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A Structural and Functional Ground Plan for Neurons in the Hindbrain of Zebrafish

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A Structural and Functional Ground Plan for Neurons in the Hindbrain of Zebrafish A structural and functional ground plan for neurons in the hindbrain of zebrafish Amina Kinkhabwalaa,b, Michael Rileya, Minoru Koyamaa, Joost Monena, Chie Satouc,d, Yukiko Kimurac, Shin-ichi Higashijimac,d, and Joseph Fetchoa,1 aDepartment of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853; bPrinceton Neuroscience Institute, Princeton University, Princeton, NJ 08544; cOkazaki Institute for Integrative Bioscience, National Institute for Physiological Sciences, National Institutes of Natural Sciences, Okazaki, Aichi 444-8787, Japan; and dDepartment of Physiological Sciences, Graduate University for Advanced Studies (SOKENDAI), Okazaki, Aichi 444-8585, Japan Edited by Lynn T. Landmesser, Case Western Reserve University, Cleveland, OH, and approved December 9, 2010 (received for review August 16, 2010) The vertebrate hindbrain contains various sensory-motor net- when they are freely swimming and most of the major adult works controlling movements of the eyes, jaw, head, and body. behaviors driven by hindbrain—e.g., swimming, feeding, and eye Here we show that stripes of neurons with shared neurotransmit- movements—are functional. This suggests that the diverse net- ter phenotype that extend throughout the hindbrain of young works in hindbrain might share an orderly functional patterning of fl zebrafish reflect a broad underlying structural and functional neurons. We now show that the transmitter stripes re ect an patterning. The neurotransmitter stripes contain cell types with underlying order in the hindbrain in which stripes contain cell shared gross morphologies and transcription factor markers. types, stacked in order by age as well as structural and functional Neurons within a stripe are stacked systematically by extent and properties. This pattern is tied to behavior because neurons are location of axonal projections, input resistance, and age, and are recruited along the axis of a stripe as the speed of a motor be- havior increases. We conclude that the diverse networks in the recruited along the axis of the stripe during behavior. The hindbrain have at their foundation a common structural and implication of this pattern is that the many networks in hindbrain functional plan. are constructed from a series of neuronal components organized into stripes that are ordered from top to bottom according to Results a neuron’s age, structural and functional properties, and behav- Hindbrain Transmitter Stripes and Transcription Factor Patterning. ioral roles. This simple organization probably forms a foundation We examined the transmitter stripe patterning in more than 20 for the construction of the networks underlying the many behav- larval, posthatching fish from each of two BAC transgenic lines iors produced by the hindbrain. expressing green (GFP) and red (DsRed) fluorescent proteins driven by promoter regions of glyt2 and vglut2.1 (vglut2) to mark interneuron | locomotion | recruitment | topography glycinergic and glutamatergic neurons, respectively (24, 25). Stripes were clearly evident in the hindbrain of dual transgenic lines (vglut: he hindbrain contains a diverse set of sensory-motor networks DsRed × glyt2:GFP), as shown in the example from a 4-d post- Tthat control movements required for vision, respiration, mas- fertilization (dpf) fish in Fig. 1A (n = 16). In cross-sections, these tication, and locomotion in all vertebrates (1, 2). Most often these stripes were organized in an interleaved manner from medial to different networks are studied separately from one another, per- lateral on each side of the brain in all hindbrain segments (rhom- haps because the behaviors are distinct, and the regional differ- bomeres), with a glutamatergic stripe located medially followed by entiation of hindbrain suggests that its several networks might alternating glycinergic and glutamatergic stripes that extend pre- have little in common. Thus, we have strong data for the hindbrain dominately dorsoventrally and rostrocaudally. This organization control of eye movements, respiration, and locomotion (3–10), but was present in all of the fish. Although the glycinergic and gluta- fewer unifying principles of structural and functional organization matergic neurons were segregated from one another in a columnar that apply across the different networks. pattern, there were other unlabeled neurons, both scattered within Structurally, the hindbrain is divided into segments, called stripes and in large contiguous areas between stripes that are rhombomeres, which differ in the expression of homeotic genes, probably neurons with other transmitter phenotypes (cholinergic in the morphological differentiation of neurons, and in their and GABAergic, e.g.) based upon prior in situ staining (23). sensory inputs and motor outputs (2, 11). Though there are clear We next used transgenic lines and immunostaining to in- distinctions among rhombomeres, there are indications from vestigate the relationship between the transmitter stripes and the previous developmental work using in situ staining for tran- transcription factors alx (called chx10 in mammals), dbx1b, en- scription factors and backfilling of hindbrain neurons that there grailed-1, and barhl2. The transcription factors were expressed may be structural patterns that cross rhombomere boundaries in stripe-like patterns resembling the patterning of transmitter (12–16). Prior work has also revealed parallels in the deve- stripes. Neurons expressing the alx (chx10) transcription factor were clustered medially and overlapped the most medial gluta- lopment of hindbrain and spinal cord, with the hindbrain sharing B features of the now-classic transcription factor code that directs matergic stripe (Fig. 1 ). Three-dimensional colocalization – revealed that most, if not all, medial glutamatergic stripe neu- development in spinal cord (17 22). Though these studies did B n not explore function because they were performed during early rons express the alx transcription factor (Fig. 1 , panel 3; =2 fish). Immunostaining for alx protein in the alx:GFP transgenic development, they raised the possibility of a broader structural- fi functional patterning that spans rhomobomeres and may un- line con rmed that this line reliably marked the alx positive derlie the organization of circuits for different behaviors. Here we show that there is indeed a broad structural and functional patterning of neurons in the hindbrain of young Author contributions: A.K. and J.F. designed research; A.K., M.R., M.K., and J.M. per- zebrafish. The work was initially prompted by a striking patterning formed research; C.S., Y.K., and S.-i.H. contributed new reagents/analytic tools; A.K., observed in earlier work in which we used in situ staining for M.R., M.K., J.M., and J.F. analyzed data; and A.K. and J.F. wrote the paper. markers of neurotransmitter phenotype to reveal putative glyci- The authors declare no conflict of interest. nergic, GABAergic, and glutamatergic neurons in the hindbrain This article is a PNAS Direct Submission. (23). We found that neurons of the same transmitter phenotype Freely available online through the PNAS open access option. were clustered together into stripes when viewed in cross-sections, 1To whom correspondence should be addressed. E-mail: [email protected]. and that these extended as columns throughout much of the This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. rostrocaudal axis of the hindbrain. The pattern is evident in fish 1073/pnas.1012185108/-/DCSupplemental. 1164–1169 | PNAS | January 18, 2011 | vol. 108 | no. 3 www.pnas.org/cgi/doi/10.1073/pnas.1012185108 Downloaded by guest on September 29, 2021 glutamatergic domain and, more lateral, most likely, glycinergic one. Neurons expressing the barhl2 transcription factor were located in a band at the lateral edge of the hindbrain (Fig. 1E; n = 10), overlapping a portion of a lateral crescent-like stripe of glutamatergic neurons throughout hindbrain (Fig. 1E, panel 3). In summary, neurons expressing particular transcription factors are clustered into bands that align with neurotransmitter stripes and, depending on the transcription factor, can be coextensive with a transmitter stripe (alx, engrailed-1), overlap multiple transmitter stripes (dbx1b), or overlap only a restricted, spatially segregated portion of a stripe (barhl2). We examined how the distribution of neurons expressing these transcription factors changes from spinal cord (where they are also expressed) into the hindbrain by examining optical cross-sections at different rostrocaudal locations from confocal image stacks from live fish in which neurons expressing two transcription factors (alx and barhl2) were labeled in different colors. A dorsoventral segregation of the different transcription factors in spinal cord gradually changed at its rostral end into a mediolateral segregation in hindbrain, indicating a topological transformation in expression domains between the two regions (Fig. 1F). Morphology of Neurons in the Transmitter Stripes. We used sto- chastic expression of membrane targeted proteins (mMCherry, mGFP, or Brainbow-1.1) to randomly label neurons in one color in 5- to 6-dpf fish in which the transmitter stripes were labeled in a different color. We then reconstructed the neurons in 3D and sorted them by stripe membership. Reconstructed neurons from four stripes—the medial glutamatergic stripe and the three gly- — Fig. 1. Interleaved transmitter stripes of neurons in hindbrain and their cinergic stripes are shown in dorsal view in Fig.
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