Visual and Nonvisual Contributions to Three-Dimensional Heading Selectivity in the Medial Superior Temporal Area

Abstract

Robust perception of self-motion requires integration of visual motion signals with nonvisual cues. Neurons in the dorsal subdivision of the medial superior temporal area (MSTd) may be involved in this sensory integration, because they respond selectively to global patterns of optic flow, as well as translational motion in darkness. Using a virtual-reality system, we have characterized the three-dimensional (3D) tuning of MSTd neurons to heading directions defined by optic flow alone, inertial motion alone, and congruent combinations of the two cues. Among 255 MSTd neurons, 98% exhibited significant 3D heading tuning in response to optic flow, whereas 64% were selective for heading defined by inertial motion. Heading preferences for visual and inertial motion could be aligned but were just as frequently opposite. Moreover, heading selectivity in response to congruent visual/vestibular stimulation was typically weaker than that obtained using optic flow alone, and heading preferences under congruent stimulation were dominated by the visual input. Thus, MSTd neurons generally did not integrate visual and nonvisual cues to achieve better heading selectivity. A simple two-layer neural network, which received eye-centered visual inputs and head-centered vestibular inputs, reproduced the major features of the MSTd data. The network was trained to compute heading in a head-centered reference frame under all stimulus conditions, such that it performed a selective reference-frame transformation of visual, but not vestibular, signals. The similarity between network hidden units and MSTd neurons suggests that MSTd may be an early stage of sensory convergence involved in transforming optic flow information into a (head-centered) reference frame that facilitates integration with vestibular signals.

A functional link between area MSTd and heading perception based on vestibular signals

“…To activate vestibular otolith organs, inertial motion stimuli contained a Gaussian velocity profile with a peak-acceleration of 1 m/s 2 (Fig. 1c) 25 . The direction of heading was varied (Fig.…”

“…Approximately two-thirds of optic flow-sensitive neurons in MSTd also exhibit spatial tuning for inertial motion without optic flow 20,25,26 . To test whether these neurons contribute to heading perception, we recorded from single units in MSTd while monkeys A and C performed the heading discrimination task.…”

“…Area MSTd was localized using a combination of magnetic resonance imaging (MRI) scans, stereotaxic coordinates (~15mm lateral and ~3-6mm posterior to AP-0), white/gray matter transitions, and physiological response properties, as described in detail in a previous study 25 . In some penetrations, electrodes were further advanced into the retinotopicallyorganized middle temporal area (MT).…”

Vestibular Signals in Primate Thalamus: Properties and Origins

“…Other portions of parietal and temporal cortex showing vestibular activity include the anterior tip of the intraparietal sulcus (area 2v) (Büttner and Buettner 1978;Fredrickson et al, 1966;Schwarz and Fredrickson 1971a,b), the medial superior temporal area (Page and Duffy, 2003;Gu et al, 2006Gu et al, , 2007, and the ventral intraparietal area (Bremmer et al, 2002;Klam and Graf, 2003;Chen et al, 2007). Whether the pulvinar units we recorded could supply these parietal and temporal areas is presently unknown.…”

“…This information will yield a basic understanding of thalamic neural processing of vestibular signals, and provide insight into previous advances regarding cortical use of vestibular information (Fukushima et al, 2000(Fukushima et al, , 2004Chen et al, , 2007Gu et al, 2006Gu et al, , 2007. In addition, we investigated the anatomical origin of these responses by injecting neuroanatomical tracers into a vestibular responsive region of the thalamus and into its putative sources of input: the VN and CN.…”