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The mouse primary visual cortex is a site of production and sensitivity to estrogens.

Jeong JK, Tremere LA, Burrows K, Majewska AK, Pinaud R - PLoS ONE (2011)

Bottom Line: We found that both monocular and binocular V1 are highly enriched in aromatase- and ER-positive neurons, indicating that V1 is a site of production and sensitivity to estrogens.Interestingly, acute episodes of visual experience do not affect the density or distribution of estrogen-associated circuits.Finally, we show that adult mice dark-reared from birth also exhibit normal distribution of aromatase and ERs throughout V1, suggesting that the implementation and maintenance of estrogen-associated circuits is independent of visual experience.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma, United States of America.

ABSTRACT
The classic female estrogen, 17β-estradiol (E2), has been repeatedly shown to affect the perceptual processing of visual cues. Although gonadal E2 has often been thought to influence these processes, the possibility that central visual processing may be modulated by brain-generated hormone has not been explored. Here we show that estrogen-associated circuits are highly prevalent in the mouse primary visual cortex (V1). Specifically, we cloned aromatase, a marker for estrogen-producing neurons, and the classic estrogen receptors (ERs) ERα and ERβ, as markers for estrogen-responsive neurons, and conducted a detailed expression analysis via in-situ hybridization. We found that both monocular and binocular V1 are highly enriched in aromatase- and ER-positive neurons, indicating that V1 is a site of production and sensitivity to estrogens. Using double-fluorescence in-situ hybridization, we reveal the neurochemical identity of estrogen-producing and -sensitive cells in V1, and demonstrate that they constitute a heterogeneous neuronal population. We further show that visual experience engages a large population of aromatase-positive neurons and, to a lesser extent, ER-expressing neurons, suggesting that E2 levels may be locally regulated by visual input in V1. Interestingly, acute episodes of visual experience do not affect the density or distribution of estrogen-associated circuits. Finally, we show that adult mice dark-reared from birth also exhibit normal distribution of aromatase and ERs throughout V1, suggesting that the implementation and maintenance of estrogen-associated circuits is independent of visual experience. Our findings demonstrate that the adult V1 is a site of production and sensitivity to estrogens, and suggest that locally-produced E2 may shape visual cortical processing.

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Neurochemical identity and heterogeneity of estrogen-associated circuits in V1.A–F) Images depicting representative dFISH signal in V1 for vGlut2, a marker for excitatory neurons (A) or GAD65, a marker for inhibitory neurons (D), and ARO (B, E) mRNAs. Note that ARO-positive neurons strongly co-localize with vGlut2 (C), but not GAD65 (F), indicating that estrogen-producing cells in V1 are largely excitatory neurons. G–L) Photomicrographs illustrating dFISH labeling for vGlut2 (G) or GAD65 (J), and ERα (H, K). Notably, whereas few ERα-positive neurons are excitatory (I), the vast majority of these cells co-express GAD65 (L), indicating a GABAergic phenotype. M–R) Images depicting dFISH signal for vGlut2 (M) or GAD65 (P), and ERβ (N, Q) in V1. The merged images (O, R) demonstrate that most ERβ-positive cells are excitatory, but not inhibitory, as revealed by co-localization of vGlut2 (O) and GAD65 (R), respectively. For all merged panels (right-most images in the figure plate), representative double-labeled neurons are highlighted by asterisks. Neurons that are exclusively labeled for either neurochemical cell marker, or markers for estrogen-associated circuits, are depicted by arrows and arrowheads, respectively. Scale bar = 25 µm.
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pone-0020400-g004: Neurochemical identity and heterogeneity of estrogen-associated circuits in V1.A–F) Images depicting representative dFISH signal in V1 for vGlut2, a marker for excitatory neurons (A) or GAD65, a marker for inhibitory neurons (D), and ARO (B, E) mRNAs. Note that ARO-positive neurons strongly co-localize with vGlut2 (C), but not GAD65 (F), indicating that estrogen-producing cells in V1 are largely excitatory neurons. G–L) Photomicrographs illustrating dFISH labeling for vGlut2 (G) or GAD65 (J), and ERα (H, K). Notably, whereas few ERα-positive neurons are excitatory (I), the vast majority of these cells co-express GAD65 (L), indicating a GABAergic phenotype. M–R) Images depicting dFISH signal for vGlut2 (M) or GAD65 (P), and ERβ (N, Q) in V1. The merged images (O, R) demonstrate that most ERβ-positive cells are excitatory, but not inhibitory, as revealed by co-localization of vGlut2 (O) and GAD65 (R), respectively. For all merged panels (right-most images in the figure plate), representative double-labeled neurons are highlighted by asterisks. Neurons that are exclusively labeled for either neurochemical cell marker, or markers for estrogen-associated circuits, are depicted by arrows and arrowheads, respectively. Scale bar = 25 µm.

Mentions: We next set out to determine the neurochemical identity of estrogen-producing and estrogen-sensitive neurons in V1. To this end, we carried out double-FISH experiments combining riboprobes directed at estrogen-associated networks (ARO, ERα or ERβ) and classic markers for excitatory or inhibitory neurons – the vesicular glutamate transporter 2 (vGlut2) and the 65 kDa glutamic acid decarboxylase (GAD65), respectively (Fig. 4).


The mouse primary visual cortex is a site of production and sensitivity to estrogens.

Jeong JK, Tremere LA, Burrows K, Majewska AK, Pinaud R - PLoS ONE (2011)

Neurochemical identity and heterogeneity of estrogen-associated circuits in V1.A–F) Images depicting representative dFISH signal in V1 for vGlut2, a marker for excitatory neurons (A) or GAD65, a marker for inhibitory neurons (D), and ARO (B, E) mRNAs. Note that ARO-positive neurons strongly co-localize with vGlut2 (C), but not GAD65 (F), indicating that estrogen-producing cells in V1 are largely excitatory neurons. G–L) Photomicrographs illustrating dFISH labeling for vGlut2 (G) or GAD65 (J), and ERα (H, K). Notably, whereas few ERα-positive neurons are excitatory (I), the vast majority of these cells co-express GAD65 (L), indicating a GABAergic phenotype. M–R) Images depicting dFISH signal for vGlut2 (M) or GAD65 (P), and ERβ (N, Q) in V1. The merged images (O, R) demonstrate that most ERβ-positive cells are excitatory, but not inhibitory, as revealed by co-localization of vGlut2 (O) and GAD65 (R), respectively. For all merged panels (right-most images in the figure plate), representative double-labeled neurons are highlighted by asterisks. Neurons that are exclusively labeled for either neurochemical cell marker, or markers for estrogen-associated circuits, are depicted by arrows and arrowheads, respectively. Scale bar = 25 µm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3101258&req=5

pone-0020400-g004: Neurochemical identity and heterogeneity of estrogen-associated circuits in V1.A–F) Images depicting representative dFISH signal in V1 for vGlut2, a marker for excitatory neurons (A) or GAD65, a marker for inhibitory neurons (D), and ARO (B, E) mRNAs. Note that ARO-positive neurons strongly co-localize with vGlut2 (C), but not GAD65 (F), indicating that estrogen-producing cells in V1 are largely excitatory neurons. G–L) Photomicrographs illustrating dFISH labeling for vGlut2 (G) or GAD65 (J), and ERα (H, K). Notably, whereas few ERα-positive neurons are excitatory (I), the vast majority of these cells co-express GAD65 (L), indicating a GABAergic phenotype. M–R) Images depicting dFISH signal for vGlut2 (M) or GAD65 (P), and ERβ (N, Q) in V1. The merged images (O, R) demonstrate that most ERβ-positive cells are excitatory, but not inhibitory, as revealed by co-localization of vGlut2 (O) and GAD65 (R), respectively. For all merged panels (right-most images in the figure plate), representative double-labeled neurons are highlighted by asterisks. Neurons that are exclusively labeled for either neurochemical cell marker, or markers for estrogen-associated circuits, are depicted by arrows and arrowheads, respectively. Scale bar = 25 µm.
Mentions: We next set out to determine the neurochemical identity of estrogen-producing and estrogen-sensitive neurons in V1. To this end, we carried out double-FISH experiments combining riboprobes directed at estrogen-associated networks (ARO, ERα or ERβ) and classic markers for excitatory or inhibitory neurons – the vesicular glutamate transporter 2 (vGlut2) and the 65 kDa glutamic acid decarboxylase (GAD65), respectively (Fig. 4).

Bottom Line: We found that both monocular and binocular V1 are highly enriched in aromatase- and ER-positive neurons, indicating that V1 is a site of production and sensitivity to estrogens.Interestingly, acute episodes of visual experience do not affect the density or distribution of estrogen-associated circuits.Finally, we show that adult mice dark-reared from birth also exhibit normal distribution of aromatase and ERs throughout V1, suggesting that the implementation and maintenance of estrogen-associated circuits is independent of visual experience.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma, United States of America.

ABSTRACT
The classic female estrogen, 17β-estradiol (E2), has been repeatedly shown to affect the perceptual processing of visual cues. Although gonadal E2 has often been thought to influence these processes, the possibility that central visual processing may be modulated by brain-generated hormone has not been explored. Here we show that estrogen-associated circuits are highly prevalent in the mouse primary visual cortex (V1). Specifically, we cloned aromatase, a marker for estrogen-producing neurons, and the classic estrogen receptors (ERs) ERα and ERβ, as markers for estrogen-responsive neurons, and conducted a detailed expression analysis via in-situ hybridization. We found that both monocular and binocular V1 are highly enriched in aromatase- and ER-positive neurons, indicating that V1 is a site of production and sensitivity to estrogens. Using double-fluorescence in-situ hybridization, we reveal the neurochemical identity of estrogen-producing and -sensitive cells in V1, and demonstrate that they constitute a heterogeneous neuronal population. We further show that visual experience engages a large population of aromatase-positive neurons and, to a lesser extent, ER-expressing neurons, suggesting that E2 levels may be locally regulated by visual input in V1. Interestingly, acute episodes of visual experience do not affect the density or distribution of estrogen-associated circuits. Finally, we show that adult mice dark-reared from birth also exhibit normal distribution of aromatase and ERs throughout V1, suggesting that the implementation and maintenance of estrogen-associated circuits is independent of visual experience. Our findings demonstrate that the adult V1 is a site of production and sensitivity to estrogens, and suggest that locally-produced E2 may shape visual cortical processing.

Show MeSH