Where Do Core Thalamocortical Axons Terminate in Mammalian Neocortex When There Is No Cytoarchitecturally Distinct Layer 4?

ABSTRACT Although the mammalian cerebral cortex is most often described as a hexalaminar structure, there are cortical areas (primary motor cortex) and species (elephants, cetaceans, and hippopotami), where a cytoarchitecturally indistinct, or absent, layer 4 is noted. Thalamocortical projections fr...

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Bibliographic Details
Published in:Journal of comparative neurology (1911) 2024-07, Vol.532 (7), p.e25652-n/a
Main Authors: Bhagwandin, Adhil, Molnár, Zoltán, Bertelsen, Mads F., Karlsson, Karl Æ., Alagaili, Abdulaziz N., Bennett, Nigel C., Hof, Patrick R., Kaswera‐Kyamakya, Consolate, Gilissen, Emmanuel, Jayakumar, Jaikishan, Manger, Paul R.
Format: Article
Language:English
Subjects:
Axons
Cerebral cortex
Cortex (motor)
cortical evolution
cortical layer IV
cortical layers
cortical processing
Glutamic acid transporter
Neocortex
Presynapse
RRID‐AB_10000321
RRID‐AB_10000340
RRID‐AB_10000343
RRID‐AB_2187552
RRID‐AB_509997
Sensorimotor integration
skin–brain axis
Thalamus
Visual cortex
Visual pathways
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Summary:ABSTRACT Although the mammalian cerebral cortex is most often described as a hexalaminar structure, there are cortical areas (primary motor cortex) and species (elephants, cetaceans, and hippopotami), where a cytoarchitecturally indistinct, or absent, layer 4 is noted. Thalamocortical projections from the core, or first order, thalamic system terminate primarily in layers 4/inner 3. We explored the termination sites of core thalamocortical projections in cortical areas and in species where there is no cytoarchitecturally distinct layer 4 using the immunolocalization of vesicular glutamate transporter 2, a known marker of core thalamocortical axon terminals, in 31 mammal species spanning the eutherian radiation. Several variations from the canonical cortical column outline of layer 4 and core thalamocortical inputs were noted. In shrews/microchiropterans, layer 4 was present, but many core thalamocortical projections terminated in layer 1 in addition to layers 4 and inner 3. In primate primary visual cortex, the sublaminated layer 4 was associated with a specialized core thalamocortical projection pattern. In primate primary motor cortex, no cytoarchitecturally distinct layer 4 was evident and the core thalamocortical projections terminated throughout layer 3. In the African elephant, cetaceans, and river hippopotamus, no cytoarchitecturally distinct layer 4 was observed and core thalamocortical projections terminated primarily in inner layer 3 and less densely in outer layer 3. These findings are contextualized in terms of cortical processing, perception, and the evolutionary trajectory leading to an indistinct or absent cortical layer 4. Immunohistochemical staining for vesicular glutamate transporter 2 reveals the “core” thalamocortical projection to the neocortex in the African elephant. In the elephant and other mammals with unusual skin (such as pachydermatous skin), layer 4 is cytoarchitecturally indistinct, possibly absent, and the thalamocortical input terminates primarily on the neurons forming the inner sublamina of layer 3. Scale bar = 1 mm.
ISSN:0021-9967
1096-9861
1096-9861
DOI:10.1002/cne.25652