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.
Highlights
Adult neurogenesis, a process encompassing the generation, maturation and synaptic integration of new neurons in the adult brain, represents a striking form of structural adult neural plasticity [1,2,3]
Because long-term potentiation (LTP) has been observed at the proximal synapses of granule cells (GCs) [25,26], it is possible that the changes in the number of synaptic contacts we found might reflect some form of synaptic plasticity
Our results provide a conceptual framework for understanding mechanisms underlying the precise control of neural wiring through presynaptic and postsynaptic events during adult neurogenesis
Summary
A process encompassing the generation, maturation and synaptic integration of new neurons in the adult brain, represents a striking form of structural adult neural plasticity [1,2,3]. The newly-formed interneurons project dendrites that establish synaptic contacts with pre-existing partners, GCs are the largest population of interneurons in the bulb, outnumbering principal neurons by 100 to one [14]. GCs form g-aminobutyric acid (GABA)ergic output synapses onto the principal neurons, the mitral cells/tufted cells (MC/TCs), through dendrodendritic reciprocal contacts in the external plexiform layer [14]. They receive spatially segregated glutamatergic inputs at distinct dendritic sites [13,16,17]. Reciprocal dendrodendritic synapses with the MCs are the main source of distal glutamatergic input
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