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Synaptic properties of the feedback connections from the thalamic reticular nucleus to the dorsal lateral geniculate nucleus.
J Neurophysiol. 2020 Aug 01; 124(2):404-417.JN

Abstract

The thalamic reticular nucleus (TRN) is a shell-like structure comprised of GABAergic neurons that surrounds the dorsal thalamus. While playing a key role in modulating thalamocortical interactions, TRN inhibition of thalamic activity is often thought of as having an all-or-none impact. Although TRN neurons have a dynamic firing range, it remains unclear how variable rates of TRN activity gate thalamocortical transmission. To address this, we examined the ultrastructural features and functional synaptic properties of the feedback connections in the mouse thalamus between TRN and the dorsal lateral geniculate nucleus (dLGN), the principal relay of retinal signals to visual cortex. Using electron microscopy to identify TRN input to dLGN, we found that TRN terminals formed synapses with non-GABAergic postsynaptic profiles. Compared with other nonretinal terminals in dLGN, those from TRN were relatively large and tended to contact proximal regions of relay cell dendrites. To evoke TRN activity in dLGN, we adopted an optogenetic approach by expressing ChR2, or a variant (ChIEF) in TRN terminals. Both in vitro and in vivo recordings revealed that repetitive stimulation of TRN terminals led to a frequency-dependent inhibition of dLGN activity, with higher rates of stimulation resulting in increasing levels of membrane hyperpolarization and corresponding decreases in spike firing. This relationship suggests that alterations in TRN activity lead to graded changes in relay cell spike firing.NEW & NOTEWORTHY The thalamic reticular nucleus (TRN) modulates thalamocortical transmission through inhibition. In mouse, TRN terminals in the dorsal lateral geniculate nucleus (dLGN) form synapses with relay neurons but not interneurons. Stimulation of TRN terminals in dLGN leads to a frequency-dependent form of inhibition, with higher rates of stimulation leading to a greater suppression of spike firing. Thus, TRN inhibition appears more dynamic than previously recognized, having a graded rather than an all-or-none impact on thalamocortical transmission.

Authors+Show Affiliations

Department of Anatomical Sciences and Neurobiology, University of Louisville School of Medicine, Louisville, Kentucky.Department of Anatomical Sciences and Neurobiology, University of Louisville School of Medicine, Louisville, Kentucky.Department of Anatomical Sciences and Neurobiology, University of Louisville School of Medicine, Louisville, Kentucky.Department of Anatomical Sciences and Neurobiology, University of Louisville School of Medicine, Louisville, Kentucky.Department of Anatomical Sciences and Neurobiology, University of Louisville School of Medicine, Louisville, Kentucky.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

32609582

Citation

Campbell, Peter W., et al. "Synaptic Properties of the Feedback Connections From the Thalamic Reticular Nucleus to the Dorsal Lateral Geniculate Nucleus." Journal of Neurophysiology, vol. 124, no. 2, 2020, pp. 404-417.
Campbell PW, Govindaiah G, Masterson SP, et al. Synaptic properties of the feedback connections from the thalamic reticular nucleus to the dorsal lateral geniculate nucleus. J Neurophysiol. 2020;124(2):404-417.
Campbell, P. W., Govindaiah, G., Masterson, S. P., Bickford, M. E., & Guido, W. (2020). Synaptic properties of the feedback connections from the thalamic reticular nucleus to the dorsal lateral geniculate nucleus. Journal of Neurophysiology, 124(2), 404-417. https://doi.org/10.1152/jn.00757.2019
Campbell PW, et al. Synaptic Properties of the Feedback Connections From the Thalamic Reticular Nucleus to the Dorsal Lateral Geniculate Nucleus. J Neurophysiol. 2020 Aug 1;124(2):404-417. PubMed PMID: 32609582.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Synaptic properties of the feedback connections from the thalamic reticular nucleus to the dorsal lateral geniculate nucleus. AU - Campbell,Peter W, AU - Govindaiah,Gubbi, AU - Masterson,Sean P, AU - Bickford,Martha E, AU - Guido,William, Y1 - 2020/07/01/ PY - 2020/7/2/pubmed PY - 2020/7/2/medline PY - 2020/7/2/entrez KW - dorsal lateral geniculate nucleus KW - inhibition KW - mouse KW - thalamic reticular nucleus SP - 404 EP - 417 JF - Journal of neurophysiology JO - J. Neurophysiol. VL - 124 IS - 2 N2 - The thalamic reticular nucleus (TRN) is a shell-like structure comprised of GABAergic neurons that surrounds the dorsal thalamus. While playing a key role in modulating thalamocortical interactions, TRN inhibition of thalamic activity is often thought of as having an all-or-none impact. Although TRN neurons have a dynamic firing range, it remains unclear how variable rates of TRN activity gate thalamocortical transmission. To address this, we examined the ultrastructural features and functional synaptic properties of the feedback connections in the mouse thalamus between TRN and the dorsal lateral geniculate nucleus (dLGN), the principal relay of retinal signals to visual cortex. Using electron microscopy to identify TRN input to dLGN, we found that TRN terminals formed synapses with non-GABAergic postsynaptic profiles. Compared with other nonretinal terminals in dLGN, those from TRN were relatively large and tended to contact proximal regions of relay cell dendrites. To evoke TRN activity in dLGN, we adopted an optogenetic approach by expressing ChR2, or a variant (ChIEF) in TRN terminals. Both in vitro and in vivo recordings revealed that repetitive stimulation of TRN terminals led to a frequency-dependent inhibition of dLGN activity, with higher rates of stimulation resulting in increasing levels of membrane hyperpolarization and corresponding decreases in spike firing. This relationship suggests that alterations in TRN activity lead to graded changes in relay cell spike firing.NEW & NOTEWORTHY The thalamic reticular nucleus (TRN) modulates thalamocortical transmission through inhibition. In mouse, TRN terminals in the dorsal lateral geniculate nucleus (dLGN) form synapses with relay neurons but not interneurons. Stimulation of TRN terminals in dLGN leads to a frequency-dependent form of inhibition, with higher rates of stimulation leading to a greater suppression of spike firing. Thus, TRN inhibition appears more dynamic than previously recognized, having a graded rather than an all-or-none impact on thalamocortical transmission. SN - 1522-1598 UR - https://www.unboundmedicine.com/medline/citation/32609582/Synaptic_properties_of_the_feedback_connections_from_the_thalamic_reticular_nucleus_to_the_dorsal_lateral_geniculate_nucleus L2 - https://journals.physiology.org/doi/10.1152/jn.00757.2019?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -
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