Invited ReviewPeripersonal space in the brain
Introduction
In everyday life, we experience the space around us as a unitary and seamless whole. Yet, a growing body of evidence in contemporary neuroscience reveals that the brain constructs not one but various functionally distinct representations of space. A key division is between near, peripersonal space and far, extrapersonal space representations. This was initially suggested by Brain (1941), who proposed the existence of a grasping distance and a walking distance to explain the selective impairment that right brain-damaged patients may show for one or the other region of space. The notion of a separate representation in the brain for the space immediately around the body was emphasized in subsequent neurophysiological studies (Hyvärinen and Poranen, 1974, Leinonen and Nyman, 1979, Mountcastle, 1976), and substantially elaborated and expanded by Rizzolatti et al., 1981a, Rizzolatti et al., 1981b), who introduced the term peripersonal space to highlight the close links between somatosensory (i.e., bodily) and visual processing exclusively pertaining to this sector of space.
Peripersonal space defines the region of space immediately surrounding our bodies in which objects can be grasped and manipulated. By contrast, extrapersonal space refers to the space beyond grasping distance, in which exploratory eye movements occur. The near vs. far space distinction has been utterly fecund in cognitive psychology and neuroscience, providing a theoretical frame of reference for several targeted studies, both in human and non-human primates, and thence an understanding of how the brain encodes the space around us.
Here, we primarily focus on peripersonal space (PPS), reviewing convergent results from several generation of studies, including neurophysiological studies in animals, neuropsychological investigations in monkeys and brain-damaged patients with spatial cognition disorders, as well as recent neuroimaging experiments in neurologically normal individuals. Collectively, these studies reveal that the primate brain constructs multiple, rapidly modifiable representations of space, centered on different body parts (i.e., hand-centered, head-centered, and trunk-centered), which arise through extensive multisensory interactions within a set of interconnected areas in the parietal and frontal cortex. PPS representations are pivotal in the sensory guidance of motor behavior, allowing us to interact with objects and, as demonstrated by recent studies, with other people near us (Fig. 1, Fig. 2).
Section snippets
Neurophysiological studies of peripersonal space in animals
Discrete processing of PPS was first revealed by single-cell recordings in monkeys, within a network of interconnected sensori-motor areas, such as the parietal and frontal premotor cortices, which are crucial for the control of somatic, head and arm movements (Graziano et al., 1994, Hyvärinen and Poranen, 1974, Rizzolatti et al., 1981a, Rizzolatti et al., 1981b, Gentilucci et al., 1983).
In the macaque monkey, the inferior aspect of the premotor cortex (area 6), particularly its caudal portion
Neuropsychological studies of peripersonal space in monkeys and humans
Studies of the behavioral effects of focal brain lesions have played a critical role in supporting the existence of a selective representation of the space near the body, often employing direct adaptations of animal paradigms, as well as seeking and exploiting homologies. One of the first pieces of empirical evidence for a double dissociation between peripersonal and extrapersonal space came from a study carried out on the frontal cortex of macaques (Rizzolatti et al., 1983). After unilateral
Neuroimaging studies of peripersonal space in humans
A more recent generation of studies has used brain imaging to investigate the anatomical underpinnings and functional mechanisms of PPS in healthy humans. These studies further highlight the homologies between cortical areas explored with single-cell recordings in the monkey and cortical regions in the human brain that are selective for processing objects in the space near us. In their functional magnetic resonance imaging (fMRI) study, Makin et al. (2007) identified regions within the
Social modulation of peripersonal space
Typically, the study of the PPS, both in human and non-human primates, has involved the use of three-dimensional objects presented near the body and its parts. However, the space close around us is not only the privileged region of space for grasping and manipulating objects but also for interacting with other individuals. Accordingly, a number of recent studies begun to explore how selectively social information can modulate our internal representation of the PPS. In their behavioral study,
The function of peripersonal space representation
What is the function of the PPS representation? Why does the brain construct multiple, body part-centered representations of the space immediately around us? Neurophysiological studies in monkey have revealed that neurons in the putamen, area VIP, and inferior area 6 have motor functions as well as multisensory functions (Rizzolatti et al., 1997). In humans, studies using single-pulse TMS have shown that auditory (Serino et al., 2009, Avenanti et al., 2012) or visual (Makin et al., 2009)
Conclusions
We have provided an inevitably limited review of the studies into the neural and functional mechanisms underlying the representation of PPS in the brain, both in humans and monkeys. Since its introduction, the concept of a segregated representation of the space near the body, i.e., the space within grasping distance, has been an important source of several ideas and experiments. We have reviewed converging evidence from several generations of studies, including neurophysiological research in
Acknowledgments
The authors wish to thank Dr. Brianna Beck for her help in editing the manuscript. This work was supported by grants from the Ministero Istruzione Università e Ricerca (PRIN 2010, protocol number: 2010XPMFW4_009) awarded to GdP, and from the University of Bologna (FARB 2014, protocol number: RFBO120993) awarded to Elisabetta Làdavas.
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