Shared contributions of the head and torso to spatial reference frames across spatial judgments

Abstract

Egocentric frames of reference take the body as the point of origin of a spatial coordinate system. Bodies, however, are not points, but extended objects, with distinct parts that can move independently of one another. We recently developed a novel paradigm to probe the use of different body parts in simple spatial judgments, what we called the misalignment paradigm. In this study, we applied the misalignment paradigm in a perspective-taking task to investigate whether the weightings given to different body parts are shared across different spatial judgments involving different spatial axes. Participants saw birds-eye images of a person with their head rotated 45° relative to the torso. On each trial, a ball appeared and participants made judgments either of whether the ball was to the person's left or right, or whether the ball was in front of the person or behind them. By analysing the pattern of responses with respect to both head and torso, we quantified the contribution of each body part to the reference frames underlying each judgment. For both judgment types we found clear contributions of both head and torso, with more weight being given on average to the torso. Individual differences in the use of the two body parts were correlated across judgment types indicating the use of a shared set of weightings used across spatial axes and judgments. Moreover, retesting of participants several months later showed high stability of these weightings, suggesting that they are stable characteristics of people.

Introduction

Egocentric frames of reference take the body as the point of origin of a spatial coordinate system (Klatzky, 1998). Recent work on self-consciousness has identified our first-person perspective with the point of origin of such an egocentric reference frame (Blanke & Metzinger, 2009; Foley, Whitwell, & Goodale, 2015; Vogeley & Fink, 2003). This raises a problem, however, since bodies are not points, but rather extended objects with multiple articulated parts which can move independently of each other. Changes in body posture therefore dissociate potential reference frames anchored to different body parts. It is therefore critical to understand the way in which different parts of the body contribute to judgments about the perceived spatial locations of objects.

The role of individual body parts in shaping judgments of visuospatial location is highlighted by Peacocke's (1992) Buckingham Palace thought experiment (pg. 62):

“Looking straight ahead at Buckingham Palace is one experience. It is another to look at the palace with one's face still toward it but with one's body turned toward a point on the right. In this second case the palace is experienced as being off to one side from the direction of straight ahead, even if the view remains exactly the same as in the first case.”

This example nicely captures the intuition that changes of body posture can dissociate the relative spatial relations of objects to different body parts, highlighting the problem of which body part – if any – serves as the origin of body-centred reference frames. Interestingly, Peacocke's own intuition seems to be torso-centric. The judgment that the palace is “experienced as being off to one side” links a change in the visuospatial location of the palace with a change in torso orientation. One could, however, pose the analogous question of where the palace would seem to be if one's torso remained oriented facing the palace but one's head was turned to the right.

It is also important to note that while it is natural to perform Peacocke's thought experiment by imagining oneself in front of Buckingham Palace, exactly the same issues arise if we make judgments about another person. This capacity for reasoning about another's visuospatial perception has been described as perspective-taking (Michelon & Zacks, 2006; Salatas & Flavell, 1976). In taking another's perspective, we may employ a body-centred frame of reference, in so far as we take (a part of) that person's body as the origin of the relevant spatial frame of reference. For instance, taking the Queen's perspective, as her procession approaches Buckingham Palace moving East along The Mall, our answer to the question “Is the palace to left or right?” may be sensitive to whether her torso is orientated toward St James's Park (roughly to the South) or St James's Square (roughly to the North), even as her gaze remains fixed on the palace ahead. The issue about which body parts shape spatial reference frames is therefore not specific to judgments in which one determines an object's location in relation to oneself. Rather, it applies more generally to judgments in which one determines an object's location in relation to any particular person.

A substantial literature on the use of reference frames for visuo-motor control of action has revealed evidence for a range of different reference frames. One influential view has linked the dorsal and ventral visual pathways to egocentric and allocentric reference frames, respectively (Foley et al., 2015; Goodale & Haffenden, 1998; Milner & Goodale, 2006). Single-unit neurophysiological studies in monkeys have demonstrated the existence of neurons with receptive fields coding the visual location of objects in references frames anchored to specific body parts, including the eyes (e.g., Andersen, Essick, & Siegel, 1985), head (e.g., Duhamel, Bremmer, BenHamed, & Graf, 1997), and hands (e.g., Graziano, Yap, & Gross, 1994). There is also evidence for neurons coding hybrid combinations of body parts (Carrozzo & Lacquaniti, 1994; Chang, Papadimitriou, & Snyder, 2009; Pesaran, Nelson, & Andersen, 2006; Piserchia et al., 2017), and modulation of responses coded in an eye-centred frame of reference by the position of other body parts (Chang et al., 2009; Zipser & Andersen, 1988) as well as idiosyncratic reference frames presumably related to transformation between different reference frames (Chang & Snyder, 2010; Gazzaniga, LeDoux, & Wilson, 1977), which has been found to involve a process of vector subtraction of the location of one body part relative to another (Batista, Buneo, Snyder, & Andersen, 1999; Buneo, Jarvis, Batista, & Andersen, 2002).

Studies in humans using both neuroimaging (Bernier & Grafton, 2010; Mcguire & Sabes, 2009; Sober & Sabes, 2005) and behavioural reaching paradigms (Beurze et al., 2006; Heuer & Sangals, 1998; Lemay & Stelmach, 2005; McIntyre, Stratta, & Lacquaniti, 1998) have shown that multiple reference frames centred on different body parts can be simultaneously activated and flexibly weighted based on the availability of different types of sensory information and task goals. Other studies have reported similar weighting of egocentric and allocentric representations (Byrne & Crawford, 2010; Chen et al., 2014). A gradient has been proposed between the posterior parietal and premotor cortices, with the former coding location more strongly in eye-centred and the latter in hand-centred reference frames (Pesaran et al., 2006). Nevertheless, introspection suggests that perceptual experience is unified to form a single first-person perspective (Bayne, 2010; Bermúdez, 1998), indicating that reference frames centred on different body parts may become integrated into a single ultimate reference frame underlying subjective perceptual experience. Various empirical and theoretical considerations have been advanced for why either the head (Avillac, Denève, Olivier, Pouget, & Duhamel, 2005; Sherrington, 1907), the eyes (Cohen & Andersen, 2002), or the torso (Alsmith & Longo, 2014; Blanke, 2012; Grubb & Reed, 2002; Grush, 2000; Karnath, Schenkel, & Fischer, 1991; Serino et al., 2015) might have such a privileged role. Sherrington (1907), for example, notes the wide range of sensory apparatus in the head, emphasising in particular the vestibular system's role in providing the overall posture of the whole body relative to gravity, a perspective also emphasised by recent research (Abekawa, Ferrè, Gallagher, Gomi, & Haggard, 2018; Pavlidou, Ferrè, & Lopez, 2018). Other researchers have emphasised the torso's position as a stable anchor for the limbs and head (Blanke, 2012; Grush, 2000), as “the great continent of the body” (Alsmith & Longo, 2014, pg. 74).

We recently developed a novel approach to quantifying the contribution of different body parts to 3rd-person spatial judgments, what we call the misalignment paradigm (Alsmith, Ferrè, & Longo, 2017). This paradigm is essentially an experimentalization of Peacocke's (1992) Buckingham Palace thought experiment, described above. Participants saw a top-down view of a person with their head rotated 45° to either the left or right of the torso, as shown in Fig. 1. On each trial, a red ball appeared, and participants judged whether the ball was to the person's left or to their right. Because the head and torso are misaligned, there are locations in which the ball is to the left with respect to one body part, but to the right with respect to the other. By presenting balls at different locations, we quantified the relative weighting given to the head and to the torso for left/right spatial judgments. We found that both the head and the torso were used, with greater weight on average being given to the torso. However, a wide range of patterns was observed across participants, with some people relying almost entirely on the torso, others relying almost entirely on the head, and others using a combination of both body parts. These results indicate that left/right spatial judgments rely, at least in some people, on a combination of frames of reference centred on the torso and on the head, and may do so with unequal weighting that may differ across people.

It remains unclear whether these results reflect the weighting of the torso and head specifically for judgments of right and left, or if they reflect a more general feature of spatial cognition. There is evidence that the Left/Right dimension may be uniquely confusable (Farrell, 1979; Nicoletti & Umiltà, 1984), which may relate the it being the axis in which vertebrate bodies are bilaterally-symmetric (Corballis & Beale, 1970). There are well-established functional connections between tactile representations of homologous locations on the left and right sides of the body (e.g., Iwamura, 2000; Tamè et al., 2012; Tamè, Farnè, & Pavani, 2011), as well as evidence that the Left/Right dimension can be selectively impaired as in conditions such as the Gerstmann syndrome (e.g., Benton, 1959; Kinsbourne & Warrington, 1963). It is therefore possible that the weighted use of the head and torso we described in our previous study (Alsmith et al., 2017) may be specific to the left/right axis rather than being a more general feature of spatial cognition. Alternatively, given that egocentric frames of reference can be used to identify locations in full 3-D space, and not only in the left/right axis, if these body-parts weightings are a more generalizable aspect of spatial cognition they may be used across very different types of spatial judgments. It is therefore important to show that the use of both torso and head we which reported previously (Alsmith et al., 2017) generalises across multiple spatial tasks, and is not specific to the left/right axis.

The present study used the misalignment paradigm to investigate whether comparable weighting is given to the head and torso for different forms of spatial judgment. Like in our previous study, participants saw a top-down view of a person with the head and torso misaligned (Fig. 1). In the Left/Right judgment task, participants judged whether each ball was to the person's left or to their right, as in our previous study. In the In front of/Behind judgment task, participants judged whether each ball was in front of the person or behind them. By comparing conditions in which the head was rotated either clockwise or anti-clockwise relative to the torso, we quantified the weighting given to both the head and to the torso for each type of judgment. If the weightings given to the head and torso that we have previously reported result from a general mechanism for determining locations in relation to particular body parts, then similar weightings should be found in the two judgment types, which should be correlated across participants. In contrast, if the weightings we found previously are specific to the left/right axis, then no such correspondence across judgments should be found.

In addition, in order the investigate the stability of these individual differences, we brought a subset of participants back into the lab several months after initial testing to examine whether the weightings they used were similar to that they used in the initial session. In our previous study (Alsmith et al., 2017), there were strong correlations (r > 0.9) between the weightings used by participants in different conditions. It is possible, however, that these correlations reflect transient differences between people in terms of their mood or other state-level characteristics. If these weightings reflect stable and enduring characteristics of people, they should be correlated across different sessions separated in time.