Humans use internal models to construct and update a sense of verticality

Abstract

Internal models serve sensory processing, sensorimotor integration and motor control. They could be a way to construct and update a sense of verticality, by combining vestibular and somatosensory graviception. We tested this hypothesis by investigating self-orientation relative to gravity in 39 normal subjects and in subjects with various somatosensory losses showing either a complete deafferentation of trunk and lower limbs (14 paraplegic patients after complete traumatic spinal cord injury) or a gradient in the degree of a hemibody sensory loss (23 hemiplegic patients after stroke). We asked subjects to estimate, in the dark, the direction of the Earth vertical in two postural conditions-upright and at lateral whole body tilt. For upright conditions, verticality estimates were not different from the direction of the Earth vertical in normal (0.24° ± 1; P = 0.42) and paraplegic subjects (0.87° ± 0.9; P = 0.14). The within-subject variability was much greater in hemiplegic than in normal subjects (2.05° ± 1.15 versus 1.06° ± 0.4; P < 0.01) and greater in paraplegic than in normal subjects (1.13° ± 0.4 versus 0.72° ± 0.4; P < 0.01). These findings indicate that, even if vestibular graviception is intact, somaesthetic graviception contributes to the sense of verticality, leading to a more robust judgement about the direction of verticality when vestibular and somaesthetic graviception yield congruent information. As expected, when normal subjects were tilted, their verticality estimates were biased in the direction of the body tilt (5.55° ± 3.9). This normal modulation of verticality perception (Aubert effect), was preserved in hemiplegics on the side of the normoaesthetic hemibody (ipsilesional) (6.09° ± 6.3), and abolished both in paraplegics (1.06° ± 2.5) and in hemiplegics (0.04° ± 6.7) on the side of hypoaesthetic hemibody (contralesional). This incongruence did not exist in deafferented paraplegics who exclusively used vestibular graviception with a similar efficacy no matter what the lateral body position. The Aubert effect was not an on-off phenomenon since the degree of hemiplegics' somatosensory loss correlated with the modulation of verticality perception when they were tilted to the side of hypoaesthetic hemibody (r = -0.55; P < 0.01). The analysis of anatomical correlates showed that the Aubert effect required the integrity of the posterolateral thalamus. This study reveals the existence of a synthesis of vestibular and somaesthetic graviception for which the posterolateral thalamus plays a major role. This corresponds to a primary property of internal models and yields the neural bases of the Aubert effect. We conclude that humans construct and update internal models of verticality in which somatosensory information plays an important role.

The thalamocortical vestibular system in animals and humans

“…Brandt and colleagues suggested that the posterior insula could represent the human PIVC (Brandt and Dieterich, 1999). In keeping with this view, there is evidence that lesions of the insula and superior/middle temporal gyrus can impair the perception of the visual vertical (Barra et al, 2010;Hegemann et al, 2004) and induce rotational vertigo and unsteadiness (Boiten et al, 2003;Brandt et al, 1995;Cereda et al, 2002;Erbayat Altay et al, 2005;Nicita et al, 2010). Kahane and colleagues questioned whether a region they called temporo-peri-Sylvian vestibular cortex, "roughly distributed around the posterior part of the insula but clearly located more superficially, without involving the insula strictly speaking" could be the human homologue of PIVC.…”

Perception of Verticality in Patients with Primary Headache Disorders

“…Perception of verticality depends on the integration of vestibular, visual, and somatosensory information [28,29] . Lesions involving the central integrating system or central or peripheral vestibular system can lead to abnormal perception of body orientation in space and abnormal perception of vertical [1] .…”

Binocular and monocular measurements of subjective visual vertical in vestibular loss

“…SVV is assumed to be based on the internal estimation of verticality by the vestibular network (11,12). Thus, we were expecting that there would be no difference in verticality perception between monocular and binocular visions with normal subjects who have no abnormal eye position nor mismatch between visual and vestibular signals.…”