MSTd Neurons Research Articles

Tuning Properties of MT and MSTd and Divisive Interactions for Eye-Movement Compensation.

The primate brain intelligently processes visual information from the world as the eyes move constantly. The brain must take into account visual motion induced by eye movements, so that visual information about the outside world can be recovered. Certain neurons in the dorsal part of monkey medial superior temporal area (MSTd) play an important role in integrating information about eye movements and visual motion. When a monkey tracks a moving target with its eyes, these neurons respond to visual motion as well as to smooth pursuit eye movements. Furthermore, the responses of some MSTd neurons to the motion of objects in the world are very similar during pursuit and during fixation, even though the visual information on the retina is altered by the pursuit eye movement. We call these neurons compensatory pursuit neurons. In this study we develop a computational model of MSTd compensatory pursuit neurons based on physiological data from single unit studies. Our model MSTd neurons can simulate the velocity tuning of monkey MSTd neurons. The model MSTd neurons also show the pursuit compensation property. We find that pursuit compensation can be achieved by divisive interaction between signals coding eye movements and signals coding visual motion. The model generates two implications that can be tested in future experiments: (1) compensatory pursuit neurons in MSTd should have the same direction preference for pursuit and retinal visual motion; (2) there should be non-compensatory pursuit neurons that show opposite preferred directions of pursuit and retinal visual motion.

Saccade-induced image motion cannot account for post-saccadic enhancement of visual processing in primate MST.

Primates use saccadic eye movements to make gaze changes. In many visual areas, including the dorsal medial superior temporal area (MSTd) of macaques, neural responses to visual stimuli are reduced during saccades but enhanced afterwards. How does this enhancement arise—from an internal mechanism associated with saccade generation or through visual mechanisms activated by the saccade sweeping the image of the visual scene across the retina? Spontaneous activity in MSTd is elevated even after saccades made in darkness, suggesting a central mechanism for post-saccadic enhancement. However, based on the timing of this effect, it may arise from a different mechanism than occurs in normal vision. Like neural responses in MSTd, initial ocular following eye speed is enhanced after saccades, with evidence suggesting both internal and visually mediated mechanisms. Here we recorded from visual neurons in MSTd and measured responses to motion stimuli presented soon after saccades and soon after simulated saccades—saccade-like displacements of the background image during fixation. We found that neural responses in MSTd were enhanced when preceded by real saccades but not when preceded by simulated saccades. Furthermore, we also observed enhancement following real saccades made across a blank screen that generated no motion signal within the recorded neurons' receptive fields. We conclude that in MSTd the mechanism leading to post-saccadic enhancement has internal origins.

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

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.

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 monkey's 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.

Contribution of correlated noise and selective decoding to choice probability measurements in extrastriate visual cortex.

Trial by trial covariations between neural activity and perceptual decisions (quantified by choice Probability, CP) have been used to probe the contribution of sensory neurons to perceptual decisions. CPs are thought to be determined by both selective decoding of neural activity and by the structure of correlated noise among neurons, but the respective roles of these factors in creating CPs have been controversial. We used biologically-constrained simulations to explore this issue, taking advantage of a peculiar pattern of CPs exhibited by multisensory neurons in area MSTd that represent self-motion. Although models that relied on correlated noise or selective decoding could both account for the peculiar pattern of CPs, predictions of the selective decoding model were substantially more consistent with various features of the neural and behavioral data. While correlated noise is essential to observe CPs, our findings suggest that selective decoding of neuronal signals also plays important roles.

Spiral motion selective neurons in area MSTd contribute to judgments of heading

Self-motion generates patterns of optic flow on the retina. Neurons in the dorsal part of the medial superior temporal area (MSTd) are selective for these optic flow patterns. It has been shown that neurons in this area that are selective for expanding optic flow fields are involved in heading judgments. We wondered how subpopulations of MSTd neurons, those tuned for expansion, rotation or spiral motion, contribute to heading perception. To investigate this question, we recorded from neurons in area MSTd with diverse tuning properties, while the animals performed a heading-discrimination task. We found a significant trial-to-trial correlation (choice probability) between the MSTd neurons and the animals' decision. Neurons in different subpopulations did not differ significantly in terms of their choice probability. Instead, choice probability was strongly related to the sensitivity of the neuron in our sample, regardless of tuning preference. We conclude that a variety of subpopulations of MSTd neurons with different tuning properties contribute to heading judgments.

Eye Velocity Gain Fields in MSTd During Optokinetic Stimulation

Lesion studies argue for an involvement of cortical area dorsal medial superior temporal area (MSTd) in the control of optokinetic response (OKR) eye movements to planar visual stimulation. Neural recordings during OKR suggested that MSTd neurons directly encode stimulus velocity. On the other hand, studies using radial visual flow together with voluntary smooth pursuit eye movements showed that visual motion responses were modulated by eye movement-related signals. Here, we investigated neural responses in MSTd during continuous optokinetic stimulation using an information-theoretic approach for characterizing neural tuning with high resolution. We show that the majority of MSTd neurons exhibit gain-field-like tuning functions rather than directly encoding one variable. Neural responses showed a large diversity of tuning to combinations of retinal and extraretinal input. Eye velocity-related activity was observed prior to the actual eye movements, reflecting an efference copy. The observed tuning functions resembled those emerging in a network model trained to perform summation of 2 population-coded signals. Together, our findings support the hypothesis that MSTd implements the visuomotor transformation from retinal to head-centered stimulus velocity signals for the control of OKR.

A Unified Model of Heading and Path Perception in Primate MSTd

Self-motion, steering, and obstacle avoidance during navigation in the real world require humans to travel along curved paths. Many perceptual models have been proposed that focus on heading, which specifies the direction of travel along straight paths, but not on path curvature, which humans accurately perceive and is critical to everyday locomotion. In primates, including humans, dorsal medial superior temporal area (MSTd) has been implicated in heading perception. However, the majority of MSTd neurons respond optimally to spiral patterns, rather than to the radial expansion patterns associated with heading. No existing theory of curved path perception explains the neural mechanisms by which humans accurately assess path and no functional role for spiral-tuned cells has yet been proposed. Here we present a computational model that demonstrates how the continuum of observed cells (radial to circular) in MSTd can simultaneously code curvature and heading across the neural population. Curvature is encoded through the spirality of the most active cell, and heading is encoded through the visuotopic location of the center of the most active cell's receptive field. Model curvature and heading errors fit those made by humans. Our model challenges the view that the function of MSTd is heading estimation, based on our analysis we claim that it is primarily concerned with trajectory estimation and the simultaneous representation of both curvature and heading. In our model, temporal dynamics afford time-history in the neural representation of optic flow, which may modulate its structure. This has far-reaching implications for the interpretation of studies that assume that optic flow is, and should be, represented as an instantaneous vector field. Our results suggest that spiral motion patterns that emerge in spatio-temporal optic flow are essential for guiding self-motion along complex trajectories, and that cells in MSTd are specifically tuned to extract complex trajectory estimation from flow.

Diverse Spatial Reference Frames of Vestibular Signals in Parietal Cortex

Reference frames are important for understanding how sensory cues from different modalities are coordinated to guide behavior, and the parietal cortex is critical to these functions. We compare reference frames of vestibular self-motion signals in the ventral intraparietal area (VIP), parietoinsular vestibular cortex (PIVC), and dorsal medial superior temporal area (MSTd). Vestibular heading tuning in VIP is invariant to changes in both eye and head positions, indicating a body (or world)-centered reference frame. Vestibular signals in PIVC have reference frames that are intermediate between head and body centered. In contrast, MSTd neurons show reference frames between head and eye centered but not body centered. Eye and head position gain fields were strongest in MSTd and weakest in PIVC. Our findings reveal distinct spatial reference frames for representing vestibular signals and pose new challenges for understanding the respective roles of these areas in potentially diverse vestibular functions.

Linking sensory neurons to visually guided behavior: relating MST activity to steering in a virtual environment.

Many complex behaviors rely on guidance from sensations. To perform these behaviors, the motor system must decode information relevant to the task from the sensory system. However, identifying the neurons responsible for encoding the appropriate sensory information remains a difficult problem for neurophysiologists. A key step toward identifying candidate systems is finding neurons or groups of neurons capable of representing the stimuli adequately to support behavior. A traditional approach involves quantitatively measuring the performance of single neurons and comparing this to the performance of the animal. One of the strongest pieces of evidence in support of a neuronal population being involved in a behavioral task comes from the signals being sufficient to support behavior. Numerous experiments using perceptual decision tasks show that visual cortical neurons in many areas have this property. However, most visually guided behaviors are not categorical but continuous and dynamic. In this article, we review the concept of sufficiency and the tools used to measure neural and behavioral performance. We show how concepts from information theory can be used to measure the ongoing performance of both neurons and animal behavior. Finally, we apply these tools to dorsal medial superior temporal (MSTd) neurons and demonstrate that these neurons can represent stimuli important to navigation to a distant goal. We find that MSTd neurons represent ongoing steering error in a virtual-reality steering task. Although most individual neurons were insufficient to support the behavior, some very nearly matched the animal's estimation performance. These results are consistent with many results from perceptual experiments and in line with the predictions of Mountcastle's "lower envelope principle."

Spatiotemporal Properties of Optic Flow and Vestibular Tuning in the Cerebellar Nodulus and Uvula

Convergence of visual motion and vestibular information is essential for accurate spatial navigation. Such multisensory integration has been shown in cortex, e.g., the dorsal medial superior temporal (MSTd) and ventral intraparietal (VIP) areas, but not in the parieto-insular vestibular cortex (PIVC). Whether similar convergence occurs subcortically remains unknown. Many Purkinje cells in vermal lobules 10 (nodulus) and 9 (uvula) of the macaque cerebellum are tuned to vestibular translation stimuli, yet little is known about their visual motion responsiveness. Here we show the existence of translational optic flow-tuned Purkinje cells, found exclusively in the anterior part of the nodulus and ventral uvula, near the midline. Vestibular responses of Purkinje cells showed a remarkable similarity to those in MSTd (but not PIVC or VIP) neurons, in terms of both response latency and relative contributions of velocity, acceleration, and position components. In contrast, the spatiotemporal properties of optic flow responses differed from those in MSTd, and matched the vestibular properties of these neurons. Compared with MSTd, optic flow responses of Purkinje cells showed smaller velocity contributions and larger visual motion acceleration responses. The remarkable similarity between the nodulus/uvula and MSTd vestibular translation responsiveness suggests a functional coupling between the two areas for vestibular processing of self-motion information.

Functional specializations of the ventral intraparietal area for multisensory heading discrimination.

The ventral intraparietal area (VIP) of the macaque brain is a multimodal cortical region with directionally selective responses to visual and vestibular stimuli. To explore how these signals contribute to self-motion perception, neural activity in VIP was monitored while macaques performed a fine heading discrimination task based on vestibular, visual, or multisensory cues. For neurons with congruent visual and vestibular heading tuning, discrimination thresholds improved during multisensory stimulation, suggesting that VIP (like the medial superior temporal area; MSTd) may contribute to the improved perceptual discrimination seen during cue combination. Unlike MSTd, however, few VIP neurons showed opposite visual/vestibular tuning over the range of headings relevant to behavior, and those few cells showed reduced sensitivity under cue combination. Our data suggest that the heading tuning of some VIP neurons may be locally remodeled to increase the proportion of cells with congruent tuning over the behaviorally relevant stimulus range. VIP neurons also showed much stronger trial-by-trial correlations with perceptual decisions (choice probabilities; CPs) than MSTd neurons. While this may suggest that VIP neurons are more strongly linked to heading perception, we also find that correlated noise is much stronger among pairs of VIP neurons, with noise correlations averaging 0.14 in VIP as compared with 0.04 in MSTd. Thus, the large CPs in VIP could be a consequence of strong interneuronal correlations. Together, our findings suggest that VIP neurons show specializations that may make them well equipped to play a role in multisensory integration for heading perception.

Task contingencies and perceptual strategies shape behavioral effects on neuronal response profiles

We presented optic flow simulating eight directions of self-movement in the ground plane, while monkeys performed delayed match-to-sample tasks, and we recorded dorsal medial superior temporal (MSTd) neuronal activity. Randomly selected sample headings yield smaller test responses to the neuron's preferred heading when it is near the sample's heading direction and larger test responses to the preferred heading when it is far from the sample's heading. Limiting test stimuli to matching or opposite headings suppresses responses to preferred stimuli in both test conditions, whereas focusing on each neuron's preferred vs. antipreferred stimuli enhances responses to the antipreferred stimulus. Match vs. opposite paradigms create bimodal heading profiles shaped by interactions with late delay-period activity. We conclude that task contingencies, determining the prior probabilities of specific stimuli, interact with the monkeys' perceptual strategy for optic flow analysis. These influences shape attentional and working memory effects on the heading direction selectivities and preferences of MSTd neurons.

Recurrent competition explains temporal effects of attention in MSTd

Navigation in a static environment along straight paths without eye movements produces radial optic flow fields. A singularity called the focus of expansion (FoE) specifies the direction of travel (heading) of the observer. Cells in primate visual area MSTd respond to radial fields and are therefore thought to be heading-sensitive. Humans frequently shift their focus of attention while navigating, for example, depending on the favorable or threatening context of approaching independently moving objects. Recent neurophysiological studies show that the spatial tuning curves of primate MSTd neurons change based on the difference in visual angle between an attentional prime and the FoE. Moreover, the peak mean population activity in MSTd retreats linearly in time as the distance between the attentional prime and FoE increases. We present a dynamical neural circuit model that demonstrates the same linear temporal peak shift observed electrophysiologically. The model qualitatively matches the neuron tuning curves and population activation profiles. After model MT dynamically pools short-range motion, model MSTd incorporates recurrent competition between units tuned to different radial optic flow templates, and integrates attentional signals from model area FEF. In the model, population activity peaks occur when the recurrent competition is most active and uncertainty is greatest about the relative position of the FoE. The nature of attention, multiplicative or non-multiplicative, is largely irrelevant, so long as attention has a Gaussian-like profile. Using an appropriately tuned sigmoidal signal function to modulate recurrent feedback affords qualitative fits of deflections in the population activity that otherwise appear to be low-frequency noise. We predict that these deflections mark changes in the balance of attention between the priming and FoE locations.

Neuronal Variability of MSTd Neurons Changes Differentially With Eye Movement and Visually Related Variables

Neurons in macaque cortical area MSTd are driven by visual motion and eye movement related signals. This multimodal characteristic makes MSTd an ideal system for studying the dependence of neuronal activity on different variables. Here, we analyzed the temporal structure of spiking patterns during visual motion stimulation using 2 distinct behavioral paradigms: fixation (FIX) and optokinetic response. For the FIX condition, inter- and intra-trial variability of spiking activity decreased with increasing stimulus strength, complying with a recent neurophysiological study reporting stimulus-related decline of neuronal variability. In contrast, for the optokinetic condition variability increased together with increasing eye velocity while retinal image velocity remained low. Analysis of stimulus signal variability revealed a correlation between the normalized variance of image velocity and neuronal variability, but no correlation with normalized eye velocity variance. We further show that the observed difference in neuronal variability allows classifying spike trains according to the paradigm used, even when mean firing rates (FRs) were similar. The stimulus-dependence of neuronal variability may result from the local network structure and/or the variability characteristics of the input signals, but may also reflect additional timing-based mechanisms independent of the neuron's mean FR and related to the modality driving the neuron.

Causal Links between Dorsal Medial Superior Temporal Area Neurons and Multisensory Heading Perception

The dorsal medial superior temporal area (MSTd) in the extrastriate visual cortex is thought to play an important role in heading perception because neurons in this area are tuned to both optic flow and vestibular signals. MSTd neurons also show significant correlations with perceptual judgments during a fine heading direction discrimination task. To test for a causal link with heading perception, we used microstimulation and reversible inactivation techniques to artificially perturb MSTd activity while monitoring behavioral performance. Electrical microstimulation significantly biased monkeys' heading percepts based on optic flow, but did not significantly impact vestibular heading judgments. The latter result may be due to the fact that vestibular heading preferences in MSTd are more weakly clustered than visual preferences and multiunit tuning for vestibular stimuli is weak. Reversible chemical inactivation, however, increased behavioral thresholds when heading judgments were based on either optic flow or vestibular cues, although the magnitude of the effects was substantially stronger for optic flow. Behavioral deficits in a combined visual/vestibular stimulus condition were intermediate between the single-cue effects. Despite deficits in discrimination thresholds, animals were able to combine visual and vestibular cues near optimally, even after large bilateral muscimol injections into MSTd. Simulations show that the overall pattern of results following inactivation is consistent with a mixture of contributions from MSTd and other areas with vestibular-dominant tuning for heading. Our results support a causal link between MSTd neurons and multisensory heading perception but suggest that other multisensory brain areas also contribute.

Recurrent competition explains temporal effects of attention in MSTd

Navigation in a static environment along straight paths without eye movements produces radial optic flow fields. A singularity called the focus of expansion (FoE) specifies the direction of travel (heading) of the observer. Cells in primate dorsal medial superior temporal area (MSTd) respond to radial fields and are therefore thought to be heading-sensitive. Humans frequently shift their focus of attention while navigating, for example, depending on the favorable or threatening context of approaching independently moving objects. Recent neurophysiological studies show that the spatial tuning curves of primate MSTd neurons change based on the difference in visual angle between an attentional prime and the FoE. Moreover, the peak mean population activity in MSTd retreats linearly in time as the distance between the attentional prime and FoE increases. We present a dynamical neural circuit model that demonstrates the same linear temporal peak shift observed electrophysiologically. The model qualitatively matches the neuron tuning curves and population activation profiles. After model MT dynamically pools short-range motion, model MSTd incorporates recurrent competition between units tuned to different radial optic flow templates, and integrates attentional signals from model area frontal eye fields (FEF). In the model, population activity peaks occur when the recurrent competition is most active and uncertainty is greatest about the relative position of the FoE. The nature of attention, multiplicative or non-multiplicative, is largely irrelevant, so long as attention has a Gaussian-like profile. Using an appropriately tuned sigmoidal signal function to modulate recurrent feedback affords qualitative fits of deflections in the population activity that otherwise appear to be low-frequency noise. We predict that these deflections mark changes in the balance of attention between the priming and FoE locations.

Binocular Disparity Tuning and Visual–Vestibular Congruency of Multisensory Neurons in Macaque Parietal Cortex

Many neurons in the dorsal medial superior temporal (MSTd) and ventral intraparietal (VIP) areas of the macaque brain are multisensory, responding to both optic flow and vestibular cues to self-motion. The heading tuning of visual and vestibular responses can be either congruent or opposite, but only congruent cells have been implicated in cue integration for heading perception. Because of the geometric properties of motion parallax, however, both congruent and opposite cells could be involved in coding self-motion when observers fixate a world-fixed target during translation, if congruent cells prefer near disparities and opposite cells prefer far disparities. We characterized the binocular disparity selectivity and heading tuning of MSTd and VIP cells using random-dot stimuli. Most (70%) MSTd neurons were disparity selective with monotonic tuning, and there was no consistent relationship between depth preference and congruency of visual and vestibular heading tuning. One-third of disparity-selective MSTd cells reversed their depth preference for opposite directions of motion [direction-dependent disparity tuning (DDD)], but most of these cells were unisensory with no tuning for vestibular stimuli. Inconsistent with previous reports, the direction preferences of most DDD neurons do not reverse with disparity. By comparison to MSTd, VIP contains fewer disparity-selective neurons (41%) and very few DDD cells. On average, VIP neurons also preferred higher speeds and nearer disparities than MSTd cells. Our findings are inconsistent with the hypothesis that visual/vestibular congruency is linked to depth preference, and also suggest that DDD cells are not involved in multisensory integration for heading perception.

Neuronal activity in medial superior temporal area (MST) during memory-based smooth pursuit eye movements in monkeys

We examined recently neuronal substrates for predictive pursuit using a memory-based smooth pursuit task that distinguishes the discharge related to memory of visual motion-direction from that related to movement preparation. We found that the supplementary eye fields (SEF) contain separate signals coding memory and assessment of visual motion-direction, decision not-to-pursue, and preparation for pursuit. Since medial superior temporal area (MST) is essential for visual motion processing and projects to SEF, we examined whether MST carried similar signals. We analyzed the discharge of 108 MSTd neurons responding to visual motion stimuli. The majority (69/108 = 64%) were also modulated during smooth pursuit. However, in nearly all (104/108 = 96%) of the MSTd neurons tested, there was no significant discharge modulation during the delay periods that required memory of visual motion-direction or preparation for smooth pursuit or not-to-pursue. Only 4 neurons of the 108 (4%) exhibited significantly higher discharge rates during the delay periods; however, their responses were non-directional and not instruction specific. Representative signals in the MSTd clearly differed from those in the SEF during memory-based smooth pursuit. MSTd neurons are unlikely to provide signals for memory of visual motion-direction or preparation for smooth pursuit eye movements.

Role of MSTd Extraretinal Signals in Smooth Pursuit Adaptation

The smooth pursuit (SP) system is able to adapt to challenges associated with development or system drift to maintain pursuit accuracy. Short-term adaptation of SP can be produced experimentally using a step-ramp tracking paradigm with 2 steps of velocity (double-step paradigm). Previous studies have demonstrated that the macaque cerebellum plays an essential role in SP adaptation. However, it remains uncertain whether neuronal activity in afferent structures to the cerebellum shows changes associated with SP adaptation. Therefore, we focused on the dorsal-medial part of medial superior temporal cortex (MSTd), which is part of the cortico-ponto-cerebellar pathway thought to provide extraretinal signals needed for maintaining SP. We found that 54% of the SP-related neurons showed significant changes in the first 100 ms of response correlated with adaptive changes of initial pursuit. Our results indicate that some cortical neurons in MSTd could be inside the circuit involved in SP adaptation. Furthermore, our sample of MSTd neurons started their discharge on average 103 ms after SP onset. Therefore, we suggest that extraretinal signals carried in MSTd might be due to efference copy of pursuit eye velocity signals, which reflect plastic changes in the downstream motor output pathways (e.g., the cerebellum).