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Cortical nNOS neurons co-express the NK1 receptor and are depolarized by Substance P in multiple mammalian species.

Dittrich L, Heiss JE, Warrier DR, Perez XA, Quik M, Kilduff TS - Front Neural Circuits (2012)

Bottom Line: These neurons are known to be GABAergic, to express Neuropeptide Y (NPY) and, in rats, to co-express the Substance P (SP) receptor NK1, suggesting a possible role for SP in sleep/wake regulation.Type I nNOS neurons co-expressed NK1 in all three species although the anatomical distribution within the cortex was species-specific.These results suggest a conserved role for SP in the regulation of cortical sleep-active neurons in mammals.

View Article: PubMed Central - PubMed

Affiliation: Biosciences Division, Center for Neuroscience, SRI International, Menlo Park CA, USA.

ABSTRACT
We have previously demonstrated that Type I neuronal nitric oxide synthase (nNOS)-expressing neurons are sleep-active in the cortex of mice, rats, and hamsters. These neurons are known to be GABAergic, to express Neuropeptide Y (NPY) and, in rats, to co-express the Substance P (SP) receptor NK1, suggesting a possible role for SP in sleep/wake regulation. To evaluate the degree of co-expression of nNOS and NK1 in the cortex among mammals, we used double immunofluorescence for nNOS and NK1 and determined the anatomical distribution in mouse, rat, and squirrel monkey cortex. Type I nNOS neurons co-expressed NK1 in all three species although the anatomical distribution within the cortex was species-specific. We then performed in vitro patch clamp recordings in cortical neurons in mouse and rat slices using the SP conjugate tetramethylrhodamine-SP (TMR-SP) to identify NK1-expressing cells and evaluated the effects of SP on these neurons. Bath application of SP (0.03-1 μM) resulted in a sustained increase in firing rate of these neurons; depolarization persisted in the presence of tetrodotoxin. These results suggest a conserved role for SP in the regulation of cortical sleep-active neurons in mammals.

No MeSH data available.


Related in: MedlinePlus

Distribution of nNOS and NK1 cells in the neocortex of three mammalian species. In mice (A,A'), virtually all cells were double-labeled for nNOS and NK1 (orange) and were most abundant in deep gray matter. Neurons single-labeled for nNOS (red) or NK1 (green) were virtually absent. In rats (B,B'), double-labeled neurons were scattered throughout the cortex and underlying white matter; single-labeled nNOS neurons were virtually absent. Neurons single-labeled for NK1 were concentrated in superficial layers. In monkeys (C,C'), double-labeled neurons were most abundant in the deep gray matter and the underlying white matter and single-labeled nNOS neurons were rare. Neurons single-labeled for NK1 were concentrated in deep gray matter. Labeled neurons were more abundant in gyri than in sulci. A, B, and C are anterior sections, A', B', and C' are posterior sections. Scale bars denote 2 mm.
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Figure 1: Distribution of nNOS and NK1 cells in the neocortex of three mammalian species. In mice (A,A'), virtually all cells were double-labeled for nNOS and NK1 (orange) and were most abundant in deep gray matter. Neurons single-labeled for nNOS (red) or NK1 (green) were virtually absent. In rats (B,B'), double-labeled neurons were scattered throughout the cortex and underlying white matter; single-labeled nNOS neurons were virtually absent. Neurons single-labeled for NK1 were concentrated in superficial layers. In monkeys (C,C'), double-labeled neurons were most abundant in the deep gray matter and the underlying white matter and single-labeled nNOS neurons were rare. Neurons single-labeled for NK1 were concentrated in deep gray matter. Labeled neurons were more abundant in gyri than in sulci. A, B, and C are anterior sections, A', B', and C' are posterior sections. Scale bars denote 2 mm.

Mentions: The distribution of labeled neurons also differed between species. In mice, nNOS neurons were located mainly in the deep gray matter (Figures 1A,A'). In rats, nNOS neurons were scattered throughout all cortical layers (Figures 1B,B'). In monkeys, nNOS neurons were concentrated on both sides of the white matter-gray matter border (Figures 1C,C'). Single-labeled NK1 neurons were concentrated in the superficial gray matter in rats (Figures 1B,B') and deep gray matter in monkeys (Figures 1C,C'). In monkeys, both cell types were more abundant in gyri than in sulci (Figure 1C').


Cortical nNOS neurons co-express the NK1 receptor and are depolarized by Substance P in multiple mammalian species.

Dittrich L, Heiss JE, Warrier DR, Perez XA, Quik M, Kilduff TS - Front Neural Circuits (2012)

Distribution of nNOS and NK1 cells in the neocortex of three mammalian species. In mice (A,A'), virtually all cells were double-labeled for nNOS and NK1 (orange) and were most abundant in deep gray matter. Neurons single-labeled for nNOS (red) or NK1 (green) were virtually absent. In rats (B,B'), double-labeled neurons were scattered throughout the cortex and underlying white matter; single-labeled nNOS neurons were virtually absent. Neurons single-labeled for NK1 were concentrated in superficial layers. In monkeys (C,C'), double-labeled neurons were most abundant in the deep gray matter and the underlying white matter and single-labeled nNOS neurons were rare. Neurons single-labeled for NK1 were concentrated in deep gray matter. Labeled neurons were more abundant in gyri than in sulci. A, B, and C are anterior sections, A', B', and C' are posterior sections. Scale bars denote 2 mm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3367498&req=5

Figure 1: Distribution of nNOS and NK1 cells in the neocortex of three mammalian species. In mice (A,A'), virtually all cells were double-labeled for nNOS and NK1 (orange) and were most abundant in deep gray matter. Neurons single-labeled for nNOS (red) or NK1 (green) were virtually absent. In rats (B,B'), double-labeled neurons were scattered throughout the cortex and underlying white matter; single-labeled nNOS neurons were virtually absent. Neurons single-labeled for NK1 were concentrated in superficial layers. In monkeys (C,C'), double-labeled neurons were most abundant in the deep gray matter and the underlying white matter and single-labeled nNOS neurons were rare. Neurons single-labeled for NK1 were concentrated in deep gray matter. Labeled neurons were more abundant in gyri than in sulci. A, B, and C are anterior sections, A', B', and C' are posterior sections. Scale bars denote 2 mm.
Mentions: The distribution of labeled neurons also differed between species. In mice, nNOS neurons were located mainly in the deep gray matter (Figures 1A,A'). In rats, nNOS neurons were scattered throughout all cortical layers (Figures 1B,B'). In monkeys, nNOS neurons were concentrated on both sides of the white matter-gray matter border (Figures 1C,C'). Single-labeled NK1 neurons were concentrated in the superficial gray matter in rats (Figures 1B,B') and deep gray matter in monkeys (Figures 1C,C'). In monkeys, both cell types were more abundant in gyri than in sulci (Figure 1C').

Bottom Line: These neurons are known to be GABAergic, to express Neuropeptide Y (NPY) and, in rats, to co-express the Substance P (SP) receptor NK1, suggesting a possible role for SP in sleep/wake regulation.Type I nNOS neurons co-expressed NK1 in all three species although the anatomical distribution within the cortex was species-specific.These results suggest a conserved role for SP in the regulation of cortical sleep-active neurons in mammals.

View Article: PubMed Central - PubMed

Affiliation: Biosciences Division, Center for Neuroscience, SRI International, Menlo Park CA, USA.

ABSTRACT
We have previously demonstrated that Type I neuronal nitric oxide synthase (nNOS)-expressing neurons are sleep-active in the cortex of mice, rats, and hamsters. These neurons are known to be GABAergic, to express Neuropeptide Y (NPY) and, in rats, to co-express the Substance P (SP) receptor NK1, suggesting a possible role for SP in sleep/wake regulation. To evaluate the degree of co-expression of nNOS and NK1 in the cortex among mammals, we used double immunofluorescence for nNOS and NK1 and determined the anatomical distribution in mouse, rat, and squirrel monkey cortex. Type I nNOS neurons co-expressed NK1 in all three species although the anatomical distribution within the cortex was species-specific. We then performed in vitro patch clamp recordings in cortical neurons in mouse and rat slices using the SP conjugate tetramethylrhodamine-SP (TMR-SP) to identify NK1-expressing cells and evaluated the effects of SP on these neurons. Bath application of SP (0.03-1 μM) resulted in a sustained increase in firing rate of these neurons; depolarization persisted in the presence of tetrodotoxin. These results suggest a conserved role for SP in the regulation of cortical sleep-active neurons in mammals.

No MeSH data available.


Related in: MedlinePlus