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.
Highlights
It is generally accepted from studies in mice that the protomap of cortical arealisation, which determines which region of the cortex is innervated by which thalamic nucleus, is driven by intrinsic programmes of gene expression (Rakic 1988; Miyashita-Lin et al 1999; O’Leary et al 2007; Rakic et al 2009; Alfano and Studer 2013) and there is evidence that this may generally hold true in primates, including humans (Šestan et al 2001; Clowry et al 2018)
Our results demonstrate that in primates, thalamocortical afferents (TCA) 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
In terms of cortical development, it would appear that both mice and humans follow a similar timetable, as layer VI neurogenesis begins about the age when thalamic afferents are leaving the diencephalon and they innervate the cortex at the time when layer IV neurogenesis is becoming established
Summary
It is generally accepted from studies in mice that the protomap of cortical arealisation, which determines which region of the cortex is innervated by which thalamic nucleus, is driven by intrinsic programmes of gene expression (Rakic 1988; Miyashita-Lin et al 1999; O’Leary et al 2007; Rakic et al 2009; Alfano and Studer 2013) and there is evidence that this may generally hold true in primates, including humans (Šestan et al 2001; Clowry et al 2018). In studies employing histological, principally acetylcholinesterase histochemistry, and imaging modalities (Krsnik et al 2017; Išasegi et al 2018) it has been reported that TCA from the ventrolateral thalamus reach the DTB boundary at 7.5 PCW, the PSB at 9.5 PCW, enter the intermediate zone (IZ) of the cortical wall by PCW, innervating the presubplate (pSP) and deep cortical plate (CP) between and 14 PCW, around the time these two structures fuse to form a large subplate characteristic of primates (Kostovicand Rakic 1990; Wang et al 2010; Duque et al 2016) These fibers correspond to somatosensory thalamic afferents and are the earliest to arrive; preceding by 2 weeks thalamic innervation of anterior and posterior cortex as described in previous studies (Kostovicand Goldman Rakic 1983; Kostovicand Rakic 1984). In terms of cortical development, it would appear that both mice and humans follow a similar timetable, as layer VI (corticothalamic) neurogenesis begins about the age when thalamic afferents are leaving the diencephalon and they innervate the cortex at the time when layer IV (eventual target for primary thalamic afferents) neurogenesis is becoming established (http://translatingtime.org; Workman et al 2013; Silbereis et al 2016)
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