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Organization and Somatotopy of Corticothalamic Projections from L5B in Mouse Barrel Cortex

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Organization and Somatotopy of Corticothalamic Projections from L5B in Mouse Barrel Cortex Organization and somatotopy of corticothalamic projections from L5B in mouse barrel cortex Anton Sumsera,b,c,d,1, Rebecca A. Measea,d, Bert Sakmanna,c,1, and Alexander Groha,d aInstitute for Neurosciences, Technische Universität München, 80802 Munich, Germany; bGraduate School of Systemic Neurosciences, Ludwig-Maximilians Universität München, 82152 Martinsried, Germany; cResearch Group Cortical Column in Silico, Max Planck Institute for Neurobiology, 82152 Martinsried, Germany; and dDepartment of Neurosurgery, Technische Universität München, 81675 Munich, Germany Contributed by Bert Sakmann, July 10, 2017 (sent for review March 21, 2017; reviewed by David Fitzpatrick, Michael Frotscher, and Jeff W. Lichtman) Neurons in cortical layer 5B (L5B) connect the cortex to numerous We labeled barrel cortical boutons by dual-color anterograde subcortical areas. Possibly the best-studied L5B cortico–subcortical tract tracing to reconstruct the 3D location of giant L5B boutons connection is that between L5B neurons in the rodent barrel cor- in the entire thalamus and the anterior midbrain. We found discrete tex (BC) and the posterior medial nucleus of the thalamus (POm). bouton clouds in four areas of the dorsal thalamus, one in the However, the spatial organization of L5B giant boutons in the POm ventral thalamus (zona incerta, ZI), and another in the anterior and other subcortical targets is not known, and therefore it is unclear pretectum (APT). L5B projections to each of these areas were if this descending pathway retains somatotopy, i.e., body map orga- somatotopically arranged, thereby mapping the whisker pad to nization, a hallmark of the ascending somatosensory pathway. We subcortical areas. The somatotopic precision, map orientation, and investigated the organization of the descending L5B pathway from numbers of boutons were target-area specific and revealed the the BC by dual-color anterograde labeling. We reconstructed and subdivision of the PO into four distinct L5B target nuclei. quantified the bouton clouds originating from adjacent L5B columns Results in the BC in three dimensions. L5B cells target six nuclei in the anterior – midbrain and thalamus, including the posterior thalamus, the zona Labeling of L5B Neurons and Boutons. We labeled cortico sub- cortical boutons by depositing two different adeno-associated virus incerta, and the anterior pretectum. The L5B subcortical innervation is A– target specific in terms of bouton numbers, density, and projection (AAV) constructs in the barrel cortex (BC) of seven mice (Fig. 1 C and Fig. S1). Transfected cells expressed the presynaptic marker volume. Common to all target nuclei investigated here is the mainte- C NEUROSCIENCE nance of projection topology from different barrel columns in the BC, Synaptophysin fused to either GFP or mOrange (Fig. 1 )(9). Deposits were targeted to L5 and labeled on average 91 [median; albeit with target-specific precision. We estimated low cortico–sub- first quartile (Q ): 50; third quartile (Q ): 141] L5B neurons in 3 cortical convergence and divergence, demonstrating that the L5B cor- 1 3 (Q1:2;Q3: 4) barrel columns. Dual virus deposits were always ticothalamic pathway is sparse and highly parallelized. Finally, the nonoverlapping, with their borders being 260 μm apart (Q :221μm; spatial organization of boutons and whisker map organization 1 Q3:355μm; equivalent to approximately two barrel diameters). In revealed the subdivision of the posterior group of the thalamus into mice, the interbarrel septa are much less prominent than in rats four subnuclei (anterior, lateral, medial, and posterior). In conclusion, (10). Viral deposits included barrel and septal regions (Fig. S1), so – corticofugal L5B neurons establish a widespread cortico subcortical putative barrel- or septal-specific projection patterns (11) could not network via sparse and somatotopically organized parallel pathways. be distinguished. Following fluorophore expression, we acquired images of the entire thalamus and adjacent midbrain regions via somatotopy | corticothalamic projections | whisker system | mosaic confocal fluorescence microscopy (Figs. 1 D and E and 2 A– posterior medial thalamic nucleus | thalamus D and Fig. S2). These images were used to reconstruct the position of giant synaptic boutons (Fig. 2 E and F). Only boutons with ap- common feature of sensory systems is the topographic or- parent diameters >1.5 μm were defined as giant boutons originating Aganization of their ascending pathways from the sensors to the cortex. A prominent example of topographic projections is the Significance rodent whisker system in which the arrangement of whisker follicles on the snout of the animal is mapped at each synaptic station up to In the somatosensory system, signals are transduced from pe- the cortex, where the whisker map forms the cortical barrel field of ripheral sensors up to the cerebral cortex in a topographic rodents (1). Although this strict topographic organization is well manner, meaning that the relative spatial organization of the established for the ascending pathway (2), the extent to which this sensory receptors is represented by a map in the cortex. Be- map organization continues beyond the primary somatosensory cor- cause the somatosensory cortex is not the terminus of sensory tex via descending projections to subcortical structures is less clear. signals, we investigated whether topographic maps are main- One major target of descending cortico-efferent projections is the tained beyond the cortex via cortical output pathways from thalamus, which is innervated by two distinct corticothalamic thick-tufted layer 5B (L5B) neurons. We found that L5B neurons pathways. First, neurons in cortical layer 6 (L6) provide numerically in the somatosensory cortex topographically target six sepa- large and somatotopically organized (3) feedback to the sensory rate subcortical nuclei with area-specific projection strength, thalamus. Secondly, layer 5B thick-tufted neurons (L5B) innervate map orientation, and topographic precision. Thus topographic exclusively higher-order thalamus with sparse but uniquely large organization persists beyond the primary cortex via the L5B – driver synapses and unclear somatotopic organization (3 5). pathway with target-specific precision. Probably the best-characterized example of a L5B target nucleus is the lateral part of the posterior group (PO) in the thalamus Author contributions: A.S., B.S., and A.G. designed research; A.S. performed research; A.S. (POm), where cortical L5B neurons provide the dominant synaptic and R.A.M. analyzed data; and A.S., R.A.M., B.S., and A.G. wrote the paper. input (6, 7). Receptive field studies support somatotopic organiza- Reviewers: D.F., Max Planck Florida Institute; M.F., University of Hamburg; and J.W.L., tion of the POm even though an anatomical whisker map has not Harvard University. been shown (8). L5B neurons also project to the ventral thalamus, The authors declare no conflict of interest. midbrain, and brainstem (4, 5), but the organization of their pro- 1To whom correspondence may be addressed. Email: [email protected] jection fields is unknown. Here we investigated by quantitative or [email protected]. – anatomy whether cortico subcortical projections to the thalamus This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. and anterior midbrain are somatotopically organized. 1073/pnas.1704302114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1704302114 PNAS Early Edition | 1of6 Downloaded by guest on September 30, 2021 Bouton Cloud Quantifications. We quantified bouton sizes and A SP-GFP SP- B C E3 E4 E5 mOrange E2 E6 E7 numbers, as well as volumes and densities of bouton clouds, in six E8 E1 D3 target nuclei in the thalamus (four of which were within the PO) BC D2 D4D5 δ D6D7 μ D1 and anterior midbrain. L5B bouton median diameters were 2.6 m C3 C4 POm γ C2 C5C6 when labeled with GFP and 2.9 μm when labeled with mOrange (no C1 VPM B3 B4 deconvolution was applied). Bouton diameters in the different β B2 B1 target areas were comparable, and medians ranged between 2.3 and A3 A4 α A2 2.9 μm with GFP labeling and between 2.6 and 3.2 μmwithmOr- A1 ange labeling (Fig. 4A and see Table 1 for quartiles). anterior Str anterior Str We next estimated the average number of boutons supplied per D E labeled L5B neuron by normalizing bouton counts in the different POa POa Rt nuclei by the number of fluorescently labeled somata in L5B for POm POm POm POm Rt each experiment. Because not all neurons in L5B are projection med- lat- VPM med- lat- VPM ial eral neurons, the reported numbers of boutons are lower-bound esti- midline eral midline ial mates. The median number of giant boutons supplied by single PoT PoT labeled L5B neurons was highly variable across target areas and HC ranged between 5.8 and 29.5. According to these estimates, a single HC APT labeled L5B neuron supplies most boutons to the POmlateral and APT APT (median >24 boutons), whereas the ZI receives ≈18 boutons, and the POa, POmmedial, and PoT receive fewer than 10 giant B Fig. 1. Cortical bouton labeling and borders of subcortical target nuclei. boutons (see Fig. 4 and Table 1 for details). Normalizing bouton Subcortical L5B boutons in the thalamus were labeled by virus-mediated numbers by the ratio of the labeled column volume to the average expression of two different fluorescent proteins in barrel cortical neurons. column volume, we estimate that one column supplies ≈1,000 giant (A) Schematic showing dual injection of viral particles encoding Synapto- boutons to the POmlateral and APT and between 220 and 480 giant physin–GFP (SP–GFP, green) and Synaptophysin–mOrange (SP–mOrange, ma- boutons to the other target nuclei (Table 1 and Fig. S4). genta) into the BC and projections in the thalamus (modified from ref. 12). When approximating bouton cloud volumes per labeled L5B (B) Merged confocal fluorescence image of tangential sections of the BC at the neuron in the respective nuclei, PO subnuclei (excluding the PoT) level of layer 4, showing barrels (gray; Streptavidin staining) and deposits of SP– had the smallest cloud volumes, with fewer than 1.1e4 mm3 per GFP (green) and SP–mOrange (magenta).
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