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Research ArticleResearch Article: New Research, Sensory and Motor Systems

Functionally Distinct Circuits Are Linked by Heterocellular Electrical Synapses in the Thalamic Reticular Nucleus

Mitchell J. Vaughn, Zachary Laswick, Huaixing Wang and Julie S. Haas
eNeuro 21 December 2023, 11 (1) ENEURO.0269-23.2023; https://doi.org/10.1523/ENEURO.0269-23.2023
Mitchell J. Vaughn
Department of Biological Sciences, Lehigh University, Bethlehem 18015, Pennsylvania
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Zachary Laswick
Department of Biological Sciences, Lehigh University, Bethlehem 18015, Pennsylvania
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Huaixing Wang
Department of Biological Sciences, Lehigh University, Bethlehem 18015, Pennsylvania
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Julie S. Haas
Department of Biological Sciences, Lehigh University, Bethlehem 18015, Pennsylvania
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  • For correspondence: juliehaas{at}lehigh.edu
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  • Figure 1.
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    Figure 1.

    Example spatial distributions and spiking responses of SOM and CB neurons in the TRN. A, Fluorescence images of a live slice from a SOM × Ai6 mouse. SOM-GFP expression, pseudocolored in magenta here, occupies the shell of the TRN. Boundaries were drawn from corresponding IR image. B, Example responses of SOM neuron to current steps of −100 pA and rheobase for each cell. From bottom to top, Vm = −74.5, −74.0, −77.0 mV. Scale bars, 20 mV, 50 ms. C, CB-GFP expression in the TRN. D, Example responses of CB neuron to current steps of −100 pA and rheobase for each cell. From bottom to top, Vm = −74.9, −72.7, −77.3 mV. Scale bars, 20 mV, 50 ms. See Extended Data Figure 1-1 for an example of a recording at the boundary between the core and shell of the TRN.

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    Figure 2.

    Intrinsic and bursting properties distinguish GFP + SOM and CB subtypes in the TRN. A, Rin for CB (mean, 124.6 ± 4.7 MΩ) and SOM (222.3 ± 7.7 MΩ; p < 0.01; n = 107 CB and 154 SOM) neurons. B, Peak instantaneous firing rate within bursts for SOM (mean, 184.4 ± 7.5 Hz) and CB (312.5 ± 10.6 Hz; p < 0.01) neurons. C, Gain of tonic spiking frequency for SOM and CB neurons (SOM, 0.37 ± 0.03 Hz/pA; CB, 0.30 ± 0.02 Hz/pA; p = 0.5). D, CB neurons fired more spikes for each burst (SOM, 4.8 ± 0.3 spikes; CB, 7.0 ± 0.3 spikes; p < 0.01). E, Spiking within a burst accelerated (expressed as the ratio of fastest to first instantaneous rate within the burst) for CB neurons more than for SOM neurons (SOM: median, 1.0, mean, 1.1 ± 0.03; CB: median, 1.13, mean, 1.20 ± 0.02; p < 0.01). F, Instantaneous firing for each interspike interval (ISI) within bursts, normalized to the first interval. Data are mean ± SEM. G, Cell identity as a function of peak burst rate, input resistance, and acceleration ratio. See Extended Data Figure 2-1 for input resistance across age.

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    Figure 3.

    Homocellular and heterocellular coupling between pairs of TRN neurons. A, Example of coupling between two pairs of SOM neurons. Top, Overlay of fluorescence and DIC images taken during live recordings. Scale bar, 20 µm. Middle, Simultaneous voltage responses of both neurons to −100 pA current steps delivered to one neuron of each pair. Scale bars, 5 mV, 50 ms. Bottom, Spiking responses of each neuron to separate injections of rheobase current. Scale bars, 20 ms, 20 mV. B, As for A, but for pairs of SOM and non-SOM neurons; scale bars in top right are 2.5 mV, 50 ms. C, As for A, but for pairs of CB neurons. D, As for A, but for pairs of CB and non-CB neurons.

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    Figure 4.

    Distribution of coupling within and without SOM and CB cell types. A, Stacked distribution of homocellular electrical synapses in the TRN; coupling was found between 9 out of 44 pairs of CB neurons tested and 30 out of 60 pairs of SOM neurons tested. cc, coupling coefficient. B, Stacked distribution of heterocellular electrical coupling between TRN neurons: synapses were identified between 8 out of 19 pairs of CB and non-CB neurons and 23 out of 34 pairs of SOM and non-SOM neurons tested. C, Schematic of distinct thalamocortical pathways linked by electrical synapses of the TRN. FO, first order; HO, higher order. See Extended Data Figure 4-1 for signal-to-noise of coupling measurements.

Extended Data

  • Figures
  • Figure 1-1

    A. Example of within-TRN location of boundaries between expressing and non-expressing areas targeted for paired recordings Left: IR image. Right: GFP image. B. Pair targeted in ATRN. FO, first order; HO, higher order. Download Figure 1-1, TIF file.

  • Figure 2-1

    Input resistance (mean ± SEM) over postnatal age for the dataset used. Fits (dotted lines) are linear. Download Figure 2-1, TIF file.

  • Figure 4-1

    Signal-to-noise of coupling measurements. SNR is change in membrane voltage in the receiving neuron during repeated current steps (see Methods) divided by the standard deviation of voltage. Heterotypic pairs are blue, homotypic pairs are in red; circles represent SOM data, and squares represent CB data. Line at cc = 0.01 represents threshold used to identify electrical coupling. Download Figure 4-1, TIF file.

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Functionally Distinct Circuits Are Linked by Heterocellular Electrical Synapses in the Thalamic Reticular Nucleus
Mitchell J. Vaughn, Zachary Laswick, Huaixing Wang, Julie S. Haas
eNeuro 21 December 2023, 11 (1) ENEURO.0269-23.2023; DOI: 10.1523/ENEURO.0269-23.2023

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Functionally Distinct Circuits Are Linked by Heterocellular Electrical Synapses in the Thalamic Reticular Nucleus
Mitchell J. Vaughn, Zachary Laswick, Huaixing Wang, Julie S. Haas
eNeuro 21 December 2023, 11 (1) ENEURO.0269-23.2023; DOI: 10.1523/ENEURO.0269-23.2023
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Keywords

  • electrical synapse
  • gap junction
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