Persistent Structural Plasticity Optimizes Sensory Information Processing in the Olfactory Bulb

Abstract

SUMMARY In the mammalian brain, the anatomical structure of neural circuits changes little during adulthood. As a result, adult learning and memory are thought to result from specific changes in synaptic strength. A possible exception is the olfactory bulb (OB), where activity guides interneuron turnover throughout adulthood. These adult-born granule cell (GC) interneurons form new GABAergic synapses that have little synaptic strength plasticity. In the face of persistent neuronal and synaptic turnover, how does the OB balance flexibility, as is required for adapting to changing sensory environments, with perceptual stability? Here we show that high dendritic spine turnover is a universal feature of GCs, regardless of their developmental origin and age. We find matching dynamics among postsynaptic sites on the principal neurons receiving the new synaptic inputs. We further demonstrate in silico that this coordinated structural plasticity is consistent with stable, yet flexible, decorrelated sensory representations. Together, our study reveals that persistent, coordinated synaptic structural plasticity between interneurons and principal neurons is a major mode of functional plasticity in the OB.

Development and Refinement of Functional Properties of Adult-Born Neurons

“…Two animals were excluded from the young dendrites population data (Figure 2) because measured odor concentrations with a PID were not consistent with concentrations during the rest of the experiment. The number of animals used and the number of trials or repetitions per animal were large enough to obtain a data set with statistical power and are congruent with previously published studies in the field (for example, Livneh et al, 2014; Sailor et al, 2016). Variance within a group was described as SEM or as interquartile range where noted in the figure legend.…”

“…The period of functional plasticity we have described also corresponds to the time period when the spines of abGCs are most dynamic (Sailor et al, 2016), providing a mechanism for abGCs to sample ongoing circuit activity during the period in which they are highly responsive. Enrichment led to a higher degree of sampling of odor information over a longer time period in our paradigm, which involved uniform enrichment with all odors.…”

Top-down inputs drive neuronal network rewiring and context-enhanced sensory processing in olfaction

“…However, for the discrimination of the Fig.6B) and MCs representing odor O 3 (MC index near 80) was small. However, these 264 MCs are activated simultaneously in the mixtures and mutual inhibition of these MCs is 265 needed to enhance the discrimination between the mixtures [17,35,40,41]. As a result 266 the inhibition significantly reduced the relative difference between the two mixtures and 267 with it their Fisher discriminant ( Figures 6F left,G).…”

“…81 The network structure arising in this model for a range of suitable parameter values 82 is illustrated in Fig.1A for a simple set of two training stimuli that activated partially 83 overlapping sets of MCs. Throughout we used such simplified odor-evoked patterns 84 rather than natural stimuli [17,35], because they facilitated the visualization and 85 understanding of the emerging network connectivities. Since all connections were 86 learned based on activities, the spatial arrangement of the various neurons played no 87 role in the model.…”

“…93 To wit, in Fig.1A one population of GCs was mostly driven by MCs and CCs 94 responding to the left training stimulus, while the other population responded to the 95 one on the right. Due to the reciprocal nature of the MC-GC synapses [36] this induced 96 disynaptic inhibition of MCs not only by other MCs with similar receptive fields [17,35], 97 but also by cortical CCs that share that receptive field (cf. supplementary Fig.S1 Fig).…”