Evolution of posterior parietal cortex and parietal-frontal networks for specific actions in primates

Abstract

Posterior parietal cortex (PPC) is an extensive region of the human brain that develops relatively late and is proportionally large compared with that of monkeys and prosimian primates. Our ongoing comparative studies have led to several conclusions about the evolution of this posterior parietal region. In early placental mammals, PPC likely was a small multisensory region much like PPC of extant rodents and tree shrews. In early primates, PPC likely resembled that of prosimian galagos, in which caudal PPC (PPCc) is visual and rostral PPC (PPCr) has eight or more multisensory domains where electrical stimulation evokes different complex motor behaviors, including reaching, hand-to-mouth, looking, protecting the face or body, and grasping. These evoked behaviors depend on connections with functionally matched domains in premotor cortex (PMC) and motor cortex (M1). Domains in each region compete with each other, and a serial arrangement of domains allows different factors to influence motor outcomes successively. Similar arrangements of domains have been retained in New and Old World monkeys, and humans appear to have at least some of these domains. The great expansion and prolonged development of PPC in humans suggest the addition of functionally distinct territories. We propose that, across primates, PMC and M1 domains are second and third levels in a number of parallel, interacting networks for mediating and selecting one type of action over others.

Keywords: cortical connections; motor behavior; motor cortex; prosimian primates; visual cortex.

Fig. 1

A surface view of the flattened neocortex of a prosimian primate (Galago garnetti). Cortex has been separated from the rest of the brain and flattened as a single sheet with proposed cortical areas imposed. This view shows cortex normally hidden in views of the intact brain. The dashed lines roughly outline the cortex that would be visible on a dorsolateral view of the cerebral hemisphere. Posterior parietal cortex contains rostral (PPCr), caudal (PPCc) and medial (PPCm) regions. Primary (V1) and secondary (V2) visual areas are common to most mammals. As in other primates galagos also have the third visual area (V3), a dorsomedial area (DM), a middle temporal area (MT), a dorsolateral area (DL or V4), fundal area of the superior temporal sulcus (FST), a MT crescent (MTc), and inferior temporal cortex (IT) of several divisions. Auditory cortex includes A1 and rostral (R) areas, plus presumed auditory belt (AB) and parabelt (APB) regions. Somatosensory cortex includes a primary area (S1 or area 3b) (note the overall somatotopy), a proprioceptive area 3a and secondary areas of 1–2, S2, parietal ventral (PV) and ventral somatosensory (VS). Motor areas include primary motor area (M1) ventral (PMV) and dorsal (PMD) premotor areas, supplementary motor area (SMA), frontal eye field (FEF) and ventral (CMv), rostral (CMr) and caudal (CMc) cingulate areas. Frontal cortex includes frontal granular cortex (gFC), medial (OFm) and ventral (OFv) orbital frontal regions. Agranular (RSag) and granular (Rsg) retrosplenial areas, area prostriata (Pst) are noted. CC= corpus callosum. Stars mark horizontal meridian. Modified from Kaas and Preuss, 2014.

Fig. 2

Movement domains in rostral posterior parietal cortex (PPCr), motor cortex (M1 and premotor cortex (PMC) of galagos. Long train electrical stimulation was used to evoke different complex movements from different regions (domains). In PPCr, hindlimb movements, or hindlimb with forelimb movements, were evoked from the most medial domain. The laterally adjacent domain was characterized by evoked defensive arm movements as if to fend off an attack. More caudally, stimulation evoked reaching movements of the contralateral arm. More laterally, stimulation evoked hand to mouth movements, sometimes with opening of the mouth. Face defensive movements were evoked from more lateral cortex, with eye movements evoked from the most lateral part of the responsive cortex. More rostrally, face and forelimb movements were evoked in patterns that suggested threat response (face aggressive domain). Matching domains were in M1 and PMC. The domains are illustrated on a photograph of frontoparietal cortex. FSa and FSp, anterior and posterior frontal sulci, IPS- intraparietal sulcus, LS, lateral sulcus. Modified from Stepniewska et al., 2005.

Fig. 3

Proposed interactions of three example classes of domains, R-reach, D-defensive and G-grasp, in rostral posterior parietal cortex (PPCr), premotor cortex (PMC) and primary motor cortex (M1) of primates. In PPC domains are activated by various combinations of visual, somatosensory, and other sensory inputs. The domains compete with each other via mutual inhibition to be most activated, and to thereby activate functionally matched domains in PMC and M1, where further competition takes place. Domains in PMC are informed by inputs from prefrontal cortex and a relay of basal ganglia inputs to the motor thalamus. Domains in M1 receive inputs from PMC and PPC, other areas of motor cortex, and a relay of cerebellar inputs to the motor thalamus. All illustrated connections are excitatory (+), but they may have inhibitory effects by selectively activating inhibitory neurons (−) that are not shown. Feedforward connections from PPCr to PMC and M1 are focused to functionally matched domains, while feedback connections are more widespread, and may result in inhibition of mismatched domains. Connections between mismatched domains largely produce inhibition while patches of cortex (satellites) around domains contribute to domain functions via dense interconnections (shown only for the PPCr domain). This model is currently under further evaluation.

Fig. 4

Dense connections of a reach domain in PPCr of a galago with surrounding satellites. The photomicrograph is of a brain section cut parallel to the cortical surface after an injection of a tracer (BDA) into the reach domain identified by electrical stimulation. The injection core (outlined oval) labeled neurons and axons most densely and uniformly within the domain and in a patchy pattern along the margins of the domain, and just outside the domain. Modified from Stepniewska et al., 2015.

Fig. 5

The arrangement of functional domains in (A) galagos, (B) squirrel monkeys, and (C) owl monkeys in PPCr, PMC, and M1. Matching domains are found in all three regions, where they are arranged in similar mediolateral sequences. No movement domains have been found in caudal PPC (PPCc). At least 3–4 domains (reach, grasp, defense and eye movements) are also present or likely in macaques (not shown, see text). Modified from Stepniewska et al., 2014.