Cervicothalamic tract terminals are enriched in glutamate-like immunoreactivity: an electron microscopic double-labeling study in the cat

Broman, Jonas; Ottersen, O. P.

doi:10.1523/jneurosci.12-01-00204.1992

Cited by 57 publications

(23 citation statements)

References 55 publications

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“…Thus, striatal profiles containing the most intense glutamate labeling were axon terminals forming asymmetric synapses, typical of cortical and thalamic input (Kemp and Powell, 1971). In agreement with previous studies in the hippocampus and the cerebellum, many gold particles in boutons were associated with synaptic vesicles (Somogyi et al, 1986;Broman and Ottersen, 1992;. Consistent with the fact that glutamate also exists in nontransmitter pools, for example, as a participant in intermediary metabolism (Fonnum, 1984), glutamate labeling was also observed in several other subcellular compartments.…”

Section: Discussionsupporting

confidence: 91%

3-Hydroxyanthranilic acid oxygenase-containing astrocytic processes surround glutamate-containing axon terminals in the rat striatum

Roberts

McCarthy

et al. 1995

J. Neurosci.

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Glutamate, the major transmitter of the corticostriatal pathway, is present in abundance in the striatum. 3-Hydroxyanthranilic acid oxygenase (3HAO) is the biosynthetic enzyme for quinolinic acid, an endogenous agonist of the NMDA glutamate receptor subtype and a potent neurotoxin. In order to explore the anatomical basis of possible functional interactions between glutamate and quinolinic acid in the rat striatum, pre- and postembedding immunocytochemical methods were used to localize 3HAO immunoreactivity (-i) and glutamate-i at the electron microscopic level. In accordance with previous light microscopic and biochemical studies, 3HAO-i was detected exclusively in astrocytes throughout the striatum. Notably, 3HAO-i was present in fine- caliber glial processes that often surrounded or abutted synaptic profiles, both asymmetric and symmetric. Glutamate-i was heavily deposited (3–13-fold higher gold particle density than tissue average) in axon terminals forming asymmetric synapses with spines and, occasionally, dendrites. In contrast, terminals forming symmetric synapses, dendrites, neuronal somata, and glial cells contained significantly less labeling than terminals forming asymmetric synapses. In double-labeled material, 3HAO-i was observed in glial processes that partially surrounded or were adjacent to glutamate-labeled terminals forming asymmetric synapses. 3HAO-labeled glial processes were also adjacent to unlabeled terminals forming symmetric synapses. Since quinolinic acid is known to enter the extracellular compartment readily, these results suggest that astrocytic quinolinic acid may participate in the regulation of glutamatergic neurotransmission in the rat striatum.

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Section: Discussionsupporting

confidence: 91%

3-Hydroxyanthranilic acid oxygenase-containing astrocytic processes surround glutamate-containing axon terminals in the rat striatum

Roberts

McCarthy

et al. 1995

J. Neurosci.

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“…These results indicate that the LPBd contains neurons that transmit cutaneous warm signals directly to the POA. The idea that this activation of warm-responsive LPBd neurons is caused by a glutamatergic input from second-order somatosensory neurons in the spinal dorsal horn is supported by previous anatomical evidence: (i) There are numerous projections from the dorsal horn to the LPB (21), some of which terminate on POAprojecting LPB neurons (8); and (ii) a substantial population of dorsal horn neurons provide their axon collaterals both to the LPB and thalamus (22), and their terminals in the thalamus contain glutamate (23).…”

Section: Discussionmentioning

confidence: 55%

A thermosensory pathway mediating heat-defense responses

Nakamura

Morrison

2010

Proc. Natl. Acad. Sci. U.S.A.

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Afferent neural transmission of temperature sensation from skin thermoreceptors to the central thermoregulatory system is important for the defense of body temperature against environmental thermal challenges. Here, we report a thermosensory pathway that triggers physiological heat-defense responses to elevated environmental temperature. Using in vivo electrophysiological and anatomical approaches in the rat, we found that neurons in the dorsal part of the lateral parabrachial nucleus (LPBd) glutamatergically transmit cutaneous warm signals from spinal somatosensory neurons directly to the thermoregulatory command center, the preoptic area (POA). Intriguingly, these LPBd neurons are located adjacent to another group of neurons that mediate cutaneous cool signaling to the POA. Functional experiments revealed that this LPBd–POA warm sensory pathway is required to elicit autonomic heat-defense responses, such as cutaneous vasodilation, to skin-warming challenges. These findings provide a fundamental framework for understanding the neural circuitry maintaining thermal homeostasis, which is critical to survive severe environmental temperatures.

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“…However, there is considerable evidence that glutamate is highly concentrated in axonal boutons from which it is released as a transmitter, and that the presence of high levels of glutamate-11 in axon terminals provides one of the most reliable ways of identifying glutamatergic neurons (Somogyi et al, 1986;Montero and Wenthold, 1989;Maxwell et al, 1990;Broman and Ottersen, 1992). By identifying the axons of particular neurons and estimating the level of glutamate-L1 in them, it should therefore be possible to determine whether or not the cells use glutamate as a transmitter.…”

Section: Discussionmentioning

confidence: 99%

“…In the cerebellum it has been shown that the level of glutamate-11 is significantly higher in mossy and parallel fiber terminals (which are thought to release glutamate) than in other cellular compartments, including granule cell bodies that give rise to parallel fibers (Somogyi et al, 1986). Elsewhere in the CNS enrichment of glutamate-L1 has been demonstrated in axon terminals that are thought to be glutamatergic (e.g., Montero and Wenthold, 1989;Maxwell et al, 1990;Broman and Ottersen, 1992). This suggests that within axon terminals it is possible to identify the "transmitter pool" of glutamate.…”

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confidence: 99%

Immunocytochemical evidence that neurotensin is present in glutamatergic neurons in the superficial dorsal horn of the rat

et al. 1994

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In order to determine whether glutamate is enriched in neurotensin- containing axons in the superficial dorsal horn of the rat spinal cord, we have carried out preembedding immunocytochemistry with an antiserum to neurotensin and then used a postembedding immunogold method with antiserum to glutamate. The immunogold label (corresponding to glutamate-like immunoreactivity) over 40 neurotensin-immunoreactive boutons in laminae I and II of the lumbar dorsal horn was compared with that over nearby axons that formed asymmetrical or symmetrical synapses. In addition, for 20 of these boutons, the labeling was compared with that over mossy and parallel fiber terminals (both of which are thought to use glutamate as a transmitter) from sections of cerebellum that had been processed together with those of spinal cord. Glutamate-like immunoreactivity was consistently high over neurotensin- immunoreactive boutons relative to most surrounding profiles. Immunostaining over these boutons was slightly (11%) lower than that over matched terminals that formed asymmetrical synapses, but considerably higher than that over the terminals that formed symmetrical synapses. The level of glutamate immunoreactivity in neurotensin-immunoreactive boutons in dorsal horn was similar to that in cerebellar parallel fiber terminals, but significantly lower than that in mossy fiber terminals. These results suggest that glutamate is a transmitter used by neurotensin-immunoreactive axons in the dorsal horn, and since these axons are thought to be largely or entirely derived from neurotensin-containing neurons in laminae I-III, they provide immunocytochemical evidence for a population of excitatory glutamatergic neurons in this region.

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Cervicothalamic tract terminals are enriched in glutamate-like immunoreactivity: an electron microscopic double-labeling study in the cat

Cited by 57 publications

References 55 publications

3-Hydroxyanthranilic acid oxygenase-containing astrocytic processes surround glutamate-containing axon terminals in the rat striatum

3-Hydroxyanthranilic acid oxygenase-containing astrocytic processes surround glutamate-containing axon terminals in the rat striatum

A thermosensory pathway mediating heat-defense responses

Immunocytochemical evidence that neurotensin is present in glutamatergic neurons in the superficial dorsal horn of the rat

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