Neuropeptide Y-containing neurons in the rat striatum: ultrastructure and cellular relations with tyrosine hydroxylase-containing terminals and with astrocytes

Chiye Aoki, Virginia M. Pickel

Research output: Contribution to journalArticle

Abstract

The ultrastructural localization of neuropeptide Y (NPY) was comparatively examined in the dorsal (caudate-putamen) and ventral (nucleus accumbens) striatum using the peroxidase-antiperoxidase (PAP) method. In both striatal regions, NPY-like immunoreactivity (IR) was detected in perikarya, dendrites and axons. The labeled perikarya were 15-25 μm in diameter and contained large, deeply and multiply indented nuclei and prominent Nissl bodies. The labeled dendrites contained a few large (80-150 nm) dense-core vesicles, lacked detectable spines and received few afferents. These morphological characteristics of NPY-IR neurons in both areas are in close accord with previous descriptions for the medium aspiny intrinsic neurons. Axon terminals with NPY-like IR contained primarily small clear round vesicles, as seen in single or serial sections. These terminals formed junctions that lacked recognizable pre- or post-synaptic densities, but showed parallel spacing between apposed plasmalemmas at presumed synaptic clefts. Targets of the axon terminals with NPY-like IR included unlabeled somata, unlabeled proximal dendrites and labeled and unlabeled distal dendrites. The NPY-IR neurons in the caudate-putamen differed from those in the nucleus accumbens in that (1) there were no recognized appositions between labeled dendrites and labeled terminals, and (2) fewer terminals contained large dense-core vesicles. These findings are consistent with the concept that in the nucleus accumbens, the excitability of the NPY-IR neurons may be more directly modulated by NPY or another transmitter co-existing in the terminals. Catecholamines are known to co-exist with NPY in certain rostrally projecting brainstem nuclei. Therefore, in the two striatal regions, we additionally sought to determine (1) whether the NPY-IR neurons might be modulated by catecholaminergic afferents and (2) whether NPY might co-exist with catecholamines in terminals. Goat antiserum against NPY and rabbit antiserum against tyrosine hydroxylase (TH), the catecholamine-synthesizing enzyme, were simultaneously localized in single sections by PAP and immunoautoradiographic methods, respectively. Quantitative analysis in dually labeled sections from both striatal areas revealed few, if any, direct synaptic contacts between TH-labeled terminals and dendrites containing NPY-like IR. However, there was convergence of separate NPY- and TH-IR terminals on unlabeled dendrites. A few terminals in the nucleus accumbens, but not in the dorsal striatum, showed immunoreactivity to TH and also contained dense-core vesicles with NPY-like IR. These results indicate (1) that NPY and catecholamines released from separate axon terminals may jointly influence the excitability principally of non-NPY-containing neurons within the dorsal and ventral striatum, and (2) that co-storage of NPY and catecholamines is limited to a few terminals in the nucleus accumbens. Finally, in both single and dual labeling studies, astrocytic processes were found in close association with NPY-IR dendrites. We discuss the possibility that these glia may participate in protecting NPY-containing neurons from neurodegeneration, as is observed in brains from patients with Huntington's chorea.

Original languageEnglish (US)
Pages (from-to)205-225
Number of pages21
JournalBrain Research
Volume459
Issue number2
DOIs
StatePublished - Sep 6 1988

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Neuropeptide Y
Tyrosine 3-Monooxygenase
Astrocytes
Neurons
Dendrites
Nucleus Accumbens
Catecholamines
Corpus Striatum
Presynaptic Terminals
Secretory Vesicles
Putamen
Peroxidase
Immune Sera
Nissl Bodies
Post-Synaptic Density

Keywords

  • Catecholamine
  • Caudate-putamen
  • Dopamine
  • Glia
  • Immunocytochemistry
  • Norepinephrine
  • Nucleus accumbens
  • Synapse

ASJC Scopus subject areas

  • Developmental Biology
  • Molecular Biology
  • Clinical Neurology
  • Neuroscience(all)

Cite this

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title = "Neuropeptide Y-containing neurons in the rat striatum: ultrastructure and cellular relations with tyrosine hydroxylase-containing terminals and with astrocytes",
abstract = "The ultrastructural localization of neuropeptide Y (NPY) was comparatively examined in the dorsal (caudate-putamen) and ventral (nucleus accumbens) striatum using the peroxidase-antiperoxidase (PAP) method. In both striatal regions, NPY-like immunoreactivity (IR) was detected in perikarya, dendrites and axons. The labeled perikarya were 15-25 μm in diameter and contained large, deeply and multiply indented nuclei and prominent Nissl bodies. The labeled dendrites contained a few large (80-150 nm) dense-core vesicles, lacked detectable spines and received few afferents. These morphological characteristics of NPY-IR neurons in both areas are in close accord with previous descriptions for the medium aspiny intrinsic neurons. Axon terminals with NPY-like IR contained primarily small clear round vesicles, as seen in single or serial sections. These terminals formed junctions that lacked recognizable pre- or post-synaptic densities, but showed parallel spacing between apposed plasmalemmas at presumed synaptic clefts. Targets of the axon terminals with NPY-like IR included unlabeled somata, unlabeled proximal dendrites and labeled and unlabeled distal dendrites. The NPY-IR neurons in the caudate-putamen differed from those in the nucleus accumbens in that (1) there were no recognized appositions between labeled dendrites and labeled terminals, and (2) fewer terminals contained large dense-core vesicles. These findings are consistent with the concept that in the nucleus accumbens, the excitability of the NPY-IR neurons may be more directly modulated by NPY or another transmitter co-existing in the terminals. Catecholamines are known to co-exist with NPY in certain rostrally projecting brainstem nuclei. Therefore, in the two striatal regions, we additionally sought to determine (1) whether the NPY-IR neurons might be modulated by catecholaminergic afferents and (2) whether NPY might co-exist with catecholamines in terminals. Goat antiserum against NPY and rabbit antiserum against tyrosine hydroxylase (TH), the catecholamine-synthesizing enzyme, were simultaneously localized in single sections by PAP and immunoautoradiographic methods, respectively. Quantitative analysis in dually labeled sections from both striatal areas revealed few, if any, direct synaptic contacts between TH-labeled terminals and dendrites containing NPY-like IR. However, there was convergence of separate NPY- and TH-IR terminals on unlabeled dendrites. A few terminals in the nucleus accumbens, but not in the dorsal striatum, showed immunoreactivity to TH and also contained dense-core vesicles with NPY-like IR. These results indicate (1) that NPY and catecholamines released from separate axon terminals may jointly influence the excitability principally of non-NPY-containing neurons within the dorsal and ventral striatum, and (2) that co-storage of NPY and catecholamines is limited to a few terminals in the nucleus accumbens. Finally, in both single and dual labeling studies, astrocytic processes were found in close association with NPY-IR dendrites. We discuss the possibility that these glia may participate in protecting NPY-containing neurons from neurodegeneration, as is observed in brains from patients with Huntington's chorea.",
keywords = "Catecholamine, Caudate-putamen, Dopamine, Glia, Immunocytochemistry, Norepinephrine, Nucleus accumbens, Synapse",
author = "Chiye Aoki and Pickel, {Virginia M.}",
year = "1988",
month = "9",
day = "6",
doi = "10.1016/0006-8993(88)90637-3",
language = "English (US)",
volume = "459",
pages = "205--225",
journal = "Brain Research",
issn = "0006-8993",
publisher = "Elsevier",
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TY - JOUR

T1 - Neuropeptide Y-containing neurons in the rat striatum

T2 - ultrastructure and cellular relations with tyrosine hydroxylase-containing terminals and with astrocytes

AU - Aoki, Chiye

AU - Pickel, Virginia M.

PY - 1988/9/6

Y1 - 1988/9/6

N2 - The ultrastructural localization of neuropeptide Y (NPY) was comparatively examined in the dorsal (caudate-putamen) and ventral (nucleus accumbens) striatum using the peroxidase-antiperoxidase (PAP) method. In both striatal regions, NPY-like immunoreactivity (IR) was detected in perikarya, dendrites and axons. The labeled perikarya were 15-25 μm in diameter and contained large, deeply and multiply indented nuclei and prominent Nissl bodies. The labeled dendrites contained a few large (80-150 nm) dense-core vesicles, lacked detectable spines and received few afferents. These morphological characteristics of NPY-IR neurons in both areas are in close accord with previous descriptions for the medium aspiny intrinsic neurons. Axon terminals with NPY-like IR contained primarily small clear round vesicles, as seen in single or serial sections. These terminals formed junctions that lacked recognizable pre- or post-synaptic densities, but showed parallel spacing between apposed plasmalemmas at presumed synaptic clefts. Targets of the axon terminals with NPY-like IR included unlabeled somata, unlabeled proximal dendrites and labeled and unlabeled distal dendrites. The NPY-IR neurons in the caudate-putamen differed from those in the nucleus accumbens in that (1) there were no recognized appositions between labeled dendrites and labeled terminals, and (2) fewer terminals contained large dense-core vesicles. These findings are consistent with the concept that in the nucleus accumbens, the excitability of the NPY-IR neurons may be more directly modulated by NPY or another transmitter co-existing in the terminals. Catecholamines are known to co-exist with NPY in certain rostrally projecting brainstem nuclei. Therefore, in the two striatal regions, we additionally sought to determine (1) whether the NPY-IR neurons might be modulated by catecholaminergic afferents and (2) whether NPY might co-exist with catecholamines in terminals. Goat antiserum against NPY and rabbit antiserum against tyrosine hydroxylase (TH), the catecholamine-synthesizing enzyme, were simultaneously localized in single sections by PAP and immunoautoradiographic methods, respectively. Quantitative analysis in dually labeled sections from both striatal areas revealed few, if any, direct synaptic contacts between TH-labeled terminals and dendrites containing NPY-like IR. However, there was convergence of separate NPY- and TH-IR terminals on unlabeled dendrites. A few terminals in the nucleus accumbens, but not in the dorsal striatum, showed immunoreactivity to TH and also contained dense-core vesicles with NPY-like IR. These results indicate (1) that NPY and catecholamines released from separate axon terminals may jointly influence the excitability principally of non-NPY-containing neurons within the dorsal and ventral striatum, and (2) that co-storage of NPY and catecholamines is limited to a few terminals in the nucleus accumbens. Finally, in both single and dual labeling studies, astrocytic processes were found in close association with NPY-IR dendrites. We discuss the possibility that these glia may participate in protecting NPY-containing neurons from neurodegeneration, as is observed in brains from patients with Huntington's chorea.

AB - The ultrastructural localization of neuropeptide Y (NPY) was comparatively examined in the dorsal (caudate-putamen) and ventral (nucleus accumbens) striatum using the peroxidase-antiperoxidase (PAP) method. In both striatal regions, NPY-like immunoreactivity (IR) was detected in perikarya, dendrites and axons. The labeled perikarya were 15-25 μm in diameter and contained large, deeply and multiply indented nuclei and prominent Nissl bodies. The labeled dendrites contained a few large (80-150 nm) dense-core vesicles, lacked detectable spines and received few afferents. These morphological characteristics of NPY-IR neurons in both areas are in close accord with previous descriptions for the medium aspiny intrinsic neurons. Axon terminals with NPY-like IR contained primarily small clear round vesicles, as seen in single or serial sections. These terminals formed junctions that lacked recognizable pre- or post-synaptic densities, but showed parallel spacing between apposed plasmalemmas at presumed synaptic clefts. Targets of the axon terminals with NPY-like IR included unlabeled somata, unlabeled proximal dendrites and labeled and unlabeled distal dendrites. The NPY-IR neurons in the caudate-putamen differed from those in the nucleus accumbens in that (1) there were no recognized appositions between labeled dendrites and labeled terminals, and (2) fewer terminals contained large dense-core vesicles. These findings are consistent with the concept that in the nucleus accumbens, the excitability of the NPY-IR neurons may be more directly modulated by NPY or another transmitter co-existing in the terminals. Catecholamines are known to co-exist with NPY in certain rostrally projecting brainstem nuclei. Therefore, in the two striatal regions, we additionally sought to determine (1) whether the NPY-IR neurons might be modulated by catecholaminergic afferents and (2) whether NPY might co-exist with catecholamines in terminals. Goat antiserum against NPY and rabbit antiserum against tyrosine hydroxylase (TH), the catecholamine-synthesizing enzyme, were simultaneously localized in single sections by PAP and immunoautoradiographic methods, respectively. Quantitative analysis in dually labeled sections from both striatal areas revealed few, if any, direct synaptic contacts between TH-labeled terminals and dendrites containing NPY-like IR. However, there was convergence of separate NPY- and TH-IR terminals on unlabeled dendrites. A few terminals in the nucleus accumbens, but not in the dorsal striatum, showed immunoreactivity to TH and also contained dense-core vesicles with NPY-like IR. These results indicate (1) that NPY and catecholamines released from separate axon terminals may jointly influence the excitability principally of non-NPY-containing neurons within the dorsal and ventral striatum, and (2) that co-storage of NPY and catecholamines is limited to a few terminals in the nucleus accumbens. Finally, in both single and dual labeling studies, astrocytic processes were found in close association with NPY-IR dendrites. We discuss the possibility that these glia may participate in protecting NPY-containing neurons from neurodegeneration, as is observed in brains from patients with Huntington's chorea.

KW - Catecholamine

KW - Caudate-putamen

KW - Dopamine

KW - Glia

KW - Immunocytochemistry

KW - Norepinephrine

KW - Nucleus accumbens

KW - Synapse

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