Abstract
Vesicular transporter proteins are an essential component of the presynaptic machinery that regulates neurotransmitter storage and release. They also provide a key point of control for homeostatic signaling pathways that maintain balanced excitation and inhibition following changes in activity levels, including the onset of sensory experience. To advance understanding of their roles in the developing auditory forebrain, we tracked the expression of the vesicular transporters of glutamate (VGluT1, VGluT2) and GABA (VGAT) in primary auditory cortex (A1) and medial geniculate body (MGB) of developing mice (P7, P11, P14, P21, adult) before and after ear canal opening (~P11–P13). RNA sequencing, in situ hybridization, and immunohistochemistry were combined to track changes in transporter expression and document regional patterns of transcript and protein localization. Overall, vesicular transporter expression changed the most between P7 and P21. The expression patterns and maturational trajectories of each marker varied by brain region, cortical layer, and MGB subdivision. VGluT1 expression was highest in A1, moderate in MGB, and increased with age in both regions. VGluT2 mRNA levels were low in A1 at all ages, but high in MGB, where adult levels were reached by P14. VGluT2 immunoreactivity was prominent in both regions. VGluT1 + and VGluT2 + transcripts were co-expressed in MGB and A1 somata, but co-localization of immunoreactive puncta was not detected. In A1, VGAT mRNA levels were relatively stable from P7 to adult, while immunoreactivity increased steadily. VGAT + transcripts were rare in MGB neurons, whereas VGAT immunoreactivity was robust at all ages. Morphological changes in immunoreactive puncta were found in two regions after ear canal opening. In the ventral MGB, a decrease in VGluT2 puncta density was accompanied by an increase in puncta size. In A1, perisomatic VGAT and VGluT1 terminals became prominent around the neuronal somata. Overall, the observed changes in gene and protein expression, regional architecture, and morphology relate to—and to some extent may enable—the emergence of mature sound-evoked activity patterns. In that regard, the findings of this study expand our understanding of the presynaptic mechanisms that regulate critical period formation associated with experience-dependent refinement of sound processing in auditory forebrain circuits.
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Abbreviations
- A1:
-
Primary auditory cortex, area 1
- AC:
-
Auditory cortex
- AuD:
-
Auditory cortex, dorsal area
- AuV:
-
Auditory cortex, ventral area
- CC:
-
Corticocortical connections
- CT:
-
Corticothalamic connections
- Ct:
-
Corticotectal connections
- D:
-
Medial geniculate body, dorsal division
- DAPI:
-
4′,6-Diamidino-2-phenylindole
- DC:
-
Inferior colliculus, dorsal cortex
- dLGN:
-
Lateral geniculate nucleus, dorsal division
- GAPDH:
-
Glyceraldehyde-3-phosphate dehydrogenase
- IC:
-
Inferior colliculus
- ICc:
-
Inferior colliculus, central nucleus
- IHC:
-
Immunohistochemistry
- ISH:
-
In situ hybridization
- Hip:
-
Hippocampus
- LC:
-
Inferior colliculus, lateral cortex
- M:
-
Medial geniculate body, medial division
- MGB:
-
Medial geniculate body
- MGd:
-
Medial geniculate body, dorsal division
- MGm:
-
Medial geniculate body, medial division
- MGv:
-
Medial geniculate body, ventral division
- NeuN:
-
Neuron-specific RNA-binding protein, Fox-3
- PAG:
-
Periaqueductal gray
- PP:
-
Thalamus, peripeduncular nucleus
- rf:
-
Rhinal fissure
- Rt:
-
Reticular nucleus
- RT:
-
Reticulothalamic connections
- SC:
-
Superior colliculus
- Sg:
-
Thalamus, suprageniculate nucleus
- TC:
-
Thalamocortical connections
- TRN:
-
Thalamic reticular nucleus
- tT:
-
Tectothalamic connections
- TeA:
-
Temporal cortex area A
- V:
-
Medial geniculate body, ventral division
- VGluT1:
-
Vesicular glutamate transporter 1
- VGluT2:
-
Vesicular glutamate transporter 2
- VGAT:
-
Vesicular GABA/glycine transporter
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Acknowledgments
Special thanks to Tia Hughes and Cara Sutcliffe in the VANTAGE core at Vanderbilt University for expert assistance with RNA isolation and sample quality assessment; Dr. Holli Hutcheson Dilks in the VANTAGE core for design and supervision of RNA sequencing; Dr. Yan Guo in the VANGARD core for expertise and implementation of bioinformatics analyses. The authors gratefully acknowledge the support of NIH/NIDCD grants K18 DC012527 to T.A.H. and R01 DC009836 to D.P.
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Hackett, T.A., Clause, A.R., Takahata, T. et al. Differential maturation of vesicular glutamate and GABA transporter expression in the mouse auditory forebrain during the first weeks of hearing. Brain Struct Funct 221, 2619–2673 (2016). https://doi.org/10.1007/s00429-015-1062-3
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DOI: https://doi.org/10.1007/s00429-015-1062-3