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Role of glutamate delta -2 receptors in activity-dependent competition between heterologous afferent fibers.

ABSTRACT: A principle that regulates detailed architecture in the brain is that active terminals have a competitive advantage over less active terminals in establishing synaptic connections. This principle is known to apply to fibers within a single neuronal population competing for a common target domain. Here we uncover an additional rule that applies when two neuronal populations compete for two contiguous territories. The cerebellar Purkinje cell dendrites have two different synaptic domains with spines innervated by two separate excitatory inputs, parallel fibers (PFs) and climbing fibers (CFs). Glutamate delta-2 receptors are normally present only on the PF spines where they are important for their innervation. After block of activity by tetrodotoxin, numerous new spines form in the CF domain and become innervated mainly by PFs; all spines, including those still innervated by the CFs, bear delta-2 receptors. Thus, in the absence of activity, PFs gain a competitive advantage over CFs. The entire dendritic arbor becomes a uniform territory with the molecular cues associated with the PFs. To access their proper territory and maintain synaptic contacts, CFs must be active and locally repress the cues of the competitor afferents.

SUBMITTER: Morando L

PROVIDER: S-EPMC55559 | biostudies-literature | 2001 Aug

REPOSITORIES: biostudies-literature

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Role of glutamate delta -2 receptors in activity-dependent competition between heterologous afferent fibers.

Morando L L Cesa R R Rasetti R R Harvey R R Strata P P

Proceedings of the National Academy of Sciences of the United States of America 20010807 17

A principle that regulates detailed architecture in the brain is that active terminals have a competitive advantage over less active terminals in establishing synaptic connections. This principle is known to apply to fibers within a single neuronal population competing for a common target domain. Here we uncover an additional rule that applies when two neuronal populations compete for two contiguous territories. The cerebellar Purkinje cell dendrites have two different synaptic domains with spin ...[more]

PMID: 11493687

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Project description:Motoneurons receive thousands of excitatory and inhibitory synapses from descending tracts and primary afferent fibers. The excitability of these neurons must be precisely regulated to respond adequately to the requirements of the environment. In this context, GABAA and GABAB receptors regulate motoneuron synaptic strength. GABAA and GABAB receptors are expressed on primary afferent fibers and motoneurons, while in the descending afferent fibers, only the GABAB receptors are expressed. However, it remains to be known where the GABA that activates them comes from since the GABAergic interneurons that make axo-axonic contacts with primary afferents have yet to be identified in the descending afferent terminals. Thus, the main aim of the present report was to investigate how GABAB receptors functionally modulate synaptic strength between Ia afferent fibers, excitatory and inhibitory descending fibers of the dorsolateral funiculus, and spinal motoneurons. Using intracellular recordings from the spinal cord of the turtle, we provide evidence that the GABAB receptor antagonist, CGP55845, not only prevents baclofen-induced depression of EPSPs but also increases motoneuron excitability and enhances the synaptic strength between the afferent fibers and motoneurons. The last action of CGP55845 was similar in excitatory and inhibitory descending afferents. Interestingly, the action of baclofen was more intense in the Ia primary afferents than in the descending afferents. Even more, CGP55845 reversed the EPSP depression induced by the increased concentration of ambient GABA produced by interneuron activation and GABA transporter blockade. Immunofluorescence data corroborated the expression of GABAB receptors in the turtle’s spinal cord. These findings suggest that GABAB receptors are extrasynaptic and tonically activated on descending afferent fibers and motoneurons by GABA released from astrocytes and GABAergic interneurons in the cellular microenvironment. Finally, our results also suggest that the antispastic action of baclofen may be due to reduced synaptic strength between descending fibers and motoneurons.

Dataset Information

Role of glutamate delta -2 receptors in activity-dependent competition between heterologous afferent fibers.

Publications

Role of glutamate delta -2 receptors in activity-dependent competition between heterologous afferent fibers.

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