Thalamocortical Afferents Innervate the Cortical Subplate much Earlier in Development in Primate than in Rodent

Ayman Alzu'bi, Jihane Homman-Ludiye, James A. Bourne, Gavin J. Clowry

Research output: Contribution to journalArticleResearchpeer-review

2 Citations (Scopus)

Abstract

The current model, based on rodent data, proposes that thalamocortical afferents (TCA) innervate the subplate towards the end of cortical neurogenesis. This implies that the laminar identity of cortical neurons is specified by intrinsic instructions rather than information of thalamic origin. In order to determine whether this mechanism is conserved in the primates, we examined the growth of thalamocortical (TCA) and corticofugal afferents in early human and monkey fetal development. In the human, TCA, identified by secretagogin, calbindin, and ROBO1 immunoreactivity, were observed in the internal capsule of the ventral telencephalon as early as 7-7.5 PCW, crossing the pallial/subpallial boundary (PSB) by 8 PCW before the calretinin immunoreactive corticofugal fibers do. Furthermore, TCA were observed to be passing through the intermediate zone and innervating the presubplate of the dorsolateral cortex, and already by 10-12 PCW TCAs were occupying much of the cortex. Observations at equivalent stages in the marmoset confirmed that this pattern is conserved across primates. Therefore, our results demonstrate that in primates, TCAs innervate the cortical presubplate at earlier stages than previously demonstrated by acetylcholinesterase histochemistry, suggesting that pioneer thalamic afferents may contribute to early cortical circuitry that can participate in defining cortical neuron phenotypes.

Original languageEnglish
Pages (from-to)1706-1718
Number of pages13
JournalCerebral Cortex
Volume29
Issue number4
DOIs
Publication statusPublished - 1 Apr 2019

Keywords

  • corticothalamic afferents
  • human cortical development
  • subplate
  • thalamocortical afferents
  • thalamus

Cite this

@article{ac0d8c1c3d6a4fc3a31fdbb78b68b2f0,
title = "Thalamocortical Afferents Innervate the Cortical Subplate much Earlier in Development in Primate than in Rodent",
abstract = "The current model, based on rodent data, proposes that thalamocortical afferents (TCA) innervate the subplate towards the end of cortical neurogenesis. This implies that the laminar identity of cortical neurons is specified by intrinsic instructions rather than information of thalamic origin. In order to determine whether this mechanism is conserved in the primates, we examined the growth of thalamocortical (TCA) and corticofugal afferents in early human and monkey fetal development. In the human, TCA, identified by secretagogin, calbindin, and ROBO1 immunoreactivity, were observed in the internal capsule of the ventral telencephalon as early as 7-7.5 PCW, crossing the pallial/subpallial boundary (PSB) by 8 PCW before the calretinin immunoreactive corticofugal fibers do. Furthermore, TCA were observed to be passing through the intermediate zone and innervating the presubplate of the dorsolateral cortex, and already by 10-12 PCW TCAs were occupying much of the cortex. Observations at equivalent stages in the marmoset confirmed that this pattern is conserved across primates. Therefore, our results demonstrate that in primates, TCAs innervate the cortical presubplate at earlier stages than previously demonstrated by acetylcholinesterase histochemistry, suggesting that pioneer thalamic afferents may contribute to early cortical circuitry that can participate in defining cortical neuron phenotypes.",
keywords = "corticothalamic afferents, human cortical development, subplate, thalamocortical afferents, thalamus",
author = "Ayman Alzu'bi and Jihane Homman-Ludiye and Bourne, {James A.} and Clowry, {Gavin J.}",
year = "2019",
month = "4",
day = "1",
doi = "10.1093/cercor/bhy327",
language = "English",
volume = "29",
pages = "1706--1718",
journal = "Cerebral Cortex",
issn = "1047-3211",
publisher = "Oxford University Press",
number = "4",

}

Thalamocortical Afferents Innervate the Cortical Subplate much Earlier in Development in Primate than in Rodent. / Alzu'bi, Ayman; Homman-Ludiye, Jihane; Bourne, James A.; Clowry, Gavin J.

In: Cerebral Cortex, Vol. 29, No. 4, 01.04.2019, p. 1706-1718.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Thalamocortical Afferents Innervate the Cortical Subplate much Earlier in Development in Primate than in Rodent

AU - Alzu'bi, Ayman

AU - Homman-Ludiye, Jihane

AU - Bourne, James A.

AU - Clowry, Gavin J.

PY - 2019/4/1

Y1 - 2019/4/1

N2 - The current model, based on rodent data, proposes that thalamocortical afferents (TCA) innervate the subplate towards the end of cortical neurogenesis. This implies that the laminar identity of cortical neurons is specified by intrinsic instructions rather than information of thalamic origin. In order to determine whether this mechanism is conserved in the primates, we examined the growth of thalamocortical (TCA) and corticofugal afferents in early human and monkey fetal development. In the human, TCA, identified by secretagogin, calbindin, and ROBO1 immunoreactivity, were observed in the internal capsule of the ventral telencephalon as early as 7-7.5 PCW, crossing the pallial/subpallial boundary (PSB) by 8 PCW before the calretinin immunoreactive corticofugal fibers do. Furthermore, TCA were observed to be passing through the intermediate zone and innervating the presubplate of the dorsolateral cortex, and already by 10-12 PCW TCAs were occupying much of the cortex. Observations at equivalent stages in the marmoset confirmed that this pattern is conserved across primates. Therefore, our results demonstrate that in primates, TCAs innervate the cortical presubplate at earlier stages than previously demonstrated by acetylcholinesterase histochemistry, suggesting that pioneer thalamic afferents may contribute to early cortical circuitry that can participate in defining cortical neuron phenotypes.

AB - The current model, based on rodent data, proposes that thalamocortical afferents (TCA) innervate the subplate towards the end of cortical neurogenesis. This implies that the laminar identity of cortical neurons is specified by intrinsic instructions rather than information of thalamic origin. In order to determine whether this mechanism is conserved in the primates, we examined the growth of thalamocortical (TCA) and corticofugal afferents in early human and monkey fetal development. In the human, TCA, identified by secretagogin, calbindin, and ROBO1 immunoreactivity, were observed in the internal capsule of the ventral telencephalon as early as 7-7.5 PCW, crossing the pallial/subpallial boundary (PSB) by 8 PCW before the calretinin immunoreactive corticofugal fibers do. Furthermore, TCA were observed to be passing through the intermediate zone and innervating the presubplate of the dorsolateral cortex, and already by 10-12 PCW TCAs were occupying much of the cortex. Observations at equivalent stages in the marmoset confirmed that this pattern is conserved across primates. Therefore, our results demonstrate that in primates, TCAs innervate the cortical presubplate at earlier stages than previously demonstrated by acetylcholinesterase histochemistry, suggesting that pioneer thalamic afferents may contribute to early cortical circuitry that can participate in defining cortical neuron phenotypes.

KW - corticothalamic afferents

KW - human cortical development

KW - subplate

KW - thalamocortical afferents

KW - thalamus

UR - http://www.scopus.com/inward/record.url?scp=85062943238&partnerID=8YFLogxK

U2 - 10.1093/cercor/bhy327

DO - 10.1093/cercor/bhy327

M3 - Article

VL - 29

SP - 1706

EP - 1718

JO - Cerebral Cortex

JF - Cerebral Cortex

SN - 1047-3211

IS - 4

ER -