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Research ArticleNew Research, Cognition and Behavior

Combinatorial Inputs to the Ventral Striatum from the Temporal Cortex, Frontal Cortex, and Amygdala: Implications for Segmenting the Striatum

Eun Young Choi, Song-Lin Ding and Suzanne N. Haber
eNeuro 11 December 2017, 4 (6) ENEURO.0392-17.2017; https://doi.org/10.1523/ENEURO.0392-17.2017
Eun Young Choi
1Department of Pharmacology and Physiology, University of Rochester Medical Center, Rochester, NY 14642
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Song-Lin Ding
2Allen Institute for Brain Science, Seattle, WA 98109
3Institute of Neuroscience, School of Basic Medical Sciences, Guangzhou Medical University, Guangzhou, Guangdong Province 511436, P. R. China
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Suzanne N. Haber
1Department of Pharmacology and Physiology, University of Rochester Medical Center, Rochester, NY 14642
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  • Figure 1.
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    Figure 1.

    Ventral striatum. The boundary between the VSd and VSv and the ventral border of the VSv were based on AChE (A, B) and CB (C) staining identifying the shell of the NAc and olfactory tubercle. D, The dorsal border of the VSd was based on corticostriatal projection zones from emotion-processing prefrontal cortical regions (vmPFC, ACC, OFC). E, Schematic of VSd and VSv boundaries (dashed lines) and six striatal retrograde injection sites. OT, olfactory tubercle; IC, internal capsule; Ca, caudate; Pu, putamen.

  • Figure 2.
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    Figure 2.

    Temporal pole, adjacent areas, and medial temporal cortex. Coronal slices of areas and structures within TP+ stained with WFA (A) or NeuN (B). C, D, Sagittal slices of TP+ stained with PV. Slice locations for A–D shown in inset of A. Coronal slices of the anterior MTC (E) and posterior MTC (F) stained with NeuN. G, Orbital view of temporal lobe showing schematic of 11 anterograde injections placed in TP+ (area TG, TEr) and MTC (EC, 36, TH, TL/TF, TF). Lines indicate slice locations for E, F. Short black lines in A–F and dashed lines in G indicate areal boundaries. Am, amygdala; CA, cornu ammonis; Hip, hippocampus; LI, limen insula; PaS, parasubiculum; ProS, prosubiculum; S, subiculum; acf, anterior calcarine fissure; amts, anterior middle temporal sulcus; ots, occipital temporal sulcus; rs, rhinal sulcus; sts, superior temporal sulcus.

  • Figure 3.
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    Figure 3.

    Temporal inputs to the striatum: anterograde labeling. Anterograde tracer injections in the TP (A), TEr in the rostral inferior temporal cortex (B), and the anterior (C, D) and posterior (E, G) MTC show three broad patterns (red, green, cyan) of dense terminal projections in the striatum. Note the split in projections from MTC to the dorsal and ventral striatum.

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    Figure 4.

    MTC projections to the striatum. 3D model of aggregate striatal projections (cyan) from anterograde injections in the anterior and posterior MTC (EC, areas 36, TH, TL/TF, and TF). Note the split in projections to the dorsal and ventral striatum and their convergence in the rostral pole of the caudate.

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    Figure 5.

    Temporal inputs to the striatum: retrograde labeling. Coronal sections of TP+ and MTC from four tracer injections in the VS (A–D) and two injections in the dorsal caudate (E, F). All parts of the VS receive strong projections from the TP and MTC. Rostral inferior temporal cortex (area TEr) sends projections primarily to the VSv and central and lateral VSd.

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    Figure 6.

    Overlap of temporal, frontal, and amygdala projections in the striatum. Outlines (black) of dense projections from TP+ and MTC are overlaid on schematic composites of dense projections (filled) from various frontal regions. Temporal injection sites shown above. Ca, caudate; Pu, putamen; NAc, nucleus accumbens.

  • Figure 7.
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    Figure 7.

    Frontal and amygdala inputs to the striatum: retrograde labeling. A–D, Four retrograde tracer injections in VS. E, One injection in the rostral dorsal caudate. Coronal sections of the frontal cortex (i, ii) and amygdala (iii). AB, accessory basal nucleus; B, basal nucleus; L, lateral nucleus. Aiii, Ciii, and Diii are reprinted with minor stylistic edits from Fudge et al. (2002) with permission from Elsevier, Inc.

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    Figure 8.

    Relative contributions (percentage) of TP+, MTC, and frontal cortical inputs to the striatum. Thick black lines separate temporal and frontal cortical areas. See Table 2 for percentage values. Same cases as in Fig. 7.

Tables

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    Table 1.

    Injection cases

    CaseSpeciesTracer (direction analyzed)Injection site
    IM143Macaca fascicularisBDA (anterograde)Temporal pole: area TG
    IM145Macaca fascicularisBDA (anterograde)Temporal pole: area TG
    IM147Macaca fascicularisBDA (anterograde)Temporal pole: area TG
    IM146Macaca fascicularisBDA (anterograde)Temporal pole+: area TEr
    MF139Macaca fascicularis[3H]AA (anterograde)Anterior MTC: entorhinal cortex
    MMEMacaca mulatta[3H]AA (anterograde)Anterior MTC: entorhinal cortex
    MNNMacaca mulatta[3H]AA (anterograde)Anterior MTC: area 36
    MPWMacaca mulatta[3H]AA (anterograde)Anterior MTC: area 36
    MPPMacaca mulatta[3H]AA (anterograde)Posterior MTC: area TH
    MPJMacaca mulatta[3H]AA (anterograde)Posterior MTC: area TL/TF
    MOEMacaca mulatta[3H]AA (anterograde)Posterior MTC: area TF
    MF205Macaca fascicularisFS (anterograde)Basolateral amygdala
    MR28Macaca mulattaWGA (retrograde)VSv (nucleus accumbens)
    MN33Macaca nemestrinaWGA (retrograde)Medial VSd
    MN38Macaca nemestrinaLY (retrograde)Central VSd
    MN40Macaca nemestrinaLY (retrograde)Lateral VSd
    MF170Macaca fascicularisFS (retrograde)Medial dorsal caudate
    MF184Macaca fascicularisWGA (retrograde)Medial dorsal caudate
    • View popup
    Table 2.

    Relative contributions (percentage) of TP+, MTC, and frontal cortical inputs to the striatum

    Region and areaVSvMedial VSdCentral VSdLateral VSdD Caud
    vmPFC
        14010.664.551.260.20
        253.9116.215.191.920.04
    ACC
        2412.0523.128.1719.008.82
        32016.310.605.500.65
    OFC
        11, 1302.4816.411.531.41
        OPAI4.7305.6600.07
        OPro2.040000
    Frontal pole
        1000.120.123.061.92
    dlPFC
        900.201.914.4815.77
        46001.001.2914.55
        9/46000.482.2211.62
        8001.145.7020.53
    vlPFC
        4700.0317.277.441.90
        44, 45001.941.429.45
        ProM001.682.100.37
    Premotor
        6004.012.866.91
    Temporal pole
        TG22.4116.6821.3415.990
        TI5.653.922.081.680
        PI00.380.330.080
        TAr03.790.581.280
        TApr0.020.241.874.700
        TEr2.110.010.832.210
    Anterior PHC
        EC23.101.061.041.930
        356.271.120.723.970
        368.890.871.004.020
    Posterior PHC
        TH01.8401.020
        TL5.040.4102.610.06
        TF2.22000.620.35
        THO00000.19
        TLO00000.85
        TFO00000.24
    • The relative contribution of inputs from each area was calculated as the percentage of counted cells within that area versus the total number of counted cells from all frontal and temporal cortical areas examined within the same case. Same cases as in Fig. 7.

    • View popup
    Table 3.

    Pairwise linear correlations and p-values of the distributions of frontal and temporal inputs for pairs of striatal regions

    Injection site 1Injection site 2rp (two-tailed)
    VsvMedial VSd0.410.02
    VsvCentral VSd0.360.05
    VsvLateral VSd0.532.1 × 10−3
    VsvDorsal caudate–0.190.30
    Medial VSdCentral VSd0.410.02
    Medial VSdLateral VSd0.692.0 × 10−5
    Medial VSdDorsal caudate–0.080.67
    Central VSdLateral VSd0.585.7 × 10−4
    Central VSdDorsal caudate–0.060.73
    Lateral VSdDorsal caudate0.210.26
    • Pairwise linear correlations were calculated between the distributions of input percentages from 31 frontal and temporal areas examined (see Table 2) for pairs of striatal regions. Two-tailed p-values were obtained with Fisher’s r-to-t transformation and Student’s t-distribution. Degrees of freedom = 29. Same cases as in Fig. 7.

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Combinatorial Inputs to the Ventral Striatum from the Temporal Cortex, Frontal Cortex, and Amygdala: Implications for Segmenting the Striatum
Eun Young Choi, Song-Lin Ding, Suzanne N. Haber
eNeuro 11 December 2017, 4 (6) ENEURO.0392-17.2017; DOI: 10.1523/ENEURO.0392-17.2017

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Combinatorial Inputs to the Ventral Striatum from the Temporal Cortex, Frontal Cortex, and Amygdala: Implications for Segmenting the Striatum
Eun Young Choi, Song-Lin Ding, Suzanne N. Haber
eNeuro 11 December 2017, 4 (6) ENEURO.0392-17.2017; DOI: 10.1523/ENEURO.0392-17.2017
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Keywords

  • anatomic connections
  • basal ganglia
  • circuit integration
  • corticostriatal circuitry

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