Gravity bias in the interpretation of biological motion by inexperienced chicks

Our ability to recognise biological motion in point-light displays is reduced when the animation sequence is upside-down, taken as evidence that past experience about direction of gravity influences the perception of biological motion. We exposed newly hatched chicks, reared in darkness and thus in the absence of previous visual experience, to point-light animation sequences of a walking hen either upright or upside-down: they responded by aligning their bodies in the apparent direction of motion in the former situation, but not in the latter, indicating that the vertebrate brain might be predisposed to make assumptions about direction of gravity. When an animal moves, its limbs and torso move in characteristic synchrony. Johansson [1] first showed that an animation sequence consisting of just a few strategically placed points of light is sufficient to give a human observer the impression of an animal engaged in a coordinated activity. The detection and recognition of point-light walking is disrupted, however, when the display is turned upside down [2–4]. It has been suggested that difficulties with inverted displays arise, not because parts of the stimulus are not in their familiar relative locations, but because it is hard to recognize the action as the dynamic relations specified by the kinematics are unfamiliar [5]. For instance, in an upside-down display of a walking human, the normal pattern of acceleration shown by the limbs as they are pulling away from and then falling back toward earth is not detected. Empirical evidence that assumptions about the direction of gravity play a crucial role in interpreting biological motion has recently been reported. For instance, it has been shown that image inversion has a larger effect on performance than does image scrambling [6]. Even if human subjects had no idea about the kind of animal represented in a scrambled display, they could promptly and accurately indicate its walking direction; but, presenting the displays upside-down had a strong disrupting impact on the perceived direction, with performance dropping almost to chance level [6]. These data have been interpreted in terms of a sensory filter tuned to the ballistic movements of the limbs of an animal during locomotion [7]. Also, when detection accuracy was determined for upright and upside-down displays depicting a point-light human figure walking on his hands, detection was greater in the upright than in the upside-down display, even though the former had an unfamiliar object orientation [5]. These observations were taken [5] as evidence that biological organisms form, by observing the motion of objects in the natural world, a bias about the normal direction of gravity. An alternative, though seemingly unlikely, hypothesis would be that the apparent gravity bias does not require learning, but reflects a predisposition manifesting even in the absence of visual experience. Developmental studies have been unable to address this issue, hard to prove or disprove unequivocally with human subjects [8]. Non-human animals have also been shown to respond to biological motion patterns [9–11]. We took advantage of the behaviour of the highly precocial domestic chick: chicks have been shown capable of discriminating point-light animation sequences [12], and are predisposed to preferentially approach biological motion patterns when first exposed to point-light animation displays [13]. Naïve, newly hatched chicks, lacking of any visual experience, were presented with a canonical (upright) or an inverted (upside-down) point-light animation sequence picturing a ‘walking hen’ (Figure 1A,B). The displays moved while staying in the same place on the screen, as though representing animals moving on a treadmill. A single point-light stimulus display was presented to a chick, and for several minutes we scored the chick’s body orientation with respect to the apparent direction of movement of the point-light stimulus (see Supplemental Experimental Procedures available online). This procedure enabled us to measure a chick’s sensitivity to the features of a single biological