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Open Access Research article

Nuclei-specific differences in nerve terminal distribution, morphology, and development in mouse visual thalamus

Sarah Hammer12, Gabriela L Carrillo13, Gubbi Govindaiah6, Aboozar Monavarfeshani14, Joseph S Bircher15, Jianmin Su1, William Guido6 and Michael A Fox145*

Author Affiliations

1 Virginia Tech Carilion Research Institute, 2 Riverside Circle, Roanoke, VA 24016, USA

2 Roanoke Valley Governor School, 2104 Grandin Road SW, Roanoke, VA 24015, USA

3 Department of Psychology, Virginia Tech, 109 Williams Hall, Blacksburg, VA 24061, USA

4 Department of Biological Sciences, Virginia Tech, 2125 Derring Hall, Blacksburg, VA 24061, USA

5 Virginia Tech Carilion School of Medicine, 2 Riverside Circle, Roanoke, VA 24016, USA

6 Department of Anatomical Sciences and Neurobiology, University of Louisville, 511 South Floyd, Louisville, KY 40202, USA

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Neural Development 2014, 9:16  doi:10.1186/1749-8104-9-16

Published: 10 July 2014

Abstract

Background

Mouse visual thalamus has emerged as a powerful model for understanding the mechanisms underlying neural circuit formation and function. Three distinct nuclei within mouse thalamus receive retinal input, the dorsal lateral geniculate nucleus (dLGN), the ventral lateral geniculate nucleus (vLGN), and the intergeniculate nucleus (IGL). However, in each of these nuclei, retinal inputs are vastly outnumbered by nonretinal inputs that arise from cortical and subcortical sources. Although retinal and nonretinal terminals associated within dLGN circuitry have been well characterized, we know little about nerve terminal organization, distribution and development in other nuclei of mouse visual thalamus.

Results

Immunolabeling specific subsets of synapses with antibodies against vesicle-associated neurotransmitter transporters or neurotransmitter synthesizing enzymes revealed significant differences in the composition, distribution and morphology of nonretinal terminals in dLGN, vLGN and IGL. For example, inhibitory terminals are more densely packed in vLGN, and cortical terminals are more densely distributed in dLGN. Overall, synaptic terminal density appears least dense in IGL. Similar nuclei-specific differences were observed for retinal terminals using immunolabeling, genetic labeling, axonal tracing and serial block face scanning electron microscopy: retinal terminals are smaller, less morphologically complex, and more densely distributed in vLGN than in dLGN. Since glutamatergic terminal size often correlates with synaptic function, we used in vitro whole cell recordings and optic tract stimulation in acutely prepared thalamic slices to reveal that excitatory postsynaptic currents (EPSCs) are considerably smaller in vLGN and show distinct responses following paired stimuli. Finally, anterograde labeling of retinal terminals throughout early postnatal development revealed that anatomical differences in retinal nerve terminal structure are not observable as synapses initially formed, but rather developed as retinogeniculate circuits mature.

Conclusions

Taken together, these results reveal nuclei-specific differences in nerve terminal composition, distribution, and morphology in mouse visual thalamus. These results raise intriguing questions about the different functions of these nuclei in processing light-derived information, as well as differences in the mechanisms that underlie their unique, nuclei-specific development.

Keywords:
Retina; Thalamus; Retinogeniculate; Lateral geniculate nucleus; Axon; Retinal terminal; Nerve terminal