Taste arbor structural variability analyzed across taste regions

Abstract

Taste ganglion neurons are functionally and molecularly diverse, but until recently morphological diversity was completely unexplored. Specifically, taste arbors (the portion of the neuron within the taste bud) vary in structure, but the reason for this variability is unclear. Here, we analyzed structural variability in taste arbors to determine which factors determine their morphological diversity. To characterize arbor morphology and its relationship to taste bud cells capable of transducing taste stimuli (taste‐transducing cell) number and type, we utilized sparse cell genetic labeling of taste ganglion neurons in combination with whole‐mount immunohistochemistry. Reconstruction of 151 taste arbors revealed variation in arbor size, complexity, and symmetry. Overall, taste arbors exist on a continuum of complexity, cannot be categorized into discrete morphological groups, and do not have stereotyped endings. Arbor size/complexity was not related to the size of the taste bud in which it was located or the type of taste‐transducing cell contacted (membranes within 180 nm). Instead, arbors could be broadly categorized into three groups: large asymmetrical arbors contacting many taste‐transducing cells, small symmetrical arbors contacting one or two taste‐transducing cells, and unbranched arbors. Neurons with multiple arbors had arbors in more than one of these categories, indicating that this variability is not an intrinsic feature of neuron type. Instead, we speculate that arbor structure is determined primarily by nerve fiber remodeling in response to cell turnover and that large asymmetrical arbors represent a particularly plastic state.

Rapid structural remodeling of peripheral taste neurons is independent of taste cell turnover

“…Therefore, we anticipated that approximately half of all arbors sampled would lose their connection to a taste bud cell and/or gain a new connection within 10 days. We expected that arbor structure would be stable while connected to a taste bud cell, remodeling only when connections were broken [ 12 ]. This type of phasic remodeling is observed in terminations of touch neurons that receive input from Merkel cells [ 48 ].…”

“…Previously, we hypothesized taste arbors remodel to connect with new taste cells over time [ 12 ]. This model assumed that taste bud cells provide an extrinsic signal to influence arbor remodeling.…”

“…Individual arbor size does vary over time; however, some individual arbors appear to change in size more than others. We recently found that individual taste neurons either have all small arbors or have a mix of large and small arbors [ 12 ]. So, it may be that arbor size only varies within a range of possibilities, particularly for small arbors.…”

“…At T0, the taste bud is outlined (green line), and the connective tissue core of the papilla is outlined specific anatomical trait, for example, terminal varicosities, in the arbor that have been described in conjunction with these connections. Contacts between taste arbors and taste bud cells frequently occur on the terminal branches of arbors [12]. If the turnover of taste bud cells regulates arbor structure, then terminal branches are likely to remodel as taste bud cells die and/or new cells enter the taste bud.…”

“…Progress toward understanding the cellular movements occurring during taste bud cell turnover has been hindered by analysis of fixed-tissue [ 1 , 2 , 10 , 11 ]. This approach fails to capture the dynamic processes within the taste bud, such as taste cell movements and axon remodeling [ 1 , 2 , 12 ]. Fixed-tissue studies also fail to describe what happens to axon remodeling when cell turnover is disrupted (e.g., chemotherapies) [ 6 , 8 , 13 ].…”