Secretagogin expression delineates functionally-specialized populations of striatal parvalbumin-containing interneurons
Corticostriatal afferents can engage parvalbumin-expressing (PV+) interneurons to rapidly curtail the activity of striatal projection neurons (SPNs), thus shaping striatal output. Schemes of basal ganglia circuit dynamics generally consider striatal PV+ interneurons to be homogenous, despite conside...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2016-09-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/16088 |
| _version_ | 1818019760124723200 |
|---|---|
| author | Farid N Garas Rahul S Shah Eszter Kormann Natalie M Doig Federica Vinciati Kouichi C Nakamura Matthijs C Dorst Yoland Smith Peter J Magill Andrew Sharott |
| author_facet | Farid N Garas Rahul S Shah Eszter Kormann Natalie M Doig Federica Vinciati Kouichi C Nakamura Matthijs C Dorst Yoland Smith Peter J Magill Andrew Sharott |
| author_sort | Farid N Garas |
| collection | DOAJ |
| description | Corticostriatal afferents can engage parvalbumin-expressing (PV+) interneurons to rapidly curtail the activity of striatal projection neurons (SPNs), thus shaping striatal output. Schemes of basal ganglia circuit dynamics generally consider striatal PV+ interneurons to be homogenous, despite considerable heterogeneity in both form and function. We demonstrate that the selective co-expression of another calcium-binding protein, secretagogin (Scgn), separates PV+ interneurons in rat and primate striatum into two topographically-, physiologically- and structurally-distinct cell populations. In rats, these two interneuron populations differed in their firing rates, patterns and relationships with cortical oscillations in vivo. Moreover, the axons of identified PV+/Scgn+ interneurons preferentially targeted the somata of SPNs of the so-called ‘direct pathway’, whereas PV+/Scgn- interneurons preferentially targeted ‘indirect pathway’ SPNs. These two populations of interneurons could therefore provide a substrate through which either of the striatal output pathways can be rapidly and selectively inhibited to subsequently mediate the expression of behavioral routines. |
| first_indexed | 2024-04-14T07:56:36Z |
| format | Article |
| id | doaj.art-47215ca2f5fb4805a7fea1929266cda8 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-14T07:56:36Z |
| publishDate | 2016-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-47215ca2f5fb4805a7fea1929266cda82022-12-22T02:05:03ZengeLife Sciences Publications LtdeLife2050-084X2016-09-01510.7554/eLife.16088Secretagogin expression delineates functionally-specialized populations of striatal parvalbumin-containing interneuronsFarid N Garas0Rahul S Shah1https://orcid.org/0000-0002-8616-8693Eszter Kormann2Natalie M Doig3https://orcid.org/0000-0001-6821-0264Federica Vinciati4Kouichi C Nakamura5https://orcid.org/0000-0001-7053-0507Matthijs C Dorst6https://orcid.org/0000-0002-1162-1481Yoland Smith7Peter J Magill8https://orcid.org/0000-0001-7141-7071Andrew Sharott9https://orcid.org/0000-0002-1594-3349Medical Research Council Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Oxford, United KingdomMedical Research Council Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Oxford, United KingdomMedical Research Council Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Oxford, United KingdomMedical Research Council Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Oxford, United KingdomMedical Research Council Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Oxford, United KingdomMedical Research Council Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Oxford, United KingdomDepartment of Neuroscience, Karolinska Institutet, Stockholm, SwedenYerkes National Primate Research Center, Department of Neurology, Emory University, Atlanta, United States; Udall Center of Excellence for Parkinson's Disease Research, Emory University, Atlanta, United StatesMedical Research Council Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Oxford, United KingdomMedical Research Council Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Oxford, United KingdomCorticostriatal afferents can engage parvalbumin-expressing (PV+) interneurons to rapidly curtail the activity of striatal projection neurons (SPNs), thus shaping striatal output. Schemes of basal ganglia circuit dynamics generally consider striatal PV+ interneurons to be homogenous, despite considerable heterogeneity in both form and function. We demonstrate that the selective co-expression of another calcium-binding protein, secretagogin (Scgn), separates PV+ interneurons in rat and primate striatum into two topographically-, physiologically- and structurally-distinct cell populations. In rats, these two interneuron populations differed in their firing rates, patterns and relationships with cortical oscillations in vivo. Moreover, the axons of identified PV+/Scgn+ interneurons preferentially targeted the somata of SPNs of the so-called ‘direct pathway’, whereas PV+/Scgn- interneurons preferentially targeted ‘indirect pathway’ SPNs. These two populations of interneurons could therefore provide a substrate through which either of the striatal output pathways can be rapidly and selectively inhibited to subsequently mediate the expression of behavioral routines.https://elifesciences.org/articles/16088striatuminterneuronparvalbuminsecretagogin |
| spellingShingle | Farid N Garas Rahul S Shah Eszter Kormann Natalie M Doig Federica Vinciati Kouichi C Nakamura Matthijs C Dorst Yoland Smith Peter J Magill Andrew Sharott Secretagogin expression delineates functionally-specialized populations of striatal parvalbumin-containing interneurons eLife striatum interneuron parvalbumin secretagogin |
| title | Secretagogin expression delineates functionally-specialized populations of striatal parvalbumin-containing interneurons |
| title_full | Secretagogin expression delineates functionally-specialized populations of striatal parvalbumin-containing interneurons |
| title_fullStr | Secretagogin expression delineates functionally-specialized populations of striatal parvalbumin-containing interneurons |
| title_full_unstemmed | Secretagogin expression delineates functionally-specialized populations of striatal parvalbumin-containing interneurons |
| title_short | Secretagogin expression delineates functionally-specialized populations of striatal parvalbumin-containing interneurons |
| title_sort | secretagogin expression delineates functionally specialized populations of striatal parvalbumin containing interneurons |
| topic | striatum interneuron parvalbumin secretagogin |
| url | https://elifesciences.org/articles/16088 |
| work_keys_str_mv | AT faridngaras secretagoginexpressiondelineatesfunctionallyspecializedpopulationsofstriatalparvalbumincontaininginterneurons AT rahulsshah secretagoginexpressiondelineatesfunctionallyspecializedpopulationsofstriatalparvalbumincontaininginterneurons AT eszterkormann secretagoginexpressiondelineatesfunctionallyspecializedpopulationsofstriatalparvalbumincontaininginterneurons AT nataliemdoig secretagoginexpressiondelineatesfunctionallyspecializedpopulationsofstriatalparvalbumincontaininginterneurons AT federicavinciati secretagoginexpressiondelineatesfunctionallyspecializedpopulationsofstriatalparvalbumincontaininginterneurons AT kouichicnakamura secretagoginexpressiondelineatesfunctionallyspecializedpopulationsofstriatalparvalbumincontaininginterneurons AT matthijscdorst secretagoginexpressiondelineatesfunctionallyspecializedpopulationsofstriatalparvalbumincontaininginterneurons AT yolandsmith secretagoginexpressiondelineatesfunctionallyspecializedpopulationsofstriatalparvalbumincontaininginterneurons AT peterjmagill secretagoginexpressiondelineatesfunctionallyspecializedpopulationsofstriatalparvalbumincontaininginterneurons AT andrewsharott secretagoginexpressiondelineatesfunctionallyspecializedpopulationsofstriatalparvalbumincontaininginterneurons |