Cortical Integration of Vestibular and Visual Cues for Navigation, Visual Processing, and Perception

Abstract

Despite increasing evidence of its involvement in several key functions of the cerebral cortex, the vestibular sense rarely enters our consciousness. Indeed, the extent to which these internal signals are incorporated within cortical sensory representation and how they might be relied upon for sensory-driven decision-making, during, for example, spatial navigation, is yet to be understood. Recent novel experimental approaches in rodents have probed both the physiological and behavioral significance of vestibular signals and indicate that their widespread integration with vision improves both the cortical representation and perceptual accuracy of self-motion and orientation. Here, we summarize these recent findings with a focus on cortical circuits involved in visual perception and spatial navigation and highlight the major remaining knowledge gaps. We suggest that vestibulo-visual integration reflects a process of constant updating regarding the status of self-motion, and access to such information by the cortex is used for sensory perception and predictions that may be implemented for rapid, navigation-related decision-making.

Keywords: cerebral cortex; multisensory integration; self-motion; spatial navigation; vestibular; vision.

Figure 1. Neural circuits for integration of visual and head motion cues in the rodent brain.

Simplified diagram of neural pathways that convey vestibular (green arrows) and visual information (orange arrows) to cortical areas involved in spatial navigation and visual perception. Solid and dashed lines represent established pathways and putative routes that require further experimental evidence, respectively. Arrows show information flow rather than a detailed anatomical connectivity. For simplicity and due to limited data on translational vestibular signals, only angular head velocity and head orientation pathways are shown. AD, anterodorsal thalamic nucleus; AM, anteromedial thalamic nucleus; AV, anteroventral thalamic nucleus; DTg, dorsal tegmental nucleus of Gudden; LD, lateral dorsal thalamic nucleus; LGN, lateral geniculate nucleus; LMN, lateral mammillary nuclei; LP, lateral posterior thalamic nucleus; MMN, medial mammillary nuclei; VTg, ventral tegmental nucleus of Gudden.

Figure 2. Behavioural significance of the integration of vestibular and visual cues.

a, The integration of visual cues into the vestibular-dependent head direction signal is important for accurate spatial orientation. The stability of the head direction signal – measured as the amount of shift in the tuning of head-direction cells – is correlated with the rat’s performance in a homing task (left and middle). In the absence of visual cues, the head direction signal becomes less stable (right, increased shift in the tuning of head-direction cells), which may lead to more heading errors. Plots are simplified and based on Valerio & Taube 2012 (left) and Goodridge et al. 1998 (right). b1-2, The combination of vestibular and visual cues improves estimation of self-motion. In a rotation-discrimination task in which mice were trained to report their angular speed under different experimental conditions (b1), their performance improved significantly when both vestibular and visual stimuli were available (b2 left, magenta) compared to when rotated in the dark (blue). Similarly, in the retrosplenial cortex, the accuracy of decoding angular self-velocity from population activity increased when both vestibular and visual cues were available (b2 right) The improved perceptual and decoding accuracy under the multisensory condition could not be explained by the use of vision alone, since both were substantially lower when only visual motion stimuli were present (green). Schematics and plots are simplified and based on Keshavarzi et al. 2022. c. The integration of head and visual motion signals is essential for disambiguating the source of motion on the retina, which may arise from head and/or eye movements, or motion in the external world.