A brief comparative review of primate posterior parietal cortex: A novel hypothesis on the human toolmaker

Abstract

The primate visual system contains two major cortical pathways: a ventral-temporal pathway that has been associated with object processing and recognition, and a dorsal-parietal pathway that has been associated with spatial processing and action guidance. Our understanding of the role of the dorsal pathway, in particular, has greatly evolved within the framework of the two-pathway hypothesis since its original conception. Here, we present a comparative review of the primate dorsal pathway in humans and monkeys based on electrophysiological, neuroimaging, neuropsychological, and neuroanatomical studies. We consider similarities and differences across species in terms of the topographic representation of visual space; specificity for eye, reaching, or grasping movements; multi-modal response properties; and the representation of objects and tools. We also review the relative anatomical location of functionally- and topographically-defined regions of the posterior parietal cortex. An emerging theme from this comparative analysis is that non-spatial information is represented to a greater degree, and with increased complexity, in the human dorsal visual system. We propose that non-spatial information in the primate parietal cortex contributes to the perception-to-action system aimed at manipulating objects in peripersonal space. In humans, this network has expanded in multiple ways, including the development of a dorsal object vision system mirroring the complexity of the ventral stream, the integration of object information with parietal working memory systems, and the emergence of tool-specific object representations in the anterior intraparietal sulcus and regions of the inferior parietal lobe. We propose that these evolutionary changes have enabled the emergence of human-specific behaviors, such as the sophisticated use of tools.

Mapping numerical perception and operations in relation to functional and anatomical landmarks of human parietal cortex

“…Therefore, the number of areas and their relative localization with respect to IPS anatomy can show some differences across the two species, and suggestions for correspondence should rather emphasize similarities in characteristic functional response properties across areas. Such tentative functional equivalence has been proposed between lower-level intraparietal field map representations and LIP, as well as higher-level field map representations and VIP (Kastner et al, 2017;Konen and Kastner, 2008). In particular neurons in macaque LIP respond to saccadic eye movements (Andersen et al, 1990), whereas the majority of the neurons in VIP prefer smooth pursuit eye-movements (Schlack et al, 2003) and multisensory motion (Avillac et al, 2005).…”

“…Identifying equivalence between areas is non-trivial related to the fact that human parietal cortex has differentially expanded and is also recruited by higher-level functions that are not present in monkeys, such as language, sophisticated tool use and higher-level mathematics (Grefkes and Fink, 2005;Kastner et al, 2017). Therefore, the number of areas and their relative localization with respect to IPS anatomy can show some differences across the two species, and suggestions for correspondence should rather emphasize similarities in characteristic functional response properties across areas.…”

“…The latter defines six areas, labelled from IPS0 to IPS5, which have been identified by means of phase-encoded mapping in human intraparietal cortex, from its most posterior to most anterior subparts (Konen and Kastner, 2008;Sereno et al, 2001;Silver et al, 2005;Swisher et al, 2007). Based on similarities in the relative anatomical localization and functional response properties, tentative homologies have been proposed between some of these field maps and the macaque LIP/VIP complex (Kastner et al, 2017;Konen and Kastner, 2008). If in humans there should be a single core system recruited to support both numerical perception and numerical operations, which is equivalent to the monkey LIP/VIP complex, we would expect activations to be centered within the visual field map representations in all conditions.…”

Human Paleoneurology and the Evolution of the Parietal Cortex

“…Brain Behav Evol 2018;91:136-147 DOI: 10.1159/000488889 in humans than in other primates, in terms of size and organization [Grefkes and Fink, 2005;Choi et al, 2006], and its evolutionary changes in our species are possibly related to tool use [Kastner et al, 2017]. The homology between humans and nonhuman primates for their parietal cortex is not clear, although the complexity of the intraparietal sulcus in H. sapiens may have displaced and repositioned internal and external folding regions, generating a lack of correspondence between human and nonhuman cortical topology [Zlatkina and Petrides, 2014].…”

Attentional amplification of neural codes for number independent of other quantities along the dorsal visual stream

“…show a clear attentional amplification of numerosity information. Given that the human IPS 1-467 5 investigated in the current work is usually considered to be the equivalent of the macaque 468 LIP/VIP complex (Kastner et al, 2017), the difference between results may be due to a 469 difference across species, but differences in paradigms and in the nature of the signal 470 recorded in the two studies make it difficult to directly relate the two findings. For example, 471 monkeys were trained initially with the color match to sample task, then re-trained to respond 472 to number, thus implying comparisons across an extended time period and different context, 473…”