An implicit body representation underlying human position sense

Abstract

Knowing the body's location in external space is a fundamental perceptual task. Perceiving the location of body parts through proprioception requires that information about the angles of each joint (i.e., body posture) be combined with information about the size and shape of the body segments between joints. Although information about body posture is specified by on-line afferent signals, no sensory signals are directly informative about body size and shape. Thus, human position sense must refer to a stored body model of the body's metric properties, such as body part size and shape. The need for such a model has long been recognized; however, the properties of this model have never been systematically investigated. We developed a technique to isolate and measure this body model. Participants judged the location in external space of 10 landmarks on the hand. By analyzing the internal configuration of the locations of these points, we produced implicit maps of the mental representation of hand size and shape. We show that this part of the body model is massively distorted, in a reliable and characteristic fashion, featuring shortened fingers and broadened hands. Intriguingly, these distortions appear to retain several characteristics of primary somatosensory representations, such as the Penfield homunculus.

Fig. 1.

(A) Schematic illustration of the need for a body model to localize the body in external space. Perceiving the elbow's location relative to the shoulder requires information about the length of the upper arm (L_ua), and perceiving the hand's location relative to the elbow requires information about the length of the forearm (L_fa). Perceiving the location of the hand relative to the shoulder clearly requires information not only about joint angles at the shoulder (Θ_s) and elbow (Θ_e), but also about the segment lengths of the upper arm (L_ua) and forearm (L_fa). Information about segment lengths, however, is not specified by on-line afferent signals, implying that they must come from a stored body model. (B) Schematic illustration of how this body model can be isolated from location judgments of distinct landmarks. Traditionally, studies of position sense have measured the error between the judged location of a body part and its actual position in space (i.e., E_ft and E_k). The represented length of a segment, such as the index finger (RL_if), can be determined by comparing the distance between the judged locations of the fingertip and knuckle, without respect to their true locations. RL_if can then be compared with true finger length (L_if). Thus, the size and shape of the body model can be assessed by investigating the internal configuration of localizations of multiple landmarks, without regard to differences in actual and perceived location. (C) Sample image showing the experimental setup and the image of the actual hand taken before and after each block. (D) Sample image showing the occluding board and localization judgment.

Fig. 2.

Results from Exp. 1. (A) Percent overestimation [i.e., (100 × judged length − actual length)/actual length] of finger lengths. Clear underestimation was observed, increasing from the radial (thumb) to the ulnar (little finger) side of the hand. Error bars are 1 SEM. (B) Percent overestimation of spacing between pairs of knuckles. Clear overestimation was observed. (C) Shape indices (100 × width/length) quantifying overall aspect ratio of the hand for the actual hand, the conscious body image measured by template matching, and the body model measured by localization judgments. (D) GPS of landmark positions for actual hands (black dots/black lines) and the body model inferred from localization judgments (white dots/dotted lines). Solid line indicates mean shape of actual hand; dotted line indicates mean shape of body model. (E) Average actual hand shape superposed on a rectangular coordinate grid. (F) Thin-plate spline depicting body model as a deformation of the actual hand.

Fig. 3.

Results from Exp. 2. (A) Percent overestimation of finger lengths in “normal” and “rotated” postures. (B) Percent overestimation of knuckle spacings in the two postures. (C) GPS of actual hands (black dots/black lines) and body model in normal posture (white dots/dotted lines). (D) GPS of actual hands (black dots/black lines) and body model in rotated posture (gray dots/dashed lines). (E) Thin-plate spline depicting shape of body model in normal posture as a deformation of actual hand shape. (F) Comparable thin-plate spline for rotated posture.

Fig. 4.

Results from Exp. 3. (A) Percent overestimation of finger lengths for left and right hands. (B) Percent overestimation of knuckle spacings for the two hands. (C) GPS of actual left hands (black dots/black lines) and left hand body model (white dots/dotted lines). (D) GPS of actual right hands (black dots/black lines) and right hand body model (gray dots/dashed lines). (E) Thin-plate spline depicting shape of left hand body model as a deformation of actual hand shape. (F) Comparable thin-plate spline for right hand body model.