Body orientation contributes to modelling the effects of gravity for target interception in humans

Abstract

Key points It is known that interception of targets accelerated by gravity involves internal models coupled with visual signals. Non‐visual signals related to head and body orientation relative to gravity may also contribute, although their role is poorly understood. In a novel experiment, we asked pitched observers to hit a virtual target approaching with an acceleration that was either coherent or incoherent with their pitch‐tilt. Initially, the timing errors were large and independent of the coherence between target acceleration and observer's pitch. With practice, however, the timing errors became substantially smaller in the coherent conditions. The results show that information about head and body orientation can contribute to modelling the effects of gravity on a moving target. Orientation cues from vestibular and somatosensory signals might be integrated with visual signals in the vestibular cortex, where the internal model of gravity is assumed to be encoded. Abstract Interception of moving targets relies on visual signals and internal models. Less is known about the additional contribution of non‐visual cues about head and body orientation relative to gravity. We took advantage of Galileo's law of motion along an incline to demonstrate the effects of vestibular and somatosensory cues about head and body orientation on interception timing. Participants were asked to hit a ball rolling in a gutter towards the eyes, resulting in image expansion. The scene was presented in a head‐mounted display, without any visual information about gravity direction. In separate blocks of trials participants were pitched backwards by 20° or 60°, whereas ball acceleration was randomized across trials so as to be compatible with rolling down a slope of 20° or 60°. Initially, the timing errors were large, independently of the coherence between ball acceleration and pitch angle, consistent with responses based exclusively on visual information because visual stimuli were identical at both tilts. At the end of the experiment, however, the timing errors were systematically smaller in the coherent conditions than the incoherent ones. Moreover, the responses were significantly (P = 0.007) earlier when participants were pitched by 60° than when they were pitched by 20°. Therefore, practice with the task led to incorporation of information about head and body orientation relative to gravity for response timing. Instead, posture did not affect response timing in a control experiment in which participants hit a static target in synchrony with the last of a predictable series of stationary audiovisual stimuli.

Representational gravity: Empirical findings and theoretical implications

“…An internal model of gravity exists. McIntyre et al (2001), La Scaleia et al (2014), , La Scaleia et al (2019), Zago et al (2004; Zago (2008) An internal model incorporates visual, vestibular, and somatosensory information.…”

“…La Scaleia et al (2019) Visual information can influence an internal model of gravity. La Scaleia et al (2014), , La Scaleia et al (2019), Lacquaniti et al (2013) An internal model of gravity can be modified by learning. La Scaleia et al (2019), An internal model of gravity is not necessary, and continuous updating of action information is sufficient.…”

“…La Scaleia et al (2014), , La Scaleia et al (2019), Lacquaniti et al (2013) An internal model of gravity can be modified by learning. La Scaleia et al (2019), An internal model of gravity is not necessary, and continuous updating of action information is sufficient. Baurès et al (2007) Naïve physics Representational gravity might be influenced by belief in impetus.…”

“…Participants had to intercept the ball as it emerged from behind the occluder. Participants were generally able to successfully intercept the ball, and La suggested an internal model of target motion that contained information regarding effects of gravity was used to extrapolate the trajectory behind the occluder, and La Scaleia et al (2019) further suggested that such an internal model incorporated information from visual, vestibular, and somatosensory sources.…”

A cross-species neural integration of gravity for motor optimisation

“…Amongst others, one of these solutions is to learn and store internal models to disambiguate sensory information and to predict forthcoming movement dynamics. On earth, a pervasive component affecting perception and motion is gravity (Bringoux et al, 2012; Dakin and Rosenberg, 2018; Elmore et al, 2014; Gaveau et al, 2011, 2016; Jorges and Lopez-Moliner, 2017; Klein et al, 2018; Lacquaniti et al, 2013; McIntyre et al, 2001; Van Pelt et al, 2005; Rosenberg and Angelaki, 2014; Saradjian et al, 2014; La Scaleia et al, 2019; Senot et al, 2005; Tajadura-Jimenez et al, 2018; De Vrijer et al, 2008). Studies in both humans and non-human primates have provided strong evidence that the brain evolved an internal representation of gravity.…”