Neighboring pallidal neurons do not exhibit more synchronous oscillations than remote ones in the MPTP primate model of Parkinson’s disease

In the healthy primate, neurons of the external and internal segments of the globus pallidus (GP) present a primarily irregular firing pattern, and a negligible level of synchrony is observed between pairs of neurons. This holds even for neighboring cells, despite their higher probability to receive...

Full description

Bibliographic Details
Main Authors: Rea eMitelman, Boris eRosin, Hila eZadka, Maya eSlovik, Gali eHeimer, Ya'acov eRitov, Hagai eBergman, Shlomo eElias
Format: Article
Language:English
Published: Frontiers Media S.A. 2011-06-01
Series:Frontiers in Systems Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fnsys.2011.00054/full
_version_ 1818163693490274304
author Rea eMitelman
Rea eMitelman
Boris eRosin
Hila eZadka
Hila eZadka
Maya eSlovik
Gali eHeimer
Ya'acov eRitov
Ya'acov eRitov
Hagai eBergman
Hagai eBergman
Hagai eBergman
Shlomo eElias
Shlomo eElias
author_facet Rea eMitelman
Rea eMitelman
Boris eRosin
Hila eZadka
Hila eZadka
Maya eSlovik
Gali eHeimer
Ya'acov eRitov
Ya'acov eRitov
Hagai eBergman
Hagai eBergman
Hagai eBergman
Shlomo eElias
Shlomo eElias
author_sort Rea eMitelman
collection DOAJ
description In the healthy primate, neurons of the external and internal segments of the globus pallidus (GP) present a primarily irregular firing pattern, and a negligible level of synchrony is observed between pairs of neurons. This holds even for neighboring cells, despite their higher probability to receive common inputs and to innervate each other via lateral connectivity. In the parkinsonian primate, this changes drastically, and many pairs of GP cells show synchronous oscillations. To address the relation between distance and synchrony in the parkinsonian state, we compared the synchrony of discharge of close pairs of neurons, recorded by the same electrode, with remote pairs, recorded by different ones. However, spike trains of neighboring cells recorded by the same extracellular electrode exhibit the shadowing effect; i.e., lack of detection of spikes that occur within a few milliseconds of each other.Here, we demonstrate that the shadowing artifact can both induce apparent correlations between non-correlated neurons, as well as conceal existing correlations between neighboring ones. We therefore introduced artificial shadowing in the remote pairs, similar to the effect we observed in the close ones. After the artificial shadowing, neighboring cells did not show a higher tendency to oscillate synchronously than remote ones. On the contrary, the average percentage (over all sessions) of artificially shadowed remote pairs exhibiting synchronous oscillations was 35.4% compared to 17.2% in the close ones. Similar trend was found when the unshadowed remote pairs were separated according to the estimated distance between electrode tips: 29.9% of pairs at approximate distance of less than 750 µm were significantly synchronized, in comparison with 28.5% of the pairs whose distance was more than 750 µm.We conclude that the synchronous oscillations in the GP of MPTP treated primates are homogenously distributed.
first_indexed 2024-12-11T16:53:37Z
format Article
id doaj.art-66466374a3674260bd754a8427aee37b
institution Directory Open Access Journal
issn 1662-5137
language English
last_indexed 2024-12-11T16:53:37Z
publishDate 2011-06-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Systems Neuroscience
spelling doaj.art-66466374a3674260bd754a8427aee37b2022-12-22T00:58:01ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372011-06-01510.3389/fnsys.2011.000549446Neighboring pallidal neurons do not exhibit more synchronous oscillations than remote ones in the MPTP primate model of Parkinson’s diseaseRea eMitelman0Rea eMitelman1Boris eRosin2Hila eZadka3Hila eZadka4Maya eSlovik5Gali eHeimer6Ya'acov eRitov7Ya'acov eRitov8Hagai eBergman9Hagai eBergman10Hagai eBergman11Shlomo eElias12Shlomo eElias13The Hebrew University of JerusalemThe Hebrew University of JerusalemThe Hebrew University of JerusalemThe Hebrew University of JerusalemThe Hebrew University of JerusalemThe Hebrew University of JerusalemSheba Medical CenterThe Hebrew University of JerusalemThe Hebrew University of JerusalemThe Hebrew University of JerusalemThe Hebrew University of JerusalemThe Hebrew University of JerusalemThe Hebrew University of JerusalemHadassah University HospitalIn the healthy primate, neurons of the external and internal segments of the globus pallidus (GP) present a primarily irregular firing pattern, and a negligible level of synchrony is observed between pairs of neurons. This holds even for neighboring cells, despite their higher probability to receive common inputs and to innervate each other via lateral connectivity. In the parkinsonian primate, this changes drastically, and many pairs of GP cells show synchronous oscillations. To address the relation between distance and synchrony in the parkinsonian state, we compared the synchrony of discharge of close pairs of neurons, recorded by the same electrode, with remote pairs, recorded by different ones. However, spike trains of neighboring cells recorded by the same extracellular electrode exhibit the shadowing effect; i.e., lack of detection of spikes that occur within a few milliseconds of each other.Here, we demonstrate that the shadowing artifact can both induce apparent correlations between non-correlated neurons, as well as conceal existing correlations between neighboring ones. We therefore introduced artificial shadowing in the remote pairs, similar to the effect we observed in the close ones. After the artificial shadowing, neighboring cells did not show a higher tendency to oscillate synchronously than remote ones. On the contrary, the average percentage (over all sessions) of artificially shadowed remote pairs exhibiting synchronous oscillations was 35.4% compared to 17.2% in the close ones. Similar trend was found when the unshadowed remote pairs were separated according to the estimated distance between electrode tips: 29.9% of pairs at approximate distance of less than 750 µm were significantly synchronized, in comparison with 28.5% of the pairs whose distance was more than 750 µm.We conclude that the synchronous oscillations in the GP of MPTP treated primates are homogenously distributed.http://journal.frontiersin.org/Journal/10.3389/fnsys.2011.00054/fullBasal GangliaGlobus PallidussynchronizationoscillationsPrimateMPTP
spellingShingle Rea eMitelman
Rea eMitelman
Boris eRosin
Hila eZadka
Hila eZadka
Maya eSlovik
Gali eHeimer
Ya'acov eRitov
Ya'acov eRitov
Hagai eBergman
Hagai eBergman
Hagai eBergman
Shlomo eElias
Shlomo eElias
Neighboring pallidal neurons do not exhibit more synchronous oscillations than remote ones in the MPTP primate model of Parkinson’s disease
Frontiers in Systems Neuroscience
Basal Ganglia
Globus Pallidus
synchronization
oscillations
Primate
MPTP
title Neighboring pallidal neurons do not exhibit more synchronous oscillations than remote ones in the MPTP primate model of Parkinson’s disease
title_full Neighboring pallidal neurons do not exhibit more synchronous oscillations than remote ones in the MPTP primate model of Parkinson’s disease
title_fullStr Neighboring pallidal neurons do not exhibit more synchronous oscillations than remote ones in the MPTP primate model of Parkinson’s disease
title_full_unstemmed Neighboring pallidal neurons do not exhibit more synchronous oscillations than remote ones in the MPTP primate model of Parkinson’s disease
title_short Neighboring pallidal neurons do not exhibit more synchronous oscillations than remote ones in the MPTP primate model of Parkinson’s disease
title_sort neighboring pallidal neurons do not exhibit more synchronous oscillations than remote ones in the mptp primate model of parkinson s disease
topic Basal Ganglia
Globus Pallidus
synchronization
oscillations
Primate
MPTP
url http://journal.frontiersin.org/Journal/10.3389/fnsys.2011.00054/full
work_keys_str_mv AT reaemitelman neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease
AT reaemitelman neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease
AT boriserosin neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease
AT hilaezadka neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease
AT hilaezadka neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease
AT mayaeslovik neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease
AT galieheimer neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease
AT yaacoveritov neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease
AT yaacoveritov neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease
AT hagaiebergman neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease
AT hagaiebergman neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease
AT hagaiebergman neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease
AT shlomoeelias neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease
AT shlomoeelias neighboringpallidalneuronsdonotexhibitmoresynchronousoscillationsthanremoteonesinthemptpprimatemodelofparkinsonsdisease