Thalamic Inputs to Posterior Parietal Cortical Areas Involved in Skilled Forelimb Movement and Tool Use in the Capuchin Monkey

Abstract

The posterior parietal cortex (PPC) is a central hub for the primate forebrain networks that control skilled manual behavior, including tool use. Here, we quantified and compared the sources of thalamic input to electrophysiologically-identified hand/forearm-related regions of several PPC areas, namely areas 5v, AIP, PFG, and PF, of the capuchin monkey (Sapajus sp). We found that these areas receive most of their thalamic connections from the Anterior Pulvinar (PuA), Lateral Posterior (LP) and Medial Pulvinar (PuM) nuclei. Each PPC area receives a specific combination of projections from these nuclei, and fewer additional projections from other nuclei. Moreover, retrograde labeling of the cells innervating different PPC areas revealed substantial intermingling of these cells within the thalamus. Differences in thalamic input may contribute to the different functional properties displayed by the PPC areas. Furthermore, the observed innervation of functionally-related PPC domains from partly intermingled thalamic cell populations accords with the notion that higher-order thalamic inputs may dynamically regulate functional connectivity between cortical areas.

Thalamocortical and corticothalamic connections of multiple functional domains in posterior parietal cortex of galagos

“…In macaques (Old World monkeys), areas PE, Pea, and PEc, occupying dorsorostral PPC above IPS and the adjacent upper bank of IPS, have major reciprocal connections with LP, APul, MPul, VL, CL, and caudal VPL (Cappe et al., 2007; Impieri et al., 2018; Schmahmann & Pandya, 1990; Yeterian & Pandya, 1985). This is in agreement with the reported connectional patterns of Area 5v in capuchin monkeys (New World monkeys; Mayer et al., 2019) as well as Area 5 in titi monkeys (New World monkeys), with sparser LP connections and denser VL connections in titi monkeys compared to macaques (Padberg & Krubitzer, 2006). In squirrel monkeys and owl monkeys (both New World monkeys), LP, APul, and VL remain the primary source of thalamic projections to PPC domains corresponding to the dorsal PPC region of other monkeys, with additional VPL projections to the grasp domain of rostrolateral PPC (Gharbawie et al., 2010).…”

“…A rostral‐to‐caudal trend appears to exist in macaques such that the strongest connections with LP and Pul shift from the ventral to dorsal portion of these nuclei (Kasdon & Jacobson, 1978; Schmahmann & Pandya, 1990; Yeterian & Pandya, 1985), lining up with the observations from Old World stump‐tailed monkeys (Weber & Yin, 1984). Inputs to areas PF and PFG of the rostral and medial parts of ventral PPC are predominated by those from LP, APul, and MPul in capuchin monkeys (Mayer et al., 2019). The present study indicates APul/Po, LP, as well as VL also to be major connectional targets of the ventral PPC grimacing domain in galagos.…”

“…However, the functional significance of such connections in macaques is less certain, as few studies used functional information to locate injection sites for anatomical tracers, and identifying presumptive PPC domains by electrical stimulation has been less commonly reported in macaques. Although some studies mapped PPC regions of several New World monkey species with electrical stimulation (Gharbawie et al., 2010) or recording (Mayer et al., 2019) to guide anatomical tracer injection sites, their efforts focused on hand and forelimb movement domains, leaving the rest of the region unexplored.…”

The Multiple Representations of Complex Digit Movements in Primary Motor Cortex Form the Building Blocks for Complex Grip Types in Capuchin Monkeys

“…This lithic percussive behavior requires the implicit knowledge of object features, such as size, shape, and density, and how objects can be manipulated to alter or transform other objects. In capuchins, these abilities and other behaviors that require complex digit movements co-evolved with an elaboration of motor areas, such as primary motor cortex (M1), sup-plementary motor area (SMA), ventral premotor cortex (PMv), and dorsal premotor cortex (PMd) (e.g., Dum and Strick, 2005;Dea et al, 2016;Hamadjida et al, 2016;Côté et al, 2017), the addition of parietal areas, such as area 2 and an expanded area 5 (e.g., Padberg et al, 2007;Mayer et al, 2016Mayer et al, , 2019, the emergence of specializations in the skeletal morphology of the hand (e.g., Spinozzi et al, 2004Spinozzi et al, , 2007Aversi-Ferreira et al, 2011), and corticospinal projections involved in fine control of individual digits (Heffner and Masterton, 1983;Bortoff and Strick, 1993). However, these features of organization have evolved independently from similar alterations in the body and brain of Old World primates, and are not present in other New World monkeys.…”

Neural Processes Underlying Tool Use in Humans, Macaques, and Corvids

“…The ability to use tools and the presence of mirror neurons in their brains make macaques an interesting model for the study of tool use in vertebrates since mirror neurons are active during object-directed actions. Although there are neurocognitive studies exploring tool-use in a number of other species of non-human primates (e.g., Hopkins et al, 2012 , 2017 ; Phillips and Thompson, 2013 ; Mayer et al, 2019 ) we have focused the following section on macaques because our objective is to suggest a possible neural network for tool use in a non-human primate species. For this purpose, using a single genus instead of a combination of findings from multiple species prevents us from generating a misleading network, since different species might differ in many ways, including anatomically, mechanistically, behaviorally, and cognitively.…”