Multisensory Convergence of Visual and Vestibular Heading Cues in the Pursuit Area of the Frontal Eye Field

Abstract

Both visual and vestibular sensory cues are important for perceiving one's direction of heading during self-motion. Previous studies have identified multisensory, heading-selective neurons in the dorsal medial superior temporal area (MSTd) and the ventral intraparietal area (VIP). Both MSTd and VIP have strong recurrent connections with the pursuit area of the frontal eye field (FEFsem), but whether FEFsem neurons may contribute to multisensory heading perception remain unknown. We characterized the tuning of macaque FEFsem neurons to visual, vestibular, and multisensory heading stimuli. About two-thirds of FEFsem neurons exhibited significant heading selectivity based on either vestibular or visual stimulation. These multisensory neurons shared many properties, including distributions of tuning strength and heading preferences, with MSTd and VIP neurons. Fisher information analysis also revealed that the average FEFsem neuron was almost as sensitive as MSTd or VIP cells. Visual and vestibular heading preferences in FEFsem tended to be either matched (congruent cells) or discrepant (opposite cells), such that combined stimulation strengthened heading selectivity for congruent cells but weakened heading selectivity for opposite cells. These findings demonstrate that, in addition to oculomotor functions, FEFsem neurons also exhibit properties that may allow them to contribute to a cortical network that processes multisensory heading cues.

Decentralized Multisensory Information Integration in Neural Systems

“…Moreover, we assumed further that the effective noise strength ␤, which is the ratio of noise variance over bump height and reflects the signal-to-noise ratio of the network, is approximately unchanged across different stimulus conditions. This assumption is supported by the experimental observation that Fano factors of neural responses change insignificantly with stimulus conditions (Gu et al, 2008). With these approximations and symmetric parameter settings, it is straightforward to derive Equations 44 and 45.…”

“…A straightforward hypothesis is that a dedicated integration area, which receives feedforward inputs from all sensory modalities to be combined, pools and integrates all of the incoming information (Ma et al, 2006;Alvarado et al, 2008;Ursino et al, 2009;Ohshiro et al, 2011). Although it has been shown that optimal multisensory integration could be achieved within such a dedicated area under certain conditions (Ma et al, 2006), the hypothesis does not touch upon the recent experimental findings that many interconnected multisensory areas are involved in the integration of sensory signals instead of just a single dedicated area (Gu et al, 2008;Chen et al, 2011bChen et al, , 2013. Here, we argue that the existence of many multisensory areas should not be just seen as added complexity to the hypothesis of having one dedicated integration area, but instead might be at the core of how the brain coordinates the flow of information.…”

“…To reproduce experimental findings (Gu et al, 2008), we designed a computational task to discriminate whether a stimulus value is smaller or larger than 0°based on single neuron activities. Similar to the experiment, we chose an example neuron from network 1 that preferred a heading direction of Ϫ40°.…”

“…In the brain, these visual and vestibular inputs can be fused seamlessly to give rise to a more reliable estimation of the motion direction than either of the modalities could deliver on its own (Gu et al, 2008;Chen et al, 2013). This capability of optimal multisensory integration seems ubiquitous across modalities, as has been reported, for example, for the integration of visual and auditory cues for inferring object location (Alais and Burr, 2004), motion and texture cues for depth perception (Jacobs, 1999), visual and proprioceptive cues for hand position (van Beers et al, 1999), and visual and haptic cues for object height (Ernst and Banks, 2002).…”

“…Anatomically, there is some supportive evidence. For instance, MSTd and VIP are two brain areas that are deeply involved in the integration of visual and vestibular information for inferring the heading direction and do so optimally (Gu et al, 2008;Chen et al, 2013). There are abundant reciprocal connections between MSTd and VIP (Boussaoud et al, 1990;Baizer et al, 1991) that cause the activities of the two areas to be correlated with each other (Vincent et al, 2007).…”