Gravity in the Brain as a Reference for Space and Time Perception

in Multisensory Research
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Moving and interacting with the environment require a reference for orientation and a scale for calibration in space and time. There is a wide variety of environmental clues and calibrated frames at different locales, but the reference of gravity is ubiquitous on Earth. The pull of gravity on static objects provides a plummet which, together with the horizontal plane, defines a three-dimensional Cartesian frame for visual images. On the other hand, the gravitational acceleration of falling objects can provide a time-stamp on events, because the motion duration of an object accelerated by gravity over a given path is fixed. Indeed, since ancient times, man has been using plumb bobs for spatial surveying, and water clocks or pendulum clocks for time keeping. Here we review behavioral evidence in favor of the hypothesis that the brain is endowed with mechanisms that exploit the presence of gravity to estimate the spatial orientation and the passage of time. Several visual and non-visual (vestibular, haptic, visceral) cues are merged to estimate the orientation of the visual vertical. However, the relative weight of each cue is not fixed, but depends on the specific task. Next, we show that an internal model of the effects of gravity is combined with multisensory signals to time the interception of falling objects, to time the passage through spatial landmarks during virtual navigation, to assess the duration of a gravitational motion, and to judge the naturalness of periodic motion under gravity.

Gravity in the Brain as a Reference for Space and Time Perception

in Multisensory Research

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ZagoM.CarrozzoM.MoscatelliA.LacquanitiF. (2011a). Time, observation, movementCogn. Crit. 46186.

ZagoM.La ScaleiaB.MillerW. L.LacquanitiF. (2011b). Coherence of structural visual cues and pictorial gravity paves the way for interceptive actionsJ. Vis. 11(10) 13.

ZaidelA.MaW. J.AngelakiD. E. (2013). Supervised calibration relies on the multisensory perceptNeuron 8015441557.

Figures

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    Model proposed by Dyde et al. (2006) for the subjective estimate of the upward direction. The vector sum of gravity, body orientation and visual cues corresponds to the estimated upward. This figure is published in colour in the online version.

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    Motor timing of punching movements. In the experiments of Zago et al. (2005), subjects intercepted a virtual sphere moving vertically downward on a screen by punching a real ball that fell under gravity hidden behind the screen (right panels). The virtual sphere and the real ball arrived in synchrony below the lower border of the screen. The virtual target descended either accelerated by gravity (1 g) or at constant speed (0 g). Wrist acceleration records are aligned relative to the arrival time of the target. Traces are ordered from the first to the last repetition from bottom to top in each panel. Notice that, for 1-g targets, the zero-crossing of acceleration occurred systematically close to target arrival, indicating that subjects generated maximum momentum to punch the ball at the right time. By contrast, for 0-g targets, hand movements were much more variable; they tended to start and to end too early, with the result that the hand arrived too soon and passed beyond destination before target arrival. With practice, performance improved with 0-g targets, but the responses often remained premature. This figure is published in colour in the online version.

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    Left column. (A) In the experiments of La Scaleia et al. (2014), a real ball rolled down an incline with a kinematics that differed as a function of the starting position and slope angle, and subjects had to punch it after its exit from the incline. (B) Timing errors (TE) for each condition (slope angle and duration of ball motion, nBMD). Responses were well within the theoretical margin of error for successful punching (grey area). Right column. (C) In the experiments of Mijatović et al. (2014), subjects pressed a button to intercept a virtual target sliding along an inclined plane, either downwards under normal gravity or upwards under artificial reversed gravity. Target motion was occluded from view over the last segment. (D) Difference in timing error (DTE) between the reversed gravity and the normal gravity conditions. The responses in the condition with unnatural forces were systematically delayed relative to those with natural forces. This figure is published in colour in the online version.

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    In the experiments of Miller et al. (2008), a virtual ball was launched vertically from the red box, rebounded at the trajectory apex, and returned to the starting point where it had to be intercepted. In g trials, target acceleration was consistent with natural gravity, that is, the target decelerated while moving up and accelerated while moving down. In rg trials, instead, target acceleration was reversed relative to natural gravity, that is, the target accelerated while moving up and decelerated while moving down. Target motion was embedded in a pictorial context (top left) or in a blank scene (top right). Bottom panel: Response timing errors (RTE) as a function of target motion (g vs. rg) and visual context (pictorial vs. non-pictorial). Responses were timed systematically better for downward accelerating (white bar) versus downward decelerating (black bar) balls with the pictorial scene, but this facilitation disappeared with the non-pictorial scene. This figure is published in colour in the online version.

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    Effect of visual congruence between background and gravity orientation. Top panels: In the experiments of Zago et al. (2011b), the virtual ball was launched vertically from the launcher, hit the opposite surface and bounced back. The target decelerated from launch to bounce (blue trajectory), and it accelerated after bounce (red trajectory). When subjects pressed the button, the standing person in the scene shot a bullet toward the interception point (cross-hair). The direction of the scene (‘s’) and the direction of virtual gravity acting on the target (‘g’) were varied in different blocks of trials: (A) normal scene and gravity, (B) normal scene and inverted target gravity, (C) inverted scene and gravity, (D) inverted scene and normal target gravity. Bottom panel: Success rate for each condition. Success rate was significantly higher for the congruent scenes (A and C) than for the incongruent ones (B and D). This figure is published in colour in the online version.

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    Time-to-passage during passive self-motion. In the experiments of Indovina et al. (2013a), subjects riding a virtual roller-coaster pressed a button at the time at which they thought the rollercoaster car passed through a reference point. Left: Still frames from animated visual stimuli simulating the roller-coaster ride. Vertical and horizontal tracks are shown at the onset of the trial and at about 2 m before crossing the passage reference point. Right: Difference between time-to-passage (DTTP) during vertical motions and that during horizontal motions, plotted as a function of motion law. Va, vertical accelerated; Vc, vertical constant speed; Vd, vertical decelerated; Ha, horizontal accelerated; Hc, horizontal constant speed; Hd, horizontal decelerated. The results show a significant anticipation in the time-to-passage estimate during the vertically accelerated downward motion (free fall) when compared with accelerated horizontal motion. This figure is published in colour in the online version.

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    Implied gravity in a pendulum motion biases the visual perception of speed (experiments of La Scaleia et al., 2014b). (A) In one experiment, the target oscillated back-and-forth along a circular arc around an invisible pivot (leftmost and middle panels). The imaginary segment from the pivot to the midpoint of the trajectory could be oriented vertically downward (consistent with an upright pendulum, leftmost panel), or vertically upward (upside-down, middle panel). In another experiment, the target moved uni-directionally, anticlockwise on a circular trajectory, being visible only in the bottom and top quadrants (rightmost panel). In all experiments, the target shifted according to one of 21 different kinematic conditions, including both harmonic and constant speed motion, and the observers were asked to choose the profile that appeared most uniform. (B) Distribution histograms of the responses (pooled over all participants) for the conditions illustrated in A. Abscissae: motion conditions: −1 g corresponds to a target moving under reverse gravity; 0 g, constant-speed motion, 1 g, motion under natural gravity; 2 g and 3 g, motions with maximum velocity twice and three times as large as 1 g, respectively. Ordinates: number of responses. Blue (black) bars: 0 g; red (grey) bars: 1 g. (C) Cumulative distribution functions for each participant (black) and for the population (red). The results show that, for both pendulum orientations (leftmost and middle columns), the responses clustered around the kinematic profile simulating the effects of a virtual gravity (1 g) acting downwards (leftmost column), or upwards (middle column), although the responses were much less variable in the former than the latter case. In contrast, the responses for unidirectional motion along the circle (rightmost column) clustered close to the constant speed profile. This figure is published in colour in the online version.

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