Ipsilateral corticotectal projections from the primary, premotor and supplementary motor cortical areas in adult macaque monkeys: a quantitative anterograde tracing study

Abstract

The corticotectal projection from cortical motor areas is one of several descending pathways involved in the indirect control of spinal motoneurons. In non-human primates, previous studies reported that cortical projections to the superior colliculus (SC) originated from the premotor cortex (PM) and the primary motor cortex, whereas no projection originated from the supplementary motor area (SMA). The aim of the present study was to investigate and compare the properties of corticotectal projections originating from these three cortical motor areas in intact adult macaques (n = 9). The anterograde tracer biotinylated dextran amine was injected into one of these cortical areas in each animal. Individual axonal boutons, both en passant and terminaux, were charted and counted in the different layers of the ipsilateral SC. The data confirmed the presence of strong corticotectal projections from the PM. A new observation was that strong corticotectal projections were also found to originate from the SMA (its proper division). The corticotectal projection from the primary motor cortex was quantitatively less strong than that from either the premotor or SMAs. The corticotectal projection from each motor area was directed mainly to the deep layer of the SC, although its intermediate layer was also a consistent target of fairly dense terminations. The strong corticotectal projections from non-primary motor areas are in position to influence the preparation and planning of voluntary movements.

Changes of motor corticobulbar projections following different lesion types affecting the central nervous system in adult macaque monkeys

“…The procedures and the analysis performed in PMRF on brainstem tissue (series stained one with BDA and one with Nissl) are the same as those recently published (Fregosi & Rouiller, ; Fregosi et al., ) for intact monkeys. Briefly, the relevant extent of the brainstem comprising PMRF included usually 12 sections from an individual series of sections, which were scanned using an Olympus BX40 microscope interfaced with the Neurolucida ® software (MBF, Bioscience‐MicroBrightField, Inc.…”

“…Boutons en passant were defined as boutons along an axon segment, visible at magnification 200x, exhibiting a diameter at least twice that of the axon's diameter. In each analysed BDA histological section, all labelled corticobulbar axonal boutons ( en passant and terminaux ) were counted in the delineated area of the brainstem, corresponding to a quantification method based on exhaustive plotting instead of stereology (see Fregosi & Rouiller, ). Furthermore, across monkeys, all histological samples were analysed according to the same procedure.…”

“…For normalization, the absolute number of corticobulbar boutons was divided by the total number of BDA‐labelled CS axons, then multiplied by 1000, corresponding to the normalized number of corticobulbar boutons. As the CS axons also arise from neurons in layer V, such normalization procedure is likely to reflect the extent of layer V which was indeed invaded by BDA, thus taking into account the probable zone of tracer uptake (see Fregosi et al., ; Fregosi & Rouiller, for more detail). The pros and cons (limits) of the normalization procedure were discussed in detail in two recent reports (Fregosi & Rouiller, ; Fregosi et al., ), and will not be repeated here.…”

The unsolved role of heightened connectivity from the unaffected hemisphere to paretic arm muscles in chronic stroke

“…A more likely connection would be an indirect cortico-reticulospinal connection (Bradnam et al, 2013;Baker et al, 2015). Indeed unilateral lesions of the pyramidal tract in primates are accompanied by an increase in excitability of reticulospinal inputs to spinal motoneurones from the non-lesioned side of the brain (Zaaimi et al, 2012;Fregosi et al, 2018;Fregosi and Rouiller, 2017) whereas there is little change in excitability of the smaller number of ipsilateral corticospinal synapses from the non-lesioned hemisphere (Zaaimi et al, 2012).…”

Emergent coordination with a brain–machine interface: implications for the neural basis of motor learning

“…Collective activity of neurons in superficial layers thus appears to encode higher-level movement parameters. In contrast, deep layers of M1, such as layer 5, contain neurons projecting out of the cortex to the spinal cord (Fregosi and Rouiller 2017;Rathelot et al 2017). Collective activity of neurons in deep layers thus appears to encode lower-level movement parameters.…”