Rodent Area Prostriata Converges Multimodal Hierarchical Inputs and Projects to the Structures Important for Visuomotor Behaviors

Abstract

Area prostriata is a limbic structure critical to fast processing of moving stimuli in far peripheral visual field. Neural substrates underlying this function remain to be discovered. Using both retrograde and anterograde tracing methods, the present study reveals that the prostriata in rat and mouse receives inputs from multimodal hierarchical cortical areas such as primary, secondary, and association visual and auditory cortices and subcortical regions such as the anterior and midline thalamic nuclei and claustrum. Surprisingly, the prostriata also receives strong afferents directly from the rostral part of the dorsal lateral geniculate nucleus. This shortcut pathway probably serves as one of the shortest circuits for fast processing of the peripheral vision and unconscious blindsight since it bypasses the primary visual cortex. The outputs of the prostriata mainly target the presubiculum (including postsubiculum), pulvinar, ventral lateral geniculate nucleus, lateral dorsal thalamic nucleus, and zona incerta as well as the pontine and pretectal nuclei, most of which are heavily involved in subcortical visuomotor functions. Taken together, these results suggest that the prostriata is poised to quickly receive and analyze peripheral visual and other related information and timely initiates and modulates adaptive visuomotor behaviors, particularly in response to unexpected quickly looming threats.

Chemoarchitecture of area prostriata in adult and developing mice: Comparison with presubiculum and parasubiculum

“…These include specific expression in layers 2-3 or layer 5 or both (Table 1), indicating the existence of different cell types in the prostriata. These findings are consistent with our recent connectional studies of the prostriata in the rat and mouse brains (Chen et al, 2020(Chen et al, , 2021Hu et al, 2020). For example, layers 2-3 of the prostriata project mainly to contralateral layers 2-3 (Chen et al, 2020) and ipsilateral PrS/PoS (Chen et al, 2021), while layer 5 projects mainly to the lateral dorsal thalamic nucleus (LD), ventral lateral geniculate nucleus (VLG), lateral-posterior thalamic F I G U R E 1 0 Identification of two subdivisions of the prostriata (Pro) in sequential sagittal sections.…”

“…These findings are consistent with our recent connectional studies of the prostriata in the rat and mouse brains (Chen et al, 2020(Chen et al, , 2021Hu et al, 2020). For example, layers 2-3 of the prostriata project mainly to contralateral layers 2-3 (Chen et al, 2020) and ipsilateral PrS/PoS (Chen et al, 2021), while layer 5 projects mainly to the lateral dorsal thalamic nucleus (LD), ventral lateral geniculate nucleus (VLG), lateral-posterior thalamic F I G U R E 1 0 Identification of two subdivisions of the prostriata (Pro) in sequential sagittal sections. Lateral (top) to medial (bottom) sections are arranged along each column and the interval between each section/level in each column is 160 µm.…”

“…(the protein coded by Calb1) are strongly expressed in the prostriata, as reported in our previous studies (Chen et al, 2021;Lu et al, 2020).…”

“…These findings strongly suggest that the triangular region (or area 29e) in rodents is the equivalent of or part of the prostriata in human and nonhuman primate brains. Our recent studies on this triangular region of the rat and mouse brains have discovered that the triangular region belongs to the superficial layers (layers 2-3) of the prostriata rather than the RS or PrSd/PoS (Chen et al, 2020(Chen et al, , 2021Hu et al, 2020;Lu et al, 2020). These studies have further revealed that rodent prostri-Abbreviations: 2900026a02rik, RIKEN cDNA 2900026A02 gene; 6430573f11rik, RIKEN cDNA 6430573F11 gene; Adra1d, adrenergic receptor, alpha 1d; Adra2a, adrenergic receptor, alpha 2a; Adra2c, adrenergic receptor, alpha 2c; Adrbk2, adrenergic receptor kinase, beta 2; Arc, activity regulated cytoskeletal-associated protein; Bcl6, B cell leukemia/lymphoma 6; C1ql2, complement component 1, q subcomponent-like 2; Cacna1g, calcium channel, voltage-dependent, T type, alpha 1G subunit; Car4, carbonic anhydrase 4; Cdc42ep3, CDC42 effector protein (Rho GTPase binding) 3; Cdh24, cadherin 24; Cdh8, cadherin 8; Chn2, chimerin 2; Chrm3, cholinergic receptor, muscarinic 3, cardiac; Chrna4, cholinergic receptor, nicotinic, alpha polypeptide 4; Chrna5, cholinergic receptor, nicotinic, alpha polypeptide 5; Chrna7, cholinergic receptor, nicotinic, alpha polypeptide 7; Chst8, carbohydrate (N-acetylgalactosamine 4-0) sulfotransferase 8; Cntn4, contactin 4; Col12a1, collagen, type XII, alpha 1; Col23a1, collagen, type XXIII, alpha 1; Col25a1, collagen, type XXV, alpha 1; Col5a1, collagen, type V, alpha 1; Col6a1, collagen, type VI, alpha 1; Coro6, coronin 6; Cpne7, copine VII; Crym, crystallin, mu; Cux2, cut-like homeobox 2; Cxcl14, chemokine (C-X-C motif) ligand 14; Ddit4l, DNA-damage-inducible transcript 4-like; Deptor, DEP domain containing MTOR-interacting protein; Dgkb, diacylglycerol kinase, beta; Drd1, dopamine receptor D1; Drd2, dopamine receptor D2; Drd5, dopamine receptor D5; Efnb3, ephrin B3; Etv1, ets variant 1; Fat3, FAT tumor suppressor homolog 3 (Drosophila); Fezf2, Fez family zinc finger 2; Flrt2, fibronectin leucine rich transmembrane protein 2; Fn1, fibronectin 1; Foxp2, forkhead box P2; Fstl1, follistatin-like 1; Gabrb3, gamma-aminobutyric acid (GABA) A receptor, subunit beta 3; Gda, guanine deaminase; Gpr123, G protein-coupled receptor 123; Gpr161, G protein-coupled receptor 161; Gpr88, G-protein coupled receptor 88; Gria3, glutamate receptor, ionotropic, AMPA3 (alpha 3); Grp, gastrin releasing peptide; Homer2, homer homolog 2 (Drosophila); Htr1a, 5-hydroxytryptamine (serotonin) receptor 1A; Htr1b, 5-hydroxytryptamine (serotonin) receptor 1B; Htr1f, 5-hydroxytryptamine (serotonin) receptor 1F; Icam5, intercellular adhesion molecule 5, telencephalin; Id2, inhibitor of DNA binding 2; Ier5, immediate early response 5; Igfbp5, insulin-like growth factor binding protein 5; Igsf3, immunoglobulin superfamily, member 3; Inpp4b, inositol polyphosphate-4-phosphatase, type II; Kcnn2, potassium intermediate/small conductance calcium-activated channel, subfamily N, member 2; Kitl, kit ligand; Lamp5, lysosomal-associated membrane protein family, member 5; Lifr, leukemia inhibitory factor receptor; Limch1, LIM and calponin homology domains 1; Loc433228, gene Loc433228; Loc434300, gene Loc434300; Lxn, latexin; Lypd1, Ly6/PLAUR domain-containing 1; Mal2, mal, T cell differentiation protein 2; Neurod6, neurogenic differentiation 6; Nnat, neuronatin; Nos1ap, nitric oxide synthase 1 (neuronal) adaptor protein; Nr2f1, nuclear receptor subfamily 2, group F, member 1; Nr4a2, nuclear receptor subfamily 4, group A, member 2; Ntng1, netrin G1; Nts, neurotensin; Ntsr1, neurotensin receptor 1; Ociad2, OCIA domain containing 2; Otof, otoferlin; Pal...…”

Retinotopic organization of feedback projections in primate early visual cortex: implications for active vision

“…Tracer studies reveal connections with the peripheral representation of the early visual cortex in macaque (Sousa et al, 1991) and rodent (Lu et al, 2020). In rodents and perhaps in humans, prostriata receives a direct input from the dorsal lateral geniculate (Chen et al, 2021; Kurzawski et al, 2020). In addition to the projection from prostriata we found a considerably weaker projection from the retrosplenial area 23, which has also been proposed to constitute a primate visual motion area (Smith, 2021).…”