Multisensory integration for orientation and movement

Abstract

Our perception of external movement relative to that of our own body and the ability to differentiate between self-induced and external movement is crucial for the huge range of complex behavioural motions of which we are capable: from crossing the deck of a ship at sea, to co-ordinating a forehand volley or catching a ball on the run. These tasks require integration of visual, vestibular, somatosensory, proprioreceptive, motor and even auditory systems. Cues to self-motion, such as the optic flow across the retina as the head moves or the change in apparent sound location, are critical for precision and orientation of the body and in co-ordinating compensatory movements, balance and motor programmes. Here we present four reviews of this fascinating physiological problem. The articles originate from a series of Symposium presentations at the July 2010 meeting of The Physiological Society at the University of Manchester. The first review, by Rebecca St George and Richard Fitzpatrick (St George & Fitzpatrick, 2011), explores the integration of different sensory inputs which create the percept of body orientation and movement. This perceptual fusion is tested in man by observing the changes in perception with head posture during locomotion and conflicting sensory input arising from galvanic stimulation of the vestibular system. In the second review, Frank Bremmer considers the remarkable processes by which we perceive the outside world as static even when the sensory systems themselves are in constant motion (Bremmer, 2011). The brain must differentiate between self-induced motion, for instance a head movement causing flow of the optic field across the retina, and real motion of an object in the outside world. He discusses the evidence that the primate posterior parietal cortex is concerned with the multisensory processing of spatial information and motion (and so is a key element in the dorsal ‘where’ pathway). This theme is continued by Dora Angelaki, Yong Gu and Gregory Deangelis by consideration of the multisensory neurons of the dorsal medial superior temporal area (MSTd), which integrate visual and vestibular cues (Angelaki et al. 2011). The activity of specific neuronal subpopulations predicts self-motion behaviour, with deficits on inactivation of the MSTd and enhanced sensitivity when the cues are congruent, supporting the idea that this site is involved in heading perception. Finally, Jeffrey Taube reviews the evidence for vestibular inputs into ‘head direction’ (HD) neurons (Taube, 2011). These cells complement hippocampal place cells, which specify spatial location, by providing a directional heading. The HD cells are located in the anterior dorsal thalamus and are dominated by visual inputs, generally responding to movement in two dimensions within a horizontal plane. When a third dimension is introduced, such as the rat being in the vertical plane, navigation is good until the animals are inverted. The reviewed evidence suggests that otolith inputs provide crucial inputs required for normal activity of the HD cells.