Cortical networks for encoding near and far space in the non-human primate

Abstract

While extra-personal space is often erroneously considered as a unique entity, early neuropsychological studies report a dissociation between near and far space processing both in humans and in monkeys. Here, we use functional MRI in a naturalistic 3D environment to describe the non-human primate near and far space cortical networks. We describe the co-occurrence of two extended functional networks respectively dedicated to near and far space processing. Specifically, far space processing involves occipital, temporal, parietal, posterior cingulate as well as orbitofrontal regions not activated by near space, possibly subserving the processing of the shape and identity of objects. In contrast, near space processing involves temporal, parietal, prefrontal and premotor regions not activated by far space, possibly subserving the preparation of an arm/hand mediated action in this proximal space. Interestingly, this network also involves somatosensory regions, suggesting a cross-modal anticipation of touch by a nearby object. Last, we also describe cortical regions that process both far and near space with a preference for one or the other. This suggests a continuous encoding of relative distance to the body, in the form of a far-to-near gradient. We propose that these cortical gradients in space representation subserve the physically delineable peripersonal spaces described in numerous psychology and psychophysics studies.

Frontier of Self and Impact Prediction

“…In a recent study based on the analysis of functional connectivity patterns, Mars et al (2013) propose that the monkey homologue of human TPJ actually lies within the superior temporal cortex, at a location often associated with the processing of faces and other social stimuli ( Perrett et al, 1992 ; Tsao et al, 2003 , 2008 ; Tsao and Livingstone, 2008 ; Rushworth et al, 2013 ; Popivanov et al, 2014 ; Premereur et al, 2016 ). Importantly, this same region is found to be activated in our impact prediction to the face study ( Cléry et al, 2017 ), as well as by objects looming toward PPS ( Cléry et al, 2018 ), or placed within PPS ( Cléry et al, 2018 ). Figure 3 captures this functional overlap.…”

“…This correlates with an enhanced tactile processing as assessed both by d’-sensitivity measures and reaction time (RT) measures ( Canzoneri et al, 2012 ; Cléry et al, 2015a ; Kandula et al, 2015 ; De Paepe et al, 2016 ). As a result, PPS has been proposed to define a safety boundary around the body ( Graziano and Cooke, 2006 ; Sambo and Iannetti, 2013 ; Cléry et al, 2015a , b , 2017 , 2018 ; de Vignemont and Iannetti, 2015 ). However, PPS is also, by definition, the space that is close to our body, or self.…”

“…As seen in Section “Peripersonal Space,” areas VIP and F4 are proposed to play a key role in the definition of PPS. In a recent monkey fMRI study we assess the neural bases of near and far space coding during naturalistic 3D moving objects ( Cléry et al, 2018 ). This study clearly confirms the involvement of both VIP and F4 for PPS encoding ( Cléry et al, 2015b :Figures 1B,C, 3; Cléry et al, 2018 : Figures 4, 8).…”

“…In a recent monkey fMRI study we assess the neural bases of near and far space coding during naturalistic 3D moving objects ( Cléry et al, 2018 ). This study clearly confirms the involvement of both VIP and F4 for PPS encoding ( Cléry et al, 2015b :Figures 1B,C, 3; Cléry et al, 2018 : Figures 4, 8). This confirms the prior observations from single neuron studies in monkeys ( Rizzolatti et al, 1981b ; Colby et al, 1993 ; Graziano et al, 1997 ; Bremmer et al, 2002a , b , 2013 ).…”

“…However, two important observations need to be highlighted at this point. First, our fMRI data show that within an area VIP anatomically defined as the fundal intraparietal sulcus region (IPS), and functionally identified as the cortical region activated by large field visual stimulation ( Colby et al, 1993 ; Bremmer et al, 2002a , b ; Guipponi et al, 2013 ), only a small portion is activated by visuo-tactile convergence ( Guipponi et al, 2013 : Figure 5; Cléry et al, 2015b : Figures 2B, 3), impact prediction to the face ( Cléry et al, 2015b : Figure 3B; Cléry et al, 2017 : Figure 3) and near space processing ( Cléry et al, 2015b : Figures 1B, 3; Cléry et al, 2018 : Figures 4, 8). Importantly, the very same voxels are activated by visuo-tactile convergence, prediction of touch/impact to the body and selective near space encoding, suggesting that these different functions are possibly implemented by unique neuronal computations (see Cléry et al, 2015b , for discussion).…”