Enhancement of Excitatory Synaptic Integration by GABAergic Inhibition in the Subthalamic Nucleus

Baufreton, Jérôme; Atherton, Jeremy F.; Surmeier, D. James; Bevan, Mark D.

doi:10.1523/jneurosci.1163-05.2005

Cited by 154 publications

(153 citation statements)

References 97 publications

Supporting

Mentioning

143

Contrasting

Order By: Relevance

“…It has been shown that blocking glutamatergic neurotransmission has anti-parkinsonian effects in a variety of rodent and primate models of Parkinson's disease (Greenamyre, 1993;Lange et al, 1997), which provides initial support to this prediction in relation with w SG . Further, it has been shown that the inhibition from GPe to STN is crucial for the appearance of beta oscillations in the STN-GPe network (Baufreton et al, 2005).…”

Section: Relationship To Experimental Datamentioning

confidence: 99%

Conditions for the Generation of Beta Oscillations in the Subthalamic Nucleus–Globus Pallidus Network

Nevado‐Holgado¹,

Terry²,

Bogacz³

2010

J. Neurosci.

245

292

View full text Add to dashboard Cite

The advance of Parkinson's disease is associated with the existence of abnormal oscillations within the basal ganglia with frequencies in the beta band (13-30 Hz). While the origin of these oscillations remains unknown, there is some evidence suggesting that oscillations observed in the basalgangliaariseduetointeractionsoftwonuclei:thesubthalamicnucleus(STN)andtheglobuspallidusparsexterna(GPe).Toinvestigatethis hypothesis, we develop a computational model of the STN-GPe network based upon anatomical and electrophysiological studies. Significantly, our study shows that for certain parameter regimes, the model intrinsically oscillates in the beta range. Through an analytical study of the model, we identify a simple set of necessary conditions on model parameters that guarantees the existence of beta oscillations. These conditions for generation of oscillations are described by a set of simple inequalities and can be summarized as follows: (1) The excitatory connections from STN to GPe and the inhibitory connections from GPe to STN need to be sufficiently strong. (2) The time required by neurons to react to their inputs needs to be short relative to synaptic transmission delays. (3) The excitatory input from the cortex to STN needs to be high relative to the inhibition from striatum to GPe. We confirmed the validity of these conditions via numerical simulation. These conditions describe changes in parameters that are consistent with those expected as a result of the development of Parkinson's disease, and predict manipulations that could inhibit the pathological oscillations.

show abstract

Section: Relationship To Experimental Datamentioning

confidence: 99%

Conditions for the Generation of Beta Oscillations in the Subthalamic Nucleus–Globus Pallidus Network

Nevado‐Holgado¹,

Terry²,

Bogacz³

2010

J. Neurosci.

245

292

View full text Add to dashboard Cite

show abstract

“…With respect to the interplay of excitatory and inhibitory input, GABAergic inhibition can increase the efficiency of STN response to excitatory input by promoting recovery of inactivated voltage-dependent Na+ (Na v ) channels (Baufreton et al, 2005). This process could contribute to the increase in oscillations in the beta frequency (15-30 Hz) range observed in STN after dopamine cell lesion in awake preparations (Baufreton et al, 2005). This appears less suited for shaping slow oscillations, however, as, in the present results, phase relationships show that peak activity in the GP precedes the period of STN bursting by several hundred ms. A recent report by Kass and Mintz (2006), potentially relevant to the firing pattern triggered in the STN by slow antiphase oscillations in cortical and pallidal input, describes three coexisting patterns in STN neurons including pacemaker firing, burst mode, and a bistable state involving a relatively long-lasting silent plateau depolarization that tends to be preceded by a burst discharge.…”

Section: Increased Burstiness and Oscillations In The Stn: Relevance mentioning

confidence: 99%

Section: Increased Burstiness and Oscillations In The Stn: Relevance mentioning

confidence: 99%

“…However, these mechanisms do not appear sufficient to generate slow oscillatory activity in the STN-GP network in brain slices that preserve connectivity between GP and STN (Loucif et al, 2005). Nevertheless, these observations provide evidence that GP and STN networks have intrinsic mechanisms for supporting oscillatory activity in slow frequency ranges and led Plenz and Kitai (1999) to propose that activity in the indirect pathway supports changes in firing patterns observed after dopamine loss in vivo.In vitro studies have made considerable progress in characterizing the neurophysiological properties of the STN neurons and exploring how different patterns of inhibitory and excitatory input might affect STN activity (Mintz et al, 1986;Nakanishi et al, 1987;Beurrier et al, 1999;Bevan and Wilson, 1999;Bevan et al, 2000Bevan et al, , 2002aWigmore and Lacey, 2000;Zhu et al, 2002;Do and Bean, 2003;Hallworth et al, 2003; Wilson et al, 2004a,b;Baufreton et al, 2005;Surmeier et al, 2005;Kass and Mintz, 2006). With respect to the interplay of excitatory and inhibitory input, GABAergic inhibition can increase the efficiency of STN response to excitatory input by promoting recovery of inactivated voltage-dependent Na+ (Na v ) channels (Baufreton et al, 2005).…”

mentioning

confidence: 99%

See 1 more Smart Citation

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

View full text Add to dashboard Cite

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...

show abstract

“…For example, both STN and GPe have been shown to fire action potentials coherently with cortical slow oscillations under the influence of cortical input (Magill et al, 2000(Magill et al, , 2001. In this network, the GPe could have a central function in enhancing oscillatory activity in two ways: first, by increasing the capability of the rhythmic excitation from the cortex to drive coherent rhythmic activity in the STN via its recurrent connections with the STN (Baufreton et al, 2005) and second, through increased transmission of cortical activity to the STN via the striatum (Tseng et al, 2001), thus suggesting that a combination of mechanisms involving certain elements of all the above-mentioned hypotheses is at work.…”

Section: Oscillations In Corticobasal Ganglia Circuitsmentioning

confidence: 99%

Mechanisms underlying cortical resonant states: implications for levodopa-induced dyskinesia

Richter

Halje

Petersson

2013

Reviews in the Neurosciences

View full text Add to dashboard Cite

A common observation in recordings of neuronal activity from the cerebral cortex is that populations of neurons show patterns of synchronized oscillatory activity. However, it has been suggested that neuronal synchronization can, in certain pathological conditions, become excessive and possibly have a pathogenic role. In particular, aberrant oscillatory activation patterns have been implicated in conditions involving cortical dysfunction. We here review the mechanisms thought to be involved in the generation of cortical oscillations and discuss their relevance in relation to a recent finding indicating that high-frequency oscillations in the cerebral cortex have an important role in the generation of levodopa-induced dyskinesia. On the basis of these insights, it is suggested that the identification of physiological changes associated with symptoms of disease is a particularly important first step toward a more rapid development of novel treatment strategies.

show abstract

Enhancement of Excitatory Synaptic Integration by GABAergic Inhibition in the Subthalamic Nucleus

Cited by 154 publications

References 97 publications

Conditions for the Generation of Beta Oscillations in the Subthalamic Nucleus–Globus Pallidus Network

Conditions for the Generation of Beta Oscillations in the Subthalamic Nucleus–Globus Pallidus Network

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

Mechanisms underlying cortical resonant states: implications for levodopa-induced dyskinesia

Contact Info

Product

Resources

About