Abstract
To better understand how individual genes and experience influence behavior, the role of a single homeotic unit, hoxb4a, was comprehensively analyzed in vivo by clonal and retrograde fluorescent labeling of caudal hindbrain neurons in a zebrafish enhancer-trap YFP line. A quantitative spatiotemporal neuronal atlas showed hoxb4a activity to be highly variable and mosaic in rhombomere 7–8 reticular, motoneuronal and precerebellar nuclei with expression decreasing differentially in all subgroups through juvenile stages. The extensive Hox mosaicism and widespread pleiotropism demonstrate that the same transcriptional protein plays a role in the development of circuits that drive behaviors from autonomic through motor function including cerebellar regulation. We propose that the continuous presence of hoxb4a positive neurons may provide a developmental plasticity for behavior-specific circuits to accommodate experience- and growth-related changes. Hence, the ubiquitous hoxb4a pleitropism and modularity likely offer an adaptable transcriptional element for circuit modification during both growth and evolution.
Highlights
The hindbrain contains a broad neuronal diversity essential for survival in all vertebrates [1,2]
Confocal microscopy was used to document hoxb4a activity reported in the CLGY 838 enhancer trap line [27]
While yellow fluorescent protein (YFP) was observed in both somites and hindbrain at,12 hrs (Fig. 1A), it was no longer detected in the somites by 1 day and became largely restricted to the caudal hindbrain through 30 days as r7–8 increased in length by,25%
Summary
The hindbrain contains a broad neuronal diversity essential for survival in all vertebrates [1,2]. Comparative developmental studies have shown it to be subdivided into segments, or rhombomeres, wherein serial repeats give rise to specific cranial motoneurons (IV–XII) along the anterior-posterior axis [3]. R7–8 gives rise to highly specialized neurons and circuits for cardiac-respiratory and intestinal function [4], locomotion [5] and posture [2,6] along with the major precerebellar circuits responsible for motor coordination and learning [7,8,9]. Many r7–8 neurons such as the inferior olivary, vocal, electromotor and respiratory exhibit pacemaker-like rhythmic physiological properties suggesting that this compartment might be uniquely specified and evolutionary conserved for premotor circuitry underlying rhythmic behaviors [2,10]. Ancestral conserved hindbrain genetic regulatory pathways exhibit a combinatorial expression of Hox genes [11,12]; the role of any 59 Hox gene in either the formation or maturation, let alone the evolutional modification, of rhythmic circuits for any behavior remains unexplored [13]
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