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Featured ArticleArticles, Systems/Circuits

Pathways for Emotions: Specializations in the Amygdalar, Mediodorsal Thalamic, and Posterior Orbitofrontal Network

Clare Timbie and Helen Barbas
Journal of Neuroscience 26 August 2015, 35 (34) 11976-11987; DOI: https://doi.org/10.1523/JNEUROSCI.2157-15.2015
Clare Timbie
1Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, Massachusetts 02118, and
2Neural Systems Laboratory, Department of Health Sciences, Boston University, Boston, Massachusetts 02215
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Helen Barbas
1Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, Massachusetts 02118, and
2Neural Systems Laboratory, Department of Health Sciences, Boston University, Boston, Massachusetts 02215
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  • Figure 1.
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    Figure 1.

    Label of pathways with neural tracer injections in the amygdala, pOFC and the thalamic MD. A, Experimental design: injections of retrograde tracer in pOFC and anterograde tracer in the amygdala label overlapping zones in MD. B, Injection sites in pOFC shown on the orbital surface of a rhesus monkey brain. Scale bar, 5 mm. C–H, Coronal sections through pOFC show injection sites of neural tracer in fluorescence microscopy (C, F, G) or converted for bright-field microscopy (D, E, H). Scale bar in C is 1 mm and applies to C–H. I, Injection sites in the amygdala are shown schematically on a coronal section. Scale bar, 1 mm. J–L, Fresh tissue sections in the amygdala show injection sites of neural tracers (arrows). Scale bar in J is 1 mm and applies to J–L. M, Coronal section through the thalamic MD shows injection site of FR tracer mostly in MDmc. Scale bar, 1 mm.

  • Figure 2.
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    Figure 2.

    In MDmc, neurons projecting to pOFC overlapped with amygdalar axons. A–C, Neurons in MDmc projecting to pOFC (left), overlapped with patches of labeled amygdalar axons (middle), as seen in the merged images (right). Scale bar in A is 100 μm and applies to A–C. D, E, Laser scanning confocal microscopy showing close appositions (white arrowheads) between pOFC projection neurons (green) and amygdalar axons (red) in MDmc. Scale bar in D is 20 μm and applies to D and E.

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    Figure 3.

    Neurons in MD projecting to pOFC colocalized with CB or PV. A, Thalamic MD neuron projecting to pOFC (top, white arrowhead) is also positive for CB (middle), as seen in the merged images (bottom). B, Thalamic MD neuron projecting to pOFC (top, white arrowhead) is also positive for PV (middle), as seen in the merged images (bottom). Scale bar in A is 10 μm and applies to A and B. C, Thalamic neurons projecting to pOFC more frequently colocalized with CB than PV, in all cases analyzed. Vertical lines indicate SEM. D, Schematic depicting the termination pattern of calbindin thalamocortical neurons, which target robustly the upper cortical layers, and parvalbumin thalamocortical neurons, which terminate focally in the middle cortical layers.

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    Figure 4.

    Amygdalar axon terminals form synapses with CB and PV thalamocortical neurons in MD. A, Amygdalar axon terminal forming a synapse (white arrowheads) with a CB dendrite labeled with TMB (black asterisk),and also forming synapses with inhibitory dendrites (black arrowheads). B, Amygdalar axon terminal forming a synapse (white arrowheads) with a CB dendrite labeled with TMB (black asterisk). C, Amygdalar axon terminal forming a synapse (white arrowheads) with a PV dendrite labeled with gold (white asterisk). D, Amygdalar axons formed synapses more frequently with labeled CB dendrites in MD. E, The majority of amygdalar axons formed a synapse with at least one excitatory thalamic dendrite. Amy At, amygdalar axon terminal; CB den, calbindin dendrite; inhib den, inhibitory dendrite; PV den, parvalbumin dendrite.

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    Figure 5.

    Amygdalar neurons that project to MD and to pOFC are distinct. A, Amygdalar neuron is labeled with tracer injected in pOFC (left, blue, white arrowhead), but is not labeled with tracer from MD (right). Scale bar in A is 10 μm and applies to A–C. B, Amygdalar neuron is labeled with tracer injected in MD (right, red, white arrowhead), but is not labeled with tracer from pOFC (left). C, Neurons in the same field show that different neurons in the amygdala were labeled retrogradely with tracer from pOFC (left, bottom arrowhead) or from MD (right, top arrowhead); neither neuron is double-labeled. D–F, Representative coronal sections from fresh tissue through the amygdala (anterior → posterior) show spatial overlap of projection neurons directed to MD (red dots) or pOFC (blue dots). Scale bar in D is 1 mm and applies to D–F. G, Mean area of labeled amygdalar projection neurons directed to MD was significantly larger than for projection neurons directed to pOFC. Vertical lines indicate SEM.

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    Figure 6.

    Amygdalar axons in MDmc and pOFC express different glutamate transporters. A, B, Amygdalar axons (top, white arrowheads) in the upper layers of pOFC colocalized with VGLUT1 (middle), but not with VGLUT2 (middle, silhouette arrowheads), as seen in the merged images (bottom). Scale bar in A is 10 μm and applies to all panels. C, D, Amygdalar axons in MDmc (top, white arrowheads) colocalized with VGLUT2 (middle, white arrowheads), but not with VGLUT1 (middle, silhouette arrowheads), as seen in the merged images (bottom). E, Scatterplot depicts the proportion of amygdalar boutons in each case which colocalized with VGLUT1 or VGLUT2 in MDmc or pOFC. F, Overall proportion of amygdalar boutons that colocalized with VGLUT1 or VGLUT2 in MDmc or pOFC.

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    Figure 7.

    Amygdalar signals reach pOFC directly and indirectly through the thalamus. Bottom, Neurons from the amygdala that project to the thalamus are large and express VGLUT2 (dark blue), whereas amygdalar neurons that project to pOFC are comparatively smaller and express VGLUT1 (light blue). Left, Excitatory CB neurons (light green) and excitatory PV neurons (dark green) in MDmc project to pOFC at a ratio of 2:1. Direct amygdalar projections target most densely the upper layers, whereas indirect projections through the thalamus may target upper and middle layers through CB and PV thalamic neurons to enhance cortical signaling of affective content.

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    Table 1.

    Injection sites in pOFC, amygdala, and thalamus

    Case/hemisphereInjection site/divisionTracerSexAge (y)
    BC/rightA13FEM3
    BJ/rightpOFC/orbital pro-isocortexLYF2
    BK/rightpOFC/orbital pro-isocortexCBLF2.5
    BM/leftpOFC/orbital pro-isocortexFEF3.5
    BP/rightpOFC/orbital pro-isocortexFRF3.5
    BL/rightAmygdala/cortical, basomedialFRM3
    BM/leftAmygdala/basolateral, lateralFRF3.5
    BN/rightAmygdala/basomedial, basolateralFEM2
    BS/leftpOFC/orbital pro-isocortexFBF3.5
    BS/leftMediodorsal thalamus/magnocellular, parvicellularFRF3.5
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The Journal of Neuroscience: 35 (34)
Journal of Neuroscience
Vol. 35, Issue 34
26 Aug 2015
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Pathways for Emotions: Specializations in the Amygdalar, Mediodorsal Thalamic, and Posterior Orbitofrontal Network
Clare Timbie, Helen Barbas
Journal of Neuroscience 26 August 2015, 35 (34) 11976-11987; DOI: 10.1523/JNEUROSCI.2157-15.2015

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Pathways for Emotions: Specializations in the Amygdalar, Mediodorsal Thalamic, and Posterior Orbitofrontal Network
Clare Timbie, Helen Barbas
Journal of Neuroscience 26 August 2015, 35 (34) 11976-11987; DOI: 10.1523/JNEUROSCI.2157-15.2015
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Keywords

  • amygdala
  • emotion
  • orbitofrontal cortex
  • prefrontal cortex
  • primate
  • thalamus

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