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Secretagogin expression delineates functionally-specialized populations of striatal parvalbumin-containing interneurons

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ABSTRACT

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.

Doi:: http://dx.doi.org/10.7554/eLife.16088.001

No MeSH data available.


In vivo electrophysiological properties of identified PV+/Scgn- and PV+/Scgn+ striatal interneurons in the rat.(A,D) Juxtacellularly-labeled PV+/Scgn- interneurons (A,B) and PV+/Scgn+ interneurons (C,D), identified by their co-localization of fluorescent labeling for neurobiotin (NB) and calcium-binding proteins. PV+ interneurons were recorded in the rostral (Aii), central (Cii) and caudal (Bii, Dii) aspects of dorsal striatum. (Aiii–Diii) Spontaneous action potential discharges (unit activity) of the same individual PV+/Scgn- and PV+/Scgn+ interneurons during robust cortical slow-wave activity (SWA), defined using the frontal electrocorticogram (ECoG). (Aiv–Div) Firing of the same interneurons during spontaneous cortical activation. (Ai–Di) Scale bars are 20 µM. (Aii–iii-Dii-iii) Vertical scale bars for unit activity are 0.5 mV; Vertical scale bars for ECoG are 1 mV; Horizontal scale bars are 1 s).DOI:http://dx.doi.org/10.7554/eLife.16088.009
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fig4: In vivo electrophysiological properties of identified PV+/Scgn- and PV+/Scgn+ striatal interneurons in the rat.(A,D) Juxtacellularly-labeled PV+/Scgn- interneurons (A,B) and PV+/Scgn+ interneurons (C,D), identified by their co-localization of fluorescent labeling for neurobiotin (NB) and calcium-binding proteins. PV+ interneurons were recorded in the rostral (Aii), central (Cii) and caudal (Bii, Dii) aspects of dorsal striatum. (Aiii–Diii) Spontaneous action potential discharges (unit activity) of the same individual PV+/Scgn- and PV+/Scgn+ interneurons during robust cortical slow-wave activity (SWA), defined using the frontal electrocorticogram (ECoG). (Aiv–Div) Firing of the same interneurons during spontaneous cortical activation. (Ai–Di) Scale bars are 20 µM. (Aii–iii-Dii-iii) Vertical scale bars for unit activity are 0.5 mV; Vertical scale bars for ECoG are 1 mV; Horizontal scale bars are 1 s).DOI:http://dx.doi.org/10.7554/eLife.16088.009

Mentions: As previously described, PV+ interneurons display the most diverse in vivo firing rates/patterns of the major striatal interneuron types in the rat (Sharott et al., 2012). We next investigated whether the selective expression of Scgn could account for any of the variability in the activity of striatal PV+ interneurons. We thus extracellularly recorded the action potentials fired by individual interneurons in the dorsal striatum of anesthetized rats, and then juxtacellularly labeled the same interneurons with neurobiotin for posthoc verification of their neurochemical identities and locations (Figure 4). We focused our analyses on the firing of identified PV+ interneurons during two distinct brain states, slow-wave activity (SWA) and ‘cortical activation’ (Sharott et al., 2012), as defined by simultaneous recordings of the electrocorticogram (ECoG).10.7554/eLife.16088.009Figure 4.In vivo electrophysiological properties of identified PV+/Scgn- and PV+/Scgn+ striatal interneurons in the rat.


Secretagogin expression delineates functionally-specialized populations of striatal parvalbumin-containing interneurons
In vivo electrophysiological properties of identified PV+/Scgn- and PV+/Scgn+ striatal interneurons in the rat.(A,D) Juxtacellularly-labeled PV+/Scgn- interneurons (A,B) and PV+/Scgn+ interneurons (C,D), identified by their co-localization of fluorescent labeling for neurobiotin (NB) and calcium-binding proteins. PV+ interneurons were recorded in the rostral (Aii), central (Cii) and caudal (Bii, Dii) aspects of dorsal striatum. (Aiii–Diii) Spontaneous action potential discharges (unit activity) of the same individual PV+/Scgn- and PV+/Scgn+ interneurons during robust cortical slow-wave activity (SWA), defined using the frontal electrocorticogram (ECoG). (Aiv–Div) Firing of the same interneurons during spontaneous cortical activation. (Ai–Di) Scale bars are 20 µM. (Aii–iii-Dii-iii) Vertical scale bars for unit activity are 0.5 mV; Vertical scale bars for ECoG are 1 mV; Horizontal scale bars are 1 s).DOI:http://dx.doi.org/10.7554/eLife.16088.009
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Related In: Results  -  Collection

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fig4: In vivo electrophysiological properties of identified PV+/Scgn- and PV+/Scgn+ striatal interneurons in the rat.(A,D) Juxtacellularly-labeled PV+/Scgn- interneurons (A,B) and PV+/Scgn+ interneurons (C,D), identified by their co-localization of fluorescent labeling for neurobiotin (NB) and calcium-binding proteins. PV+ interneurons were recorded in the rostral (Aii), central (Cii) and caudal (Bii, Dii) aspects of dorsal striatum. (Aiii–Diii) Spontaneous action potential discharges (unit activity) of the same individual PV+/Scgn- and PV+/Scgn+ interneurons during robust cortical slow-wave activity (SWA), defined using the frontal electrocorticogram (ECoG). (Aiv–Div) Firing of the same interneurons during spontaneous cortical activation. (Ai–Di) Scale bars are 20 µM. (Aii–iii-Dii-iii) Vertical scale bars for unit activity are 0.5 mV; Vertical scale bars for ECoG are 1 mV; Horizontal scale bars are 1 s).DOI:http://dx.doi.org/10.7554/eLife.16088.009
Mentions: As previously described, PV+ interneurons display the most diverse in vivo firing rates/patterns of the major striatal interneuron types in the rat (Sharott et al., 2012). We next investigated whether the selective expression of Scgn could account for any of the variability in the activity of striatal PV+ interneurons. We thus extracellularly recorded the action potentials fired by individual interneurons in the dorsal striatum of anesthetized rats, and then juxtacellularly labeled the same interneurons with neurobiotin for posthoc verification of their neurochemical identities and locations (Figure 4). We focused our analyses on the firing of identified PV+ interneurons during two distinct brain states, slow-wave activity (SWA) and ‘cortical activation’ (Sharott et al., 2012), as defined by simultaneous recordings of the electrocorticogram (ECoG).10.7554/eLife.16088.009Figure 4.In vivo electrophysiological properties of identified PV+/Scgn- and PV+/Scgn+ striatal interneurons in the rat.

View Article: PubMed Central - PubMed

ABSTRACT

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.

Doi:: http://dx.doi.org/10.7554/eLife.16088.001

No MeSH data available.