Abstract
Structural connections between cortical areas form an intricate network with a high degree of specificity. Many aspects of this complex network organization in the adult mammalian cortex are captured by an architectonic type principle, which relates structural connections to the architectonic differentiation of brain regions. In particular, the laminar patterns of projection origins are a prominent feature of structural connections that varies in a graded manner with the relative architectonic differentiation of connected areas in the adult brain. Here we show that the architectonic type principle is already apparent for the laminar origins of cortico-cortical projections in the immature cortex of the macaque monkey. We find that prenatal and neonatal laminar patterns correlate with cortical architectonic differentiation, and that the relation of laminar patterns to architectonic differences between connected areas is not substantially altered by the complete loss of visual input. Moreover, we find that the degree of change in laminar patterns that projections undergo during development varies in proportion to the relative architectonic differentiation of the connected areas. Hence, it appears that initial biases in laminar projection patterns become progressively strengthened by later developmental processes. These findings suggest that early neurogenetic processes during the formation of the brain are sufficient to establish the characteristic laminar projection patterns. This conclusion is in line with previously suggested mechanistic explanations underlying the emergence of the architectonic type principle and provides further constraints for exploring the fundamental factors that shape structural connectivity in the mammalian brain.
Highlights
Brain regions are linked by a complex, characteristically organized network of structural connections
The first support of the suggested mechanistic explanation for the emergence of the architectonic type principle has come from in silico models, where simulation results have shown that simple interactions between the time and place of neurogenesis can result in structural networks that capture many of the relationships observed in empirical mammalian cortico-cortical connections (Beul et al 2018; Goulas et al 2019)
Making use of tract-tracing data detailing laminar patterns of projection origins obtained in the immature macaque cortex (Kennedy et al 1989; Batardière et al 2002; Magrou et al 2018), we here investigate the extent to which the architectonic type principle applies to the connectional data from early development and enucleated animals, presenting findings which indicate that the processes very early during ontogenesis are sufficient to establish laminar projection patterns that are consistent with the architectonic type principle
Summary
Brain regions are linked by a complex, characteristically organized network of structural connections. One principle that has been shown to capture reliably multiple topological features of cortico-cortical connectivity in the adult mammalian brain is the structural model (Barbas 1986, 2015; Barbas and Rempel-Clower 1997; García-Cabezas et al 2019), called architectonic type principle (Hilgetag et al 2019). The first support of the suggested mechanistic explanation for the emergence of the architectonic type principle has come from in silico models, where simulation results have shown that simple interactions between the time and place of neurogenesis can result in structural networks that capture many of the relationships observed in empirical mammalian cortico-cortical connections (Beul et al 2018; Goulas et al 2019) These simulation experiments have explored how the existence of connections (i.e., whether brain areas are connected or not) and the strength of projections can be shaped. Making use of tract-tracing data detailing laminar patterns of projection origins obtained in the immature macaque cortex (Kennedy et al 1989; Batardière et al 2002; Magrou et al 2018), we here investigate the extent to which the architectonic type principle applies to the connectional data from early development and enucleated animals, presenting findings which indicate that the processes very early during ontogenesis are sufficient to establish laminar projection patterns that are consistent with the architectonic type principle
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