneration of dopaminergic neurons in the substantia nigra pars compacta leads to parkinsonian motor symptoms via changes in electrophysiological activity throughout the basal ganglia. High-frequency deep brain stimulation (DBS) partially treats these symptoms, but the mechanisms are unclear. We hypothesize that motor symptoms of Parkinson’s disease (PD) are associated with increased information transmission from basal ganglia output neurons to motor thalamus input neurons and that therapeutic DBS of the subthalamic nucleus (STN) treats these symptoms by reducing this extraneous information transmission. We tested these hypotheses in a unilateral, 6-hydroxydopamine-lesioned rodent model of hemiparkinsonism. Information transfer between basal ganglia output neurons and motor thalamus input neurons increased in both the orthodromic and antidromic directions with hemiparkinsonian (hPD) onset, and these changes were reversed by behaviorally therapeutic STN-DBS. Omnidirectional information increases in the parkinsonian state underscore the detrimental nature of that pathological information and suggest a loss of information channel independence. Therapeutic STN-DBS reduced that pathological information, suggesting an effective increase in the number of independent information channels. We interpret these data with a model in which pathological information and fewer information channels diminishes the scope of possible motor activities, driving parkinsonian symptoms. In this model, STN-DBS restores information-channel independence by eliminating or masking the parkinsonism-associated information, and thus enlarges the scope of possible motor activities, alleviating parkinsonian symptoms.

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“…The PPN has extensive efferent connections with the STN and also with a number of other structures that modulate the brain's response to conflict, such as the intralaminar nuclei of the thalamus and the striatum (Pahapill and Lozano, 2000). In rats, low-frequency stimulation of the PPN leads to decreased firing in the STN (Alam et al, 2012) and as such, impairments in the effectiveness of this signaling pathway could potentially lead to an increase in the influence of the STN over the basal ganglia. These concepts are supported by the functional improvements experienced by patients with freezing following DBS of the PPN nucleus (Stefani et al, 2007; Strafella et al, 2008; Ferraye et al, 2010; Hamani et al, 2011; Tykocki et al, 2011; Follett and Torres-Russotto, 2012; Khan et al, 2012), along with increases in regional cerebral blood flow observed during stimulation of the PPN (Strafella et al, 2008; Ballanger et al, 2009).…”

Section: Insights Into Potential Pathological Processesmentioning

confidence: 99%

The role of frontostriatal impairment in freezing of gait in Parkinson's disease

Shine

Moustafa

Matar³

et al. 2013

Front. Syst. Neurosci.

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Freezing of gait (FOG) is a disabling symptom of advanced Parkinson's disease (PD) that leads to an increased risk of falls and nursing home placement. Interestingly, multiple lines of evidence suggest that the manifestation of FOG is related to specific deficits in cognition, such as set shifting and the ability to process conflict-related signals. These findings are consistent with the specific patterns of abnormal cortical processing seen during functional neuroimaging experiments of FOG, implicating increased neural activation within cortical structures underlying cognition, such as the Cognitive Control Network. In addition, these studies show that freezing episodes are associated with abnormalities in the BOLD response within key structures of the basal ganglia, such as the striatum and the subthalamic nucleus. In this article, we discuss the implications of these findings on current models of freezing behavior and propose an updated model of basal ganglia impairment during FOG episodes that integrates the neural substrates of freezing from the cortex and the basal ganglia to the cognitive dysfunctions inherent in the condition.

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Deep brain stimulation of the pedunculopontine tegmental nucleus modulates neuronal hyperactivity and enhanced beta oscillatory activity of the subthalamic nucleus in the rat 6-hydroxydopamine model

Cited by 42 publications

References 70 publications

Neuronal activity in the medial associative‐limbic and lateral motor part of the rat subthalamic nucleus and the effect of 6‐hydroxydopamine‐induced lesions of the dorsolateral striatum

Neuronal activity in the medial associative‐limbic and lateral motor part of the rat subthalamic nucleus and the effect of 6‐hydroxydopamine‐induced lesions of the dorsolateral striatum

Subthalamic deep brain stimulation reduces pathological information transmission to the thalamus in a rat model of parkinsonism

The role of frontostriatal impairment in freezing of gait in Parkinson's disease

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