Abstract
A unique feature of the olfactory system is the continuous generation and integration of new neurons throughout adulthood. Adult-born neuron survival and integration is dependent on activity and sensory experience, which is largely mediated by early synaptic inputs that adult-born neurons receive upon entering the olfactory bulb (OB). As in early postnatal development, the first synaptic inputs onto adult-born neurons are GABAergic. However, the specific sources of early synaptic GABA and the influence of specific inputs on adult-born neuron development are poorly understood. Here, we use retrograde and anterograde viral tracing to reveal robust GABAergic projections from the basal forebrain horizontal limb of the diagonal band of Broca (HDB) to the granule cell layer (GCL) and glomerular layer (GL) of the mouse OB. Whole-cell electrophysiological recordings indicate that these projections target interneurons in the GCL and GL, including adult-born granule cells (abGCs). Recordings from birth-dated abGCs reveal a developmental time course in which HDB GABAergic input onto abGCs emerges as the neurons first enter the OB, and strengthens throughout the critical period of abGC development. Finally, we show that removing GABAergic signaling from HDB neurons results in decreased abGC survival. Together these data show that GABAergic projections from the HDB synapse onto immature abGCs in the OB to promote their survival through the critical period, thus representing a source of long-range input modulating plasticity in the adult OB.
Highlights
Olfaction is a key sensory modality guiding behaviors from feeding to mating
Given the influence that long-range GABAergic signaling has over both acute circuit function and neuronal development, we first sought to identify GABAergic neuron populations that project to the olfactory bulb (OB)
While OB-projecting GABAergic neurons comprised significant populations of anterior olfactory nucleus (AON), lateral septum (LS), and horizontal diagonal band of Broca (HDB) neurons, OB-projecting GABAergic neurons in ventral subiculum (vSUB) were merely trending toward significance as a population, reflecting their relative sparseness (Figure 1H)
Summary
Olfaction is a key sensory modality guiding behaviors from feeding to mating. To interpret olfactory information in different contexts, sensory processing adapts throughout life to an animal’s experience, and changes moment-to-moment based on context and behavioral state. Only about half of the adult-born neurons that enter the OB survive (Petreanu and Alvarez-Buylla, 2002; Winner et al, 2002; Yamaguchi and Mori, 2005) This process is influenced by sensory experience, with olfactory deprivation leading to decreased survival and enrichment leading to increased survival, integration, and maturation of receptive fields (Corotto et al, 1994; Fiske and Brunjes, 2001; Petreanu and Alvarez-Buylla, 2002; Rochefort et al, 2002; Alonso et al, 2006; Quast et al, 2016). To this end, rabies-based retrograde tracing from abGCs showed local OB inputs to young abGCs (Deshpande et al, 2013). It is necessary to take additional anatomical and functional approaches to investigate potential, early inputs onto abGCs that may influence abGC survival and maturation
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