Differential distribution of neurons in the gyral white matter of the human cerebral cortex

Abstract

The neurons in the cortical white matter (WM neurons) originate from the first set of postmitotic neurons that migrates from the ventricular zone. In particular, they arise in the subplate that contains the earliest cells generated in the telencephalon, prior to the appearance of neurons in gray matter cortical layers. These cortical WM neurons are very numerous during development, when they are thought to participate in transient synaptic networks, although many of these cells later die, and relatively few cells survive as WM neurons in the adult. We used light and electron microscopy to analyze the distribution and density of WM neurons in various areas of the adult human cerebral cortex. Furthermore, we examined the perisomatic innervation of these neurons and estimated the density of synapses in the white matter. Finally, we examined the distribution and neurochemical nature of interneurons that putatively innervate the somata of WM neurons. From the data obtained, we can draw three main conclusions: first, the density of WM neurons varies depending on the cortical areas; second, calretinin-immunoreactive neurons represent the major subpopulation of GABAergic WM neurons; and, third, the somata of WM neurons are surrounded by both glutamatergic and GABAergic axon terminals, although only symmetric axosomatic synapses were found. By contrast, both symmetric and asymmetric axodendritic synapses were observed in the neuropil. We discuss the possible functional implications of these findings in terms of cortical circuits.

Individual Differences in Verbal Abilities Associated with Regional Blurring of the Left Gray and White Matter Boundary

“…Another factor is the presence of white matter neurons just below cortical layer VI, the density of which is unrelated to aging (Rojiani et al, 1996). Interstitial white matter neurons thinly populate the superficial white matter of healthy adult brains (Hardiman et al, 1988;Ramó n y Cajal, 1995;Suárez-Solá et al, 2009;García-Marín et al, 2010). They are believed to be remnants of the embryonic subplate (Chun and Shatz, 1989) that have either failed to undergo programmed cell death (Luhmann et al, 2009) or are the result of disrupted migrational processes (Chevassus-au-Louis and Represa, 1999).…”

Development, evolution and pathology of neocortical subplate neurons

“…In cats, opposite distributions for these cell types are observed 36,66 . Around the time of birth, both types of interstitial white matter neurons are present in equal numbers 38 in monkeys and humans, but there are conflicting reports about which cell morphology is more common in adult brains 38,65 . It is not clear whether multipolar neurons alter their morphology as a result of spatial constraints (the increasing ingrowth of thalamic axons decreases the available space in a non-uniform manner) or whether they are clearly distinct cell types that have distinct functions.…”

“…Calretinin and parvalbumin are rarely present in the sparsely distributed deep white matter neurons. One study found that within the superficial white matter, calretinin-positive cells comprise up to 15% of all neurons, whereas parvalbumin-positive cells comprise up to 6% of neurons, but the overlap between both populations was not assessed 65 . In cats, estimates of interneuron percentages range from 7% of cells in young postnatal subplate 66 to 25% of neurons in adult subplate 36 .…”

“…Interstitial white matter neurons in monkeys and humans are polymorphic neurons with large cell bodies and radially symmetric dendrites or fusiform neurons with a smaller soma and two main dendrites oriented parallel to the main fibre tracts 38 . In monkeys and humans, multipolar neurons are mainly found near the boundary with layer 6a and fusiform cells are located deep within white matter 38,65 . In cats, opposite distributions for these cell types are observed 36,66 .…”

Expression profiling of mouse subplate reveals a dynamic gene network and disease association with autism and schizophrenia

“…The early postnatal SP neurons in rodents and cats are involved in generating oscillations in cortex (8,9) and are necessary for the maturation of the inhibitory circuitry in cortical layer (L)4 (10,11). The remaining adult SP/L6b cells in nonrodent species have been suggested to support corticocortical connectivity (1,(12)(13)(14)(15).…”