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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.


Related in: MedlinePlus

The firing of PV+/Scgn- and PV+/Scgn+ striatal interneurons is distinctly phase locked to cortical oscillations in the rat.(A,B) Mean phase histograms of the firing of striatal PV+/Scgn- (A) and PV+/Scgn+ (B) interneurons with respect to cortical oscillations of 0.4–80 Hz during SWA. Note the stronger locking of the firing of PV+/Scgn- interneurons to slow (0.4–1.6 Hz) and spindle (7–12 Hz) frequencies, and the stronger locking of PV+/Scgn+ interneurons to gamma oscillations (30–80 Hz) (C) Histogram showing the proportions of PV+/Scgn- (green) and PV+/Scgn+ (blue) interneurons that exhibited significantly phase-locked firing (as measured by the Raleigh test, with p<0.05) in each frequency range of cortical oscillation during SWA. (D) Mean vector lengths calculated across all PV+/Scgn- (green) and PV+/Scgn+ (blue) neurons recorded during SWA (PV+/Scgn+ n = 9; PV+/Scgn- n = 8) from 0 to 80 Hz. Shaded areas show SEMs across neurons. (E,F) Mean phase histograms of striatal PV+/Scgn- (E) and PV+/Scgn+ (F) interneurons for cortical oscillations of 0.4–80 Hz during cortical activation. (G) Histogram showing the proportions of PV+/Scgn- (green) and PV+/Scgn+ (blue) neurons that were significantly locked in each frequency range of cortical oscillation during cortical activation. (H) Mean vector lengths calculated across all PV+/Scgn- (green) and PV+/Scgn+ (blue) neurons recorded during cortical activation (PV+/Scgn+ n = 11; PV+/Scgn- n = 7). Shaded areas show SEMs across neurons. (A, B, E, F, frequencies between 0–5 Hz are separated to allow for a wider color scale)DOI:http://dx.doi.org/10.7554/eLife.16088.01210.7554/eLife.16088.013Figure 6—source data 1.Source data for Figures 6C,D,G,H.DOI:http://dx.doi.org/10.7554/eLife.16088.013
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fig6: The firing of PV+/Scgn- and PV+/Scgn+ striatal interneurons is distinctly phase locked to cortical oscillations in the rat.(A,B) Mean phase histograms of the firing of striatal PV+/Scgn- (A) and PV+/Scgn+ (B) interneurons with respect to cortical oscillations of 0.4–80 Hz during SWA. Note the stronger locking of the firing of PV+/Scgn- interneurons to slow (0.4–1.6 Hz) and spindle (7–12 Hz) frequencies, and the stronger locking of PV+/Scgn+ interneurons to gamma oscillations (30–80 Hz) (C) Histogram showing the proportions of PV+/Scgn- (green) and PV+/Scgn+ (blue) interneurons that exhibited significantly phase-locked firing (as measured by the Raleigh test, with p<0.05) in each frequency range of cortical oscillation during SWA. (D) Mean vector lengths calculated across all PV+/Scgn- (green) and PV+/Scgn+ (blue) neurons recorded during SWA (PV+/Scgn+ n = 9; PV+/Scgn- n = 8) from 0 to 80 Hz. Shaded areas show SEMs across neurons. (E,F) Mean phase histograms of striatal PV+/Scgn- (E) and PV+/Scgn+ (F) interneurons for cortical oscillations of 0.4–80 Hz during cortical activation. (G) Histogram showing the proportions of PV+/Scgn- (green) and PV+/Scgn+ (blue) neurons that were significantly locked in each frequency range of cortical oscillation during cortical activation. (H) Mean vector lengths calculated across all PV+/Scgn- (green) and PV+/Scgn+ (blue) neurons recorded during cortical activation (PV+/Scgn+ n = 11; PV+/Scgn- n = 7). Shaded areas show SEMs across neurons. (A, B, E, F, frequencies between 0–5 Hz are separated to allow for a wider color scale)DOI:http://dx.doi.org/10.7554/eLife.16088.01210.7554/eLife.16088.013Figure 6—source data 1.Source data for Figures 6C,D,G,H.DOI:http://dx.doi.org/10.7554/eLife.16088.013

Mentions: Identified striatal PV+ interneurons, as well as FSIs, show a strong tendency to phase lock their firing to cortical oscillations (Berke, 2004, 2009; Sharott et al., 2012). Thus, we next examined whether PV+/Scgn- and PV+/Scgn+ interneurons fired differently with respect to the phase of cortical population oscillations (as recorded in ipsilateral, frontal ECoG) across frequencies from 0.4–80 Hz in SWA and cortical activation (Figure 6). As suggested by the raw data (Figure 4), both PV+/Scgn- and PV+/Scgn+ interneurons tended to fire around the peaks of cortical slow oscillations (0.4–1.6 Hz) during SWA (Figure 6A,B). Although the firing of all PV+ interneurons was significantly locked to cortical slow oscillations to some extent (Figure 6C, Figure 6—source data 1), the locking across the population was stronger in the PV+/Scgn- neurons (Figure 6A,B). In line with these results, the vector length of firing of PV+/Scgn- interneurons was around twice that of PV+/Scgn+ interneurons (Figure 6D; Mann Whitney, p=0.04). Similarly, the firing of PV+/Scgn- interneurons was more strongly locked to cortical spindle oscillations (7–12 Hz), which was reflected in both a greater number of significantly locked neurons (Figure 6C, Figure 6—source data 1) and greater vector length (Figure 6D, Mann Whitney, p=0.008). In contrast, the firing of PV+/Scgn+ interneurons was more tightly locked to cortical gamma (30–80 Hz) oscillations (Figure 6A,B), and a greater proportion of PV+/Scgn+ interneurons were significantly locked to gamma oscillations (Figure 6C). The phase-locked firing of PV+/Scgn- and PV+/Scgn+ interneurons was generally more similar across all cortical oscillation frequencies during the activated brain state (Figure 6E,F,H, Figure 6—source data 1). However, around three times as many PV+/Scgn+ interneurons were locked at gamma frequencies between 30 and 60 Hz as compared to PV+/Scgn- interneurons (Figure 6G, Figure 6—source data 1). These results indicate that the temporal organization of the firing of PV+/Scgn- and PV+/Scgn+ interneurons with respect to ongoing cortical oscillations is distinct and brain state-dependent, thus demonstrating further physiological divergence between these cell populations.10.7554/eLife.16088.012Figure 6.The firing of PV+/Scgn- and PV+/Scgn+ striatal interneurons is distinctly phase locked to cortical oscillations in the rat.


Secretagogin expression delineates functionally-specialized populations of striatal parvalbumin-containing interneurons
The firing of PV+/Scgn- and PV+/Scgn+ striatal interneurons is distinctly phase locked to cortical oscillations in the rat.(A,B) Mean phase histograms of the firing of striatal PV+/Scgn- (A) and PV+/Scgn+ (B) interneurons with respect to cortical oscillations of 0.4–80 Hz during SWA. Note the stronger locking of the firing of PV+/Scgn- interneurons to slow (0.4–1.6 Hz) and spindle (7–12 Hz) frequencies, and the stronger locking of PV+/Scgn+ interneurons to gamma oscillations (30–80 Hz) (C) Histogram showing the proportions of PV+/Scgn- (green) and PV+/Scgn+ (blue) interneurons that exhibited significantly phase-locked firing (as measured by the Raleigh test, with p<0.05) in each frequency range of cortical oscillation during SWA. (D) Mean vector lengths calculated across all PV+/Scgn- (green) and PV+/Scgn+ (blue) neurons recorded during SWA (PV+/Scgn+ n = 9; PV+/Scgn- n = 8) from 0 to 80 Hz. Shaded areas show SEMs across neurons. (E,F) Mean phase histograms of striatal PV+/Scgn- (E) and PV+/Scgn+ (F) interneurons for cortical oscillations of 0.4–80 Hz during cortical activation. (G) Histogram showing the proportions of PV+/Scgn- (green) and PV+/Scgn+ (blue) neurons that were significantly locked in each frequency range of cortical oscillation during cortical activation. (H) Mean vector lengths calculated across all PV+/Scgn- (green) and PV+/Scgn+ (blue) neurons recorded during cortical activation (PV+/Scgn+ n = 11; PV+/Scgn- n = 7). Shaded areas show SEMs across neurons. (A, B, E, F, frequencies between 0–5 Hz are separated to allow for a wider color scale)DOI:http://dx.doi.org/10.7554/eLife.16088.01210.7554/eLife.16088.013Figure 6—source data 1.Source data for Figures 6C,D,G,H.DOI:http://dx.doi.org/10.7554/eLife.16088.013
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fig6: The firing of PV+/Scgn- and PV+/Scgn+ striatal interneurons is distinctly phase locked to cortical oscillations in the rat.(A,B) Mean phase histograms of the firing of striatal PV+/Scgn- (A) and PV+/Scgn+ (B) interneurons with respect to cortical oscillations of 0.4–80 Hz during SWA. Note the stronger locking of the firing of PV+/Scgn- interneurons to slow (0.4–1.6 Hz) and spindle (7–12 Hz) frequencies, and the stronger locking of PV+/Scgn+ interneurons to gamma oscillations (30–80 Hz) (C) Histogram showing the proportions of PV+/Scgn- (green) and PV+/Scgn+ (blue) interneurons that exhibited significantly phase-locked firing (as measured by the Raleigh test, with p<0.05) in each frequency range of cortical oscillation during SWA. (D) Mean vector lengths calculated across all PV+/Scgn- (green) and PV+/Scgn+ (blue) neurons recorded during SWA (PV+/Scgn+ n = 9; PV+/Scgn- n = 8) from 0 to 80 Hz. Shaded areas show SEMs across neurons. (E,F) Mean phase histograms of striatal PV+/Scgn- (E) and PV+/Scgn+ (F) interneurons for cortical oscillations of 0.4–80 Hz during cortical activation. (G) Histogram showing the proportions of PV+/Scgn- (green) and PV+/Scgn+ (blue) neurons that were significantly locked in each frequency range of cortical oscillation during cortical activation. (H) Mean vector lengths calculated across all PV+/Scgn- (green) and PV+/Scgn+ (blue) neurons recorded during cortical activation (PV+/Scgn+ n = 11; PV+/Scgn- n = 7). Shaded areas show SEMs across neurons. (A, B, E, F, frequencies between 0–5 Hz are separated to allow for a wider color scale)DOI:http://dx.doi.org/10.7554/eLife.16088.01210.7554/eLife.16088.013Figure 6—source data 1.Source data for Figures 6C,D,G,H.DOI:http://dx.doi.org/10.7554/eLife.16088.013
Mentions: Identified striatal PV+ interneurons, as well as FSIs, show a strong tendency to phase lock their firing to cortical oscillations (Berke, 2004, 2009; Sharott et al., 2012). Thus, we next examined whether PV+/Scgn- and PV+/Scgn+ interneurons fired differently with respect to the phase of cortical population oscillations (as recorded in ipsilateral, frontal ECoG) across frequencies from 0.4–80 Hz in SWA and cortical activation (Figure 6). As suggested by the raw data (Figure 4), both PV+/Scgn- and PV+/Scgn+ interneurons tended to fire around the peaks of cortical slow oscillations (0.4–1.6 Hz) during SWA (Figure 6A,B). Although the firing of all PV+ interneurons was significantly locked to cortical slow oscillations to some extent (Figure 6C, Figure 6—source data 1), the locking across the population was stronger in the PV+/Scgn- neurons (Figure 6A,B). In line with these results, the vector length of firing of PV+/Scgn- interneurons was around twice that of PV+/Scgn+ interneurons (Figure 6D; Mann Whitney, p=0.04). Similarly, the firing of PV+/Scgn- interneurons was more strongly locked to cortical spindle oscillations (7–12 Hz), which was reflected in both a greater number of significantly locked neurons (Figure 6C, Figure 6—source data 1) and greater vector length (Figure 6D, Mann Whitney, p=0.008). In contrast, the firing of PV+/Scgn+ interneurons was more tightly locked to cortical gamma (30–80 Hz) oscillations (Figure 6A,B), and a greater proportion of PV+/Scgn+ interneurons were significantly locked to gamma oscillations (Figure 6C). The phase-locked firing of PV+/Scgn- and PV+/Scgn+ interneurons was generally more similar across all cortical oscillation frequencies during the activated brain state (Figure 6E,F,H, Figure 6—source data 1). However, around three times as many PV+/Scgn+ interneurons were locked at gamma frequencies between 30 and 60 Hz as compared to PV+/Scgn- interneurons (Figure 6G, Figure 6—source data 1). These results indicate that the temporal organization of the firing of PV+/Scgn- and PV+/Scgn+ interneurons with respect to ongoing cortical oscillations is distinct and brain state-dependent, thus demonstrating further physiological divergence between these cell populations.10.7554/eLife.16088.012Figure 6.The firing of PV+/Scgn- and PV+/Scgn+ striatal interneurons is distinctly phase locked to cortical oscillations 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 &lsquo;direct pathway&rsquo;, whereas PV+/Scgn- interneurons preferentially targeted &lsquo;indirect pathway&rsquo; 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.


Related in: MedlinePlus