Sensory experience shapes the integration of adult-born neurons into the olfactory bulb

Abstract

Olfaction is an ancient sensory modality which is heavily involved in viscerally-important tasks like finding food and identifying mates. Olfactory processing involves interpreting stimuli from a non-continuous odor space, and translating them into an organized pattern of neuronal activity in the olfactory bulb. Additionally, olfactory processing is rapidly modulated by behavioral states and vice versa. This implies strong bidirectional neuromodulation between the olfactory bulb and other brain regions that include the cortex, hippocampus, and basal forebrain. Intriguingly, the olfactory bulb is one of the only brain regions where adult-born neurons are integrated into existing networks throughout life. The ongoing integration of adult-born neurons is known to be important for olfactory processing, odor discrimination, and odor learning. Furthermore, the survival and integration of the adult-born neurons is regulated by neuromodulatory signaling, sensory experience, and olfactory learning. Studies making use of new genetic markers to label and manipulate immature adult-born neurons reveal an increase in their population response to odors as they mature. Importantly, this reflects a period of developmental plasticity where adult-born neurons are especially sensitive to sensory experience and olfactory learning. In this review, we discuss the contribution of adult neurogenesis to olfactory bulb plasticity and information processing, with a focus on the developmental plasticity of adult born neurons, and how it is influenced by sensory experience and olfactory learning. Ultimately, recent studies raise important questions about behavioral-state-dependent effects on adult-born neurons, and the consequences of neuromodulation on the developmental plasticity of newborn neurons in the olfactory bulb.

Keywords: Adult neurogenesis; development; experience; learning; olfaction.

Figure 1. The integration of adult born neurons into OB networks is influenced by sensory experience and learning

A. Inhibitory granule cells (GCs), located in the granule cell layer (GCL) and excitatory mitral cells (orange triangles), located in the mitral cell layer (MCL), make dendrodendritic reciprocal synapses (orange and green circles) in the external plexiform layer (EPL, grey dashed line). Adult-born GCs (green circles) initially receive few excitatory inputs from mitral and tufted cells (M/TCs) (left). Over the course of their development and integration into OB networks, they receive progressively more inputs from M/TCs (right). B. The limited synaptic connectivity between M/TCs and immature adult-born GCs results in a smaller population of immature GCs activated in response to specific odors (left). This corresponds to a small sensory response area in immature GCs (dashed outline). As adult-born GCs mature, they respond to a broader array of odors, causing the GC sensory maps for individual odors to expand (right). The mouse head diagram (inset) shows the OB (green) and the location and orientation of sensory map recordings made through the thinned skull (yellow box). Importantly, the developmental expansion of GC sensory maps is modulated by sensory experience and olfactory learning. Sensory deprivation inhibits the expansion of GC sensory maps. Associative odor learning, on the other hand, potentiates the developmental map expansion.