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

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.


Related in: MedlinePlus

PV+/Scgn+ and PV+/Scgn- interneurons have different biases in their distributions in the caudate and putamen of macaque monkey.(Ai, Aii) Confocal micrographs of the macaque striatum showing PV-expressing interneurons that co-expressed (Ai) and did not co-express (Aii) Scgn (arrow). (B) Typical distributions of PV+/Scgn- interneurons (left) and PV+/Scgn+ interneurons (right) across 7 coronal planes of macaque caudate and putamen, with each dot representing a single neuron. (C) Mean densities of all PV+ interneurons across the entirety of the caudate nucleus (Ci) and the putamen (Cii), including those populations that co-express Scgn (blue) and do not express Scgn (green). In the macaque caudate-putamen, PV+/Scgn+ neurons represent nearly three quarters of all PV-expressing neurons. Dots and squares indicate the values for individual animals. (D) Densities of PV+/Scgn+ interneurons (blue) and PV+/Scgn- interneurons (green) along the rostro-caudal axis of the caudate (Di) and the putamen (Dii). Note that the PV+/Scgn+ population in the macaque increases in density towards the caudal planes of the caudate and the putamen. (E) Medio-lateral distribution of PV+/Scgn+ and PV+/Scgn- interneurons along 7 coronal planes of the caudate nucleus (Ei) and the putamen (Eii). The presence of the asterisk (*) indicates a distribution that is significantly biased in one direction along the specified axis. Squares (□) indicate a significant difference in the distribution of the two PV+ interneuron populations along the specified axis within a given coronal plane. Data are means of the position of all neurons counted ± SEMs.DOI:http://dx.doi.org/10.7554/eLife.16088.00710.7554/eLife.16088.008Figure 3—source data 1.Source data for Figures 3B–E.DOI:http://dx.doi.org/10.7554/eLife.16088.008
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC5036963&req=5

fig3: PV+/Scgn+ and PV+/Scgn- interneurons have different biases in their distributions in the caudate and putamen of macaque monkey.(Ai, Aii) Confocal micrographs of the macaque striatum showing PV-expressing interneurons that co-expressed (Ai) and did not co-express (Aii) Scgn (arrow). (B) Typical distributions of PV+/Scgn- interneurons (left) and PV+/Scgn+ interneurons (right) across 7 coronal planes of macaque caudate and putamen, with each dot representing a single neuron. (C) Mean densities of all PV+ interneurons across the entirety of the caudate nucleus (Ci) and the putamen (Cii), including those populations that co-express Scgn (blue) and do not express Scgn (green). In the macaque caudate-putamen, PV+/Scgn+ neurons represent nearly three quarters of all PV-expressing neurons. Dots and squares indicate the values for individual animals. (D) Densities of PV+/Scgn+ interneurons (blue) and PV+/Scgn- interneurons (green) along the rostro-caudal axis of the caudate (Di) and the putamen (Dii). Note that the PV+/Scgn+ population in the macaque increases in density towards the caudal planes of the caudate and the putamen. (E) Medio-lateral distribution of PV+/Scgn+ and PV+/Scgn- interneurons along 7 coronal planes of the caudate nucleus (Ei) and the putamen (Eii). The presence of the asterisk (*) indicates a distribution that is significantly biased in one direction along the specified axis. Squares (□) indicate a significant difference in the distribution of the two PV+ interneuron populations along the specified axis within a given coronal plane. Data are means of the position of all neurons counted ± SEMs.DOI:http://dx.doi.org/10.7554/eLife.16088.00710.7554/eLife.16088.008Figure 3—source data 1.Source data for Figures 3B–E.DOI:http://dx.doi.org/10.7554/eLife.16088.008

Mentions: Our data in rats and mice show that the co-expression of Scgn by striatal PV+ interneurons is not highly conserved across rodent species. Because Scgn+ neurons have also been reported in the primate striatum (Mulder et al., 2009), we further explored the possibility of phylogenetic conservation by analyzing the co-expression of PV and Scgn in interneurons of the monkey (rhesus macaque) striatum. Secretagogin was expressed by some neurons in both the caudate nucleus and putamen of monkeys; it was frequently co-expressed with PV (Figure 3A–C, Figure 3—source data 1). Compared to the rat, co-expression of PV and Scgn was more common in primates; about three quarters of PV+ interneurons in caudate nucleus and putamen also expressed Scgn (Figure 3C, Figure 3—source data 1). Thus, Scgn is itself a novel marker of a major class of striatal interneuron in both monkeys and rats. Along the rostro-caudal axis of monkey striatum, but most notably in the caudate nucleus, there was a marked increase in the density of PV+/Scgn+ interneurons in caudal planes (Figure 3D, Supplementary file 2, Figure 3—source data 1), mirroring the biased rostro-caudal distribution of PV+/Scgn+ interneurons in the rat striatum (Figure 2B). The density of PV+/Scgn- interneurons remained relatively constant across the rostro-caudal extent of monkey striatum, which is again in line with our observations in rats (Figure 3D, Supplementary file 2, Figure 3—source data 1.). Interestingly, the distribution of PV+/Scgn- interneurons, but not PV+/Scgn+ neurons, was laterally biased throughout rostro-caudal aspect putamen, but not caudate (Figure 3E, Supplementary file 2, Figure 3—source data 1). When taken together, the data from monkey and rat not only show that a substantial proportion of striatal PV+ interneurons co-express Scgn, a population enriched in caudal striatum, but also that these novel constituents of the striatal microcircuit are phylogenetically conserved to some extent.10.7554/eLife.16088.007Figure 3.PV+/Scgn+ and PV+/Scgn- interneurons have different biases in their distributions in the caudate and putamen of macaque monkey.


Secretagogin expression delineates functionally-specialized populations of striatal parvalbumin-containing interneurons
PV+/Scgn+ and PV+/Scgn- interneurons have different biases in their distributions in the caudate and putamen of macaque monkey.(Ai, Aii) Confocal micrographs of the macaque striatum showing PV-expressing interneurons that co-expressed (Ai) and did not co-express (Aii) Scgn (arrow). (B) Typical distributions of PV+/Scgn- interneurons (left) and PV+/Scgn+ interneurons (right) across 7 coronal planes of macaque caudate and putamen, with each dot representing a single neuron. (C) Mean densities of all PV+ interneurons across the entirety of the caudate nucleus (Ci) and the putamen (Cii), including those populations that co-express Scgn (blue) and do not express Scgn (green). In the macaque caudate-putamen, PV+/Scgn+ neurons represent nearly three quarters of all PV-expressing neurons. Dots and squares indicate the values for individual animals. (D) Densities of PV+/Scgn+ interneurons (blue) and PV+/Scgn- interneurons (green) along the rostro-caudal axis of the caudate (Di) and the putamen (Dii). Note that the PV+/Scgn+ population in the macaque increases in density towards the caudal planes of the caudate and the putamen. (E) Medio-lateral distribution of PV+/Scgn+ and PV+/Scgn- interneurons along 7 coronal planes of the caudate nucleus (Ei) and the putamen (Eii). The presence of the asterisk (*) indicates a distribution that is significantly biased in one direction along the specified axis. Squares (□) indicate a significant difference in the distribution of the two PV+ interneuron populations along the specified axis within a given coronal plane. Data are means of the position of all neurons counted ± SEMs.DOI:http://dx.doi.org/10.7554/eLife.16088.00710.7554/eLife.16088.008Figure 3—source data 1.Source data for Figures 3B–E.DOI:http://dx.doi.org/10.7554/eLife.16088.008
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5036963&req=5

fig3: PV+/Scgn+ and PV+/Scgn- interneurons have different biases in their distributions in the caudate and putamen of macaque monkey.(Ai, Aii) Confocal micrographs of the macaque striatum showing PV-expressing interneurons that co-expressed (Ai) and did not co-express (Aii) Scgn (arrow). (B) Typical distributions of PV+/Scgn- interneurons (left) and PV+/Scgn+ interneurons (right) across 7 coronal planes of macaque caudate and putamen, with each dot representing a single neuron. (C) Mean densities of all PV+ interneurons across the entirety of the caudate nucleus (Ci) and the putamen (Cii), including those populations that co-express Scgn (blue) and do not express Scgn (green). In the macaque caudate-putamen, PV+/Scgn+ neurons represent nearly three quarters of all PV-expressing neurons. Dots and squares indicate the values for individual animals. (D) Densities of PV+/Scgn+ interneurons (blue) and PV+/Scgn- interneurons (green) along the rostro-caudal axis of the caudate (Di) and the putamen (Dii). Note that the PV+/Scgn+ population in the macaque increases in density towards the caudal planes of the caudate and the putamen. (E) Medio-lateral distribution of PV+/Scgn+ and PV+/Scgn- interneurons along 7 coronal planes of the caudate nucleus (Ei) and the putamen (Eii). The presence of the asterisk (*) indicates a distribution that is significantly biased in one direction along the specified axis. Squares (□) indicate a significant difference in the distribution of the two PV+ interneuron populations along the specified axis within a given coronal plane. Data are means of the position of all neurons counted ± SEMs.DOI:http://dx.doi.org/10.7554/eLife.16088.00710.7554/eLife.16088.008Figure 3—source data 1.Source data for Figures 3B–E.DOI:http://dx.doi.org/10.7554/eLife.16088.008
Mentions: Our data in rats and mice show that the co-expression of Scgn by striatal PV+ interneurons is not highly conserved across rodent species. Because Scgn+ neurons have also been reported in the primate striatum (Mulder et al., 2009), we further explored the possibility of phylogenetic conservation by analyzing the co-expression of PV and Scgn in interneurons of the monkey (rhesus macaque) striatum. Secretagogin was expressed by some neurons in both the caudate nucleus and putamen of monkeys; it was frequently co-expressed with PV (Figure 3A–C, Figure 3—source data 1). Compared to the rat, co-expression of PV and Scgn was more common in primates; about three quarters of PV+ interneurons in caudate nucleus and putamen also expressed Scgn (Figure 3C, Figure 3—source data 1). Thus, Scgn is itself a novel marker of a major class of striatal interneuron in both monkeys and rats. Along the rostro-caudal axis of monkey striatum, but most notably in the caudate nucleus, there was a marked increase in the density of PV+/Scgn+ interneurons in caudal planes (Figure 3D, Supplementary file 2, Figure 3—source data 1), mirroring the biased rostro-caudal distribution of PV+/Scgn+ interneurons in the rat striatum (Figure 2B). The density of PV+/Scgn- interneurons remained relatively constant across the rostro-caudal extent of monkey striatum, which is again in line with our observations in rats (Figure 3D, Supplementary file 2, Figure 3—source data 1.). Interestingly, the distribution of PV+/Scgn- interneurons, but not PV+/Scgn+ neurons, was laterally biased throughout rostro-caudal aspect putamen, but not caudate (Figure 3E, Supplementary file 2, Figure 3—source data 1). When taken together, the data from monkey and rat not only show that a substantial proportion of striatal PV+ interneurons co-express Scgn, a population enriched in caudal striatum, but also that these novel constituents of the striatal microcircuit are phylogenetically conserved to some extent.10.7554/eLife.16088.007Figure 3.PV+/Scgn+ and PV+/Scgn- interneurons have different biases in their distributions in the caudate and putamen of macaque monkey.

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.


Related in: MedlinePlus