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"Latent" inhibitory connections become functional during activity-dependent plasticity
S Charpier1, J C Behrends, A Triller
1Laboratoire de Neurobiologie Cellulaire, Institut National de la Santé et de la Recherche Médicale U261, Institut Pasteur, Paris, France.
Insights
Silent inhibitory synapses can be unmasked by tetanic stimulation, revealing a reserve pool of connections. This finding supports long-term potentiation in inhibitory synapses and influences reflex activity thresholds.
Area of Science:
- Neuroscience
- Synaptic Plasticity
Background:
- Glycinergic inhibitory interneurons play a crucial role in modulating neuronal network activity.
- The Mauthner cell, a key component in escape behaviors, receives significant inhibitory input.
Purpose of the Study:
- To investigate the functional state of glycinergic inhibitory synapses on the Mauthner cell.
- To explore the plasticity and potential reserve capacity of these inhibitory connections.
Main Methods:
- Simultaneous pre- and postsynaptic recordings from identified interneurons and the Mauthner cell.
- Morphological analysis of synaptic contacts.
- Pharmacological manipulation (4-aminopyridine, Ca2+) and tetanic stimulation of afferents.
Main Results:
- 25% of afferent connections showed minimal or no postsynaptic response, suggesting silent synapses.
- Pharmacological agents enhanced functional synapses but not silent ones.
- Tetanic stimulation unmasked or potentiated silent synapses, demonstrating long-term potentiation (LTP) of inhibitory connections.
Conclusions:
- Weakly functional inhibitory synapses act as a reserve pool, crucial for network plasticity.
- These reserve synapses can significantly influence reflex activity thresholds, such as escape responses.
Abstract:
Simultaneous pre- and postsynaptic recordings from identified glycinergic inhibitory interneurons and the Mauthner cell showed that 25% of the afferents produced no or extremely small postsynaptic responses. Morphological determination of the number of contacts made by these cells on the Mauthner cell revealed a connectivity similar to that of functional neurons which always produce clear inhibitory postsynaptic potentials, suggesting that most of the endings, made by weak interneurons are silent. Intraaxonal injection of 4-aminopyridine or Ca2+ greatly enhanced transmission at functional connections but did not modify those which were ineffective. However, after eighth nerve tetanic stimuli, transmission at the weak connections was unmasked or enhanced for prolonged periods and was twice as likely to be potentiated, with a 6-fold greater mean enhancement than the potent ones. This result provides additional support for long-term potentiation of inhibitory synapses. Furthermore, weakly functional junctions represent a "reserve" pool which can be critical for the expression of plasticity within a network, and, consequently, for setting the threshold of reflex activities such as the escape reaction mediated by the Mauthner cell.