William K. Page

EYE POSITION SIGNALS IN THE ABDUCENS AND OCULOMOTOR NUCLEI OF MONKEYS DURING OCULAR CONVERGENCE

Many neurons in oculomotor pathways encode signals related to eye position. For example, motoneurons in the third, fourth, and sixth cranial nuclei discharge at highly regular rates during fixation intervals. During fixations of far targets, their tonic discharge is linearly related to conjugate eye position. Previous studies provided evidence that premotor cells in brainstem pathways also encoded conjugate eye position. McConville et al. (this volume), however, measured eye movements during binocular fixations when the eyes were converged and concluded that the position signal encoded by premotor position-vestibular-pause (PVP) cells in the vestibular nuclei is related to monocular (right or left) eye position rather than to conjugate eye position. This surprising relationship would not have been noticed in earlier studies that measured the movements of only one eye (using a single eye coil) or that measured only the conjugate movements of the two eyes (using bitemporal EOG electrodes). How general a feature of oculomotor signal processing is this finding? In this paper, we re-examine the eye position signal in abducens and oculomotor neurons when the movements of the two eyes are conjugate and when they are disjunctive and therefore disassociated. The data suggest that abducens neurons (AMNs and AINs) and oculomotor neurons (putative medial rectus motoneurons), unlike PVP cells, are not monocular but encode mixtures of right and left eye position signals.

Receptive field dynamics underlying MST neuronal optic flow selectivity.

Optic flow informs moving observers about their heading direction. Neurons in monkey medial superior temporal (MST) cortex show heading selective responses to optic flow and planar direction selective responses to patches of local motion. We recorded MST neuronal responses to a 90 x 90 degrees optic flow display and to a 3 x 3 array of local motion patches covering the same area. Our goal was to test the hypothesis that the optic flow responses reflect the sum of the local motion responses. The local motion responses of each neuron were modeled as mixtures of Gaussians, combining the effects of two Gaussian response functions derived using a genetic algorithm, and then used to predict that neurons optic flow responses. Some neurons showed good correspondence between local motion models and optic flow responses, others showed substantial differences. We used the genetic algorithm to modulate the relative strength of each local motion segments responses to accommodate interactions between segments that might modulate their relative efficacy during co-activation by global patterns of optic flow. These gain modulated models showed uniformly better fits to the optic flow responses, suggesting that coactivation of receptive field segments alters neuronal response properties. We tested this hypothesis by simultaneously presenting local motion stimuli at two different sites. These two-segment stimuli revealed that interactions between response segments have direction and location specific effects that can account for aspects of optic flow selectivity. We conclude that MSTs optic flow selectivity reflects dynamic interactions between spatially distributed local planar motion response mechanisms.

Driving strategy alters neuronal responses to self-movement: cortical mechanisms of distracted driving

We presented naturalistic combinations of virtual self-movement stimuli while recording neuronal activity in monkey cerebral cortex. Monkeys used a joystick to drive to a straight ahead heading direction guided by either object motion or optic flow. The selected cue dominates neuronal responses, often mimicking responses evoked when that stimulus is presented alone. In some neurons, driving strategy creates selective response additivities. In others, it creates vulnerabilities to the disruptive effects of independently moving objects. Such cue interactions may be related to the disruptive effects of independently moving objects in Alzheimers disease patients with navigational deficits.

Cortical Neurons Combine Visual Cues about Self-Movement

Visual cues about self-movement are derived from the patterns of optic flow and the relative motion of discrete objects. We recorded dorsal medial superior temporal (MSTd) cortical neurons in monkeys that held centered visual fixation while viewing optic flow and object motion stimuli simulating the self-movement cues seen during translation on a circular path. Twenty stimulus configurations presented naturalistic combinations of optic flow with superimposed objects that simulated either earth-fixed landmark objects or independently moving animate objects. Landmarks and animate objects yield the same response interactions with optic flow; mainly additive effects, with a substantial number of sub- and super-additive responses. Sub- and super-additive interactions reflect each neuron’s local and global motion sensitivities: Local motion sensitivity is based on the spatial arrangement of directions created by object motion and the surrounding optic flow. Global motion sensitivity is based on the temporal sequence of self-movement headings that define a simulated path through the environment. We conclude that MST neurons’ spatio-temporal response properties combine object motion and optic flow cues to represent self-movement in diverse, naturalistic circumstances.

Navigational path integration by cortical neurons: origins in higher-order direction selectivity

Navigation relies on the neural processing of sensory cues about observer self-movement and spatial location. Neurons in macaque dorsal medial superior temporal cortex (MSTd) respond to visual and vestibular self-movement cues, potentially contributing to navigation and orientation. We moved monkeys on circular paths around a room while recording the activity of MSTd neurons. MSTd neurons show a variety of sensitivities to the monkeys heading direction, circular path through the room, and place in the room. Changing visual cues alters the relative prevalence of those response properties. Disrupting the continuity of self-movement paths through the environment disrupts path selectivity in a manner linked to the time course of single neuron responses. We hypothesize that sensory cues interact with the spatial and temporal integrative properties of MSTd neurons to derive path selectivity for navigational path integration supporting spatial orientation.

Optic flow and vestibular self-movement cues: multi-sensory interactions in cortical area MST

An efficient observer must optimize the use of sensory signals about self-movement. Optimization includes adaptation to the varying availability of cues in the range of environments that are encountered. Because vision dominates sensation in primates, the critical distinction in self-movement environments is that between self-movement in darkness and in light.

Path perturbation detection tasks reduce MSTd neuronal self-movement heading responses

We presented optic flow and real movement heading stimuli while recording MSTd neuronal activity. Monkeys were alternately engaged in three tasks: visual detection of optic flow heading perturbations, vestibular detection of real movement heading perturbations, and auditory detection of brief tones. Push-button RTs were fastest for tones and slower for visual and vestibular heading perturbations, suggesting that the tone detection task was easier. Neuronal heading selectivity was strongest during the tone detection task, and weaker during the visual and vestibular heading perturbation detection tasks. Heading selectivity was weaker during visual and vestibular path perturbation detection, despite our presented heading cues only in the visual and vestibular modalities. We conclude that focusing on the self-movement transients of path perturbation distracted the monkeys from their heading and reduced neuronal responsiveness to heading direction. NEW & NOTEWORTHY Heading analysis is critical for steering and navigation. We recorded the activity of monkey cortical heading neurons during naturalistic self-movement. When the monkeys were required to respond to transient changes in their path, neuronal responses to heading direction were diminished. This suggests that the need to respond to momentary path perturbations reduces your ability to process your heading direction.

Computational model of cortical neuronal receptive fields for self-motion perception

Biologically inspired approaches are an alternative to conventional engineering approaches when developing complex algorithms for intelligent systems. In this paper, we present a novel approach to the computational modeling of primate cortical neurons in the dorsal medial superior temporal area (MSTd). Our approach is based-on a spatially distributed mixture of Gaussians, where MSTs primary function is detecting self-motion from optic flow stimulus. Each biological neuron was modeled using a genetic algorithm to determine the parameters of the mixture of Gaussians, resulting in firing rate responses that accurately match the observed responses of the corresponding biological neurons. We also present the possibility of applying the trained models to machine vision as part of a simple dorsal stream processing model for self-motion detection, which has applications to motion analysis and unmanned vehicle navigation.