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Dynamic development of the first synapse impinging on adult-born neurons in the olfactory bulb circuit.

Katagiri H, Pallotto M, Nissant A, Murray K, Sassoè-Pognetto M, Lledo PM - Neural Syst Circuits (2011)

Bottom Line: We found that both the ratio of N-methyl-D-aspartate receptor (NMDAR) to α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR), and the number of functional release sites at proximal inputs reached a maximum during the critical period for the sensory-dependent survival of newborn cells, well before the completion of dendritic arborization.Interestingly, the latter morphological changes disappeared in more mature newly-formed neurons, when the NMDAR to AMPAR ratio had decreased and functional presynaptic terminals expressed only single release sites.Together, these findings show that the first glutamatergic inputs to adult-generated OB interneurons undergo a unique sequence of maturation stages.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratory for Perception and Memory, Institut Pasteur, Paris, France. pmlledo@pasteur.fr.

ABSTRACT
The olfactory bulb (OB) receives and integrates newborn interneurons throughout life. This process is important for the proper functioning of the OB circuit and consequently, for the sense of smell. Although we know how these new interneurons are produced, the way in which they integrate into the pre-existing ongoing circuits remains poorly documented. Bearing in mind that glutamatergic inputs onto local OB interneurons are crucial for adjusting the level of bulbar inhibition, it is important to characterize when and how these inputs from excitatory synapses develop on newborn OB interneurons. We studied early synaptic events that lead to the formation and maturation of the first glutamatergic synapses on adult-born granule cells (GCs), the most abundant subtype of OB interneuron. Patch-clamp recordings and electron microscopy (EM) analysis were performed on adult-born interneurons shortly after their arrival in the adult OB circuits. We found that both the ratio of N-methyl-D-aspartate receptor (NMDAR) to α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR), and the number of functional release sites at proximal inputs reached a maximum during the critical period for the sensory-dependent survival of newborn cells, well before the completion of dendritic arborization. EM analysis showed an accompanying change in postsynaptic density shape during the same period of time. Interestingly, the latter morphological changes disappeared in more mature newly-formed neurons, when the NMDAR to AMPAR ratio had decreased and functional presynaptic terminals expressed only single release sites. Together, these findings show that the first glutamatergic inputs to adult-generated OB interneurons undergo a unique sequence of maturation stages.

No MeSH data available.


Short-term plasticity of developing adult-generated GCs. (A) AMPAR-mediated EPSC amplitude plotted against time for responses to first (top) and second (bottom) stimuli during paired-pulse stimulation. (B) Paired-pulse ratios determined for successful responses (class 3: six slices, six mice; class 4: eleven slices, nine mice; class 5: eight slices, seven mice). (C) Mean responses (successes and failures) to paired-pulse stimulation. Scale bar = 10 ms and 5 pA. (D) Paired-pulse ratios for mean AMPAR-mediated EPSC amplitude (successes and failures) (class 3: six slices, six mice; class 4: eleven slices, nine mice; class 5: eight slices, seven mice).
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Figure 5: Short-term plasticity of developing adult-generated GCs. (A) AMPAR-mediated EPSC amplitude plotted against time for responses to first (top) and second (bottom) stimuli during paired-pulse stimulation. (B) Paired-pulse ratios determined for successful responses (class 3: six slices, six mice; class 4: eleven slices, nine mice; class 5: eight slices, seven mice). (C) Mean responses (successes and failures) to paired-pulse stimulation. Scale bar = 10 ms and 5 pA. (D) Paired-pulse ratios for mean AMPAR-mediated EPSC amplitude (successes and failures) (class 3: six slices, six mice; class 4: eleven slices, nine mice; class 5: eight slices, seven mice).

Mentions: Functional changes in proximal synapses on new GCs may be simultaneously regulated at postsynaptic and presynaptic sites. We examined presynaptic features using a paired-pulse protocol (interstimulus interval 50 ms) (Figure 5A) previously used to measure the efficacy of neurotransmitter release from the presynaptic terminal [37]. The ratio of the success rate of the second response to the success rate of the first response was >1 and remained constant for all neuronal classes (class 3: 1.41 ± 0.10; class 4: 1.36 ± 0.13; class 5: 1.37 ± 0.04) (Figure 5B). We also compared the ratio of the average amplitude of AMPAR-mediated EPSCs (all successes and failures) for the first stimulus to that of the second for developing GCs (Figure 5C). The degree of facilitation in response to paired-pulse stimuli was similar for all classes (class 3: 1.35 ± 0.07; class 4: 1.39 ± 0.12; class 5: 1.42 ± 0.09) (Figure 5D), which suggested that maturation of new GCs was not linked to a change in the probability of glutamate release. Thus, the rapid increase in the NMDAR/AMPAR ratio over time results primarily from postsynaptic changes.


Dynamic development of the first synapse impinging on adult-born neurons in the olfactory bulb circuit.

Katagiri H, Pallotto M, Nissant A, Murray K, Sassoè-Pognetto M, Lledo PM - Neural Syst Circuits (2011)

Short-term plasticity of developing adult-generated GCs. (A) AMPAR-mediated EPSC amplitude plotted against time for responses to first (top) and second (bottom) stimuli during paired-pulse stimulation. (B) Paired-pulse ratios determined for successful responses (class 3: six slices, six mice; class 4: eleven slices, nine mice; class 5: eight slices, seven mice). (C) Mean responses (successes and failures) to paired-pulse stimulation. Scale bar = 10 ms and 5 pA. (D) Paired-pulse ratios for mean AMPAR-mediated EPSC amplitude (successes and failures) (class 3: six slices, six mice; class 4: eleven slices, nine mice; class 5: eight slices, seven mice).
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Related In: Results  -  Collection

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Figure 5: Short-term plasticity of developing adult-generated GCs. (A) AMPAR-mediated EPSC amplitude plotted against time for responses to first (top) and second (bottom) stimuli during paired-pulse stimulation. (B) Paired-pulse ratios determined for successful responses (class 3: six slices, six mice; class 4: eleven slices, nine mice; class 5: eight slices, seven mice). (C) Mean responses (successes and failures) to paired-pulse stimulation. Scale bar = 10 ms and 5 pA. (D) Paired-pulse ratios for mean AMPAR-mediated EPSC amplitude (successes and failures) (class 3: six slices, six mice; class 4: eleven slices, nine mice; class 5: eight slices, seven mice).
Mentions: Functional changes in proximal synapses on new GCs may be simultaneously regulated at postsynaptic and presynaptic sites. We examined presynaptic features using a paired-pulse protocol (interstimulus interval 50 ms) (Figure 5A) previously used to measure the efficacy of neurotransmitter release from the presynaptic terminal [37]. The ratio of the success rate of the second response to the success rate of the first response was >1 and remained constant for all neuronal classes (class 3: 1.41 ± 0.10; class 4: 1.36 ± 0.13; class 5: 1.37 ± 0.04) (Figure 5B). We also compared the ratio of the average amplitude of AMPAR-mediated EPSCs (all successes and failures) for the first stimulus to that of the second for developing GCs (Figure 5C). The degree of facilitation in response to paired-pulse stimuli was similar for all classes (class 3: 1.35 ± 0.07; class 4: 1.39 ± 0.12; class 5: 1.42 ± 0.09) (Figure 5D), which suggested that maturation of new GCs was not linked to a change in the probability of glutamate release. Thus, the rapid increase in the NMDAR/AMPAR ratio over time results primarily from postsynaptic changes.

Bottom Line: We found that both the ratio of N-methyl-D-aspartate receptor (NMDAR) to α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR), and the number of functional release sites at proximal inputs reached a maximum during the critical period for the sensory-dependent survival of newborn cells, well before the completion of dendritic arborization.Interestingly, the latter morphological changes disappeared in more mature newly-formed neurons, when the NMDAR to AMPAR ratio had decreased and functional presynaptic terminals expressed only single release sites.Together, these findings show that the first glutamatergic inputs to adult-generated OB interneurons undergo a unique sequence of maturation stages.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratory for Perception and Memory, Institut Pasteur, Paris, France. pmlledo@pasteur.fr.

ABSTRACT
The olfactory bulb (OB) receives and integrates newborn interneurons throughout life. This process is important for the proper functioning of the OB circuit and consequently, for the sense of smell. Although we know how these new interneurons are produced, the way in which they integrate into the pre-existing ongoing circuits remains poorly documented. Bearing in mind that glutamatergic inputs onto local OB interneurons are crucial for adjusting the level of bulbar inhibition, it is important to characterize when and how these inputs from excitatory synapses develop on newborn OB interneurons. We studied early synaptic events that lead to the formation and maturation of the first glutamatergic synapses on adult-born granule cells (GCs), the most abundant subtype of OB interneuron. Patch-clamp recordings and electron microscopy (EM) analysis were performed on adult-born interneurons shortly after their arrival in the adult OB circuits. We found that both the ratio of N-methyl-D-aspartate receptor (NMDAR) to α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR), and the number of functional release sites at proximal inputs reached a maximum during the critical period for the sensory-dependent survival of newborn cells, well before the completion of dendritic arborization. EM analysis showed an accompanying change in postsynaptic density shape during the same period of time. Interestingly, the latter morphological changes disappeared in more mature newly-formed neurons, when the NMDAR to AMPAR ratio had decreased and functional presynaptic terminals expressed only single release sites. Together, these findings show that the first glutamatergic inputs to adult-generated OB interneurons undergo a unique sequence of maturation stages.

No MeSH data available.