Laminar Origin of Corticostriatal Projections to the Motor Putamen in the Macaque Brain

Abstract

In the macaque brain, projections from distant, interconnected cortical areas converge in specific zones of the striatum. For example, specific zones of the motor putamen are targets of projections from frontal motor, inferior parietal, and ventrolateral prefrontal hand-related areas and thus are integral part of the so-called "lateral grasping network." In the present study, we analyzed the laminar distribution of corticostriatal neurons projecting to different parts of the motor putamen. Retrograde neural tracers were injected in different parts of the putamen in 3 Macaca mulatta (one male) and the laminar distribution of the labeled corticostriatal neurons was analyzed quantitatively. In frontal motor areas and frontal operculum, where most labeled cells were located, almost everywhere the proportion of corticostriatal labeled neurons in layers III and/ or VI was comparable or even stronger than in layer V. Furthermore, within these regions, the laminar distribution pattern of corticostriatal labeled neurons largely varied independently from their density and from the projecting area/sector, but likely according to the target striatal zone. Accordingly, the present data show that cortical areas may project in different ways to different striatal zones, which can be targets of specific combinations of signals originating from the various cortical layers of the areas of a given network. These observations extend current models of corticostriatal interactions, suggesting more complex modes of information processing in the basal ganglia for different motor and nonmotor functions and opening new questions on the architecture of the corticostriatal circuitry.

Crossed Corticostriatal Projections in the Macaque Brain

“…First, the cortical input to a specific striatal zone originates not only from a limited set of closely related neighbor areas, as initially described (Takada et al, 1998;Nambu, 2011;Averbeck et al, 2014) but also from distant, interconnected areas jointly involved in large-scale functionally specialized cortical networks (Gerbella et al, 2016;Choi et al, 2017). Second, the different striatal zones are targets of characteristically weighted laminar projections from multiple input areas (Griggs et al, 2017;Borra et al, 2021). Finally, the present data suggest that information processing in the striatum can also rely on substantial input from the contralateral hemisphere.…”

“…First, there is evidence for overlap in restricted striatal zones of projection fields of distant, interconnected areas jointly involved in specific large-scale functionally specialized cortical networks (Gerbella et al, 2016;Choi et al, 2017). Second, the laminar origin of the CSt projections from a given area can largely vary according to the target striatal zone so that different striatal zones are targets of characteristically weighted laminar projections from the various input areas (Borra et al, 2021).…”

Parietal maps of visual signals for bodily action planning

“…Notably, these signals converge up to the single-neuron level in the premotor cortex (Maranesi et al 2012 ; Bonini et al 2014 ) and very likely in AIP as well (Ferroni et al 2021 ), although a direct demonstration of the latter integration is still lacking. In addition, both area F5 and AIP receive consistent afferents, directly and indirectly, from the prefrontal and presupplementary motor cortices (Bruni et al 2018 ; Lanzilotto et al 2019 ; Albertini et al 2020 ) as well as from the basal ganglia (Gerbella et al 2016 ; Borra et al 2021 ), which also contribute to the evaluation and selection of action plans based on the external and internal state and goals of the subject.…”

A cortical mechanism linking saliency detection and motor reactivity in rhesus monkeys

“…A third potential route is the dense bilateral area BA9 projection to the caudate nucleus, and the re-entrant signaling through the thalamus. This projection has recently been detailed in both monkeys and humans (56), and further elaborated in monkeys by Borra et al (57). Which of these routes subserves the otherwise slow force response observed in our study, and their eventual interactions, remains to be determined.…”