Retinal Stabilization Reveals Limited Influence of Extraretinal Signals on Heading Tuning in the Medial Superior Temporal Area.

Heading perception in primates depends heavily on visual optic-flow cues. Yet during self-motion, heading percepts remain stable, even though smooth-pursuit eye movements often distort optic flow. According to theoretical work, self-motion can be represented accurately by compensating for these distortions in two ways: via retinal mechanisms or via extraretinal efference-copy signals, which predict the sensory consequences of movement. Psychophysical evidence strongly supports the efference-copy hypothesis, but physiological evidence remains inconclusive. Neurons that signal the true heading direction during pursuit are found in visual areas of monkey cortex, including the dorsal medial superior temporal area (MSTd). Here we measured heading tuning in MSTd using a novel stimulus paradigm, in which we stabilize the optic-flow stimulus on the retina during pursuit. This approach isolates the effects on neuronal heading preferences of extraretinal signals, which remain active while the retinal stimulus is prevented from changing. Our results from 3 female monkeys demonstrate a significant but small influence of extraretinal signals on the preferred heading directions of MSTd neurons. Under our stimulus conditions, which are rich in retinal cues, we find that retinal mechanisms dominate physiological corrections for pursuit eye movements, suggesting that extraretinal cues, such as predictive efference-copy mechanisms, have a limited role under naturalistic conditions.SIGNIFICANCE STATEMENT Sensory systems discount stimulation caused by an animal's own behavior. For example, eye movements cause irrelevant retinal signals that could interfere with motion perception. The visual system compensates for such self-generated motion, but how this happens is unclear. Two theoretical possibilities are a purely visual calculation or one using an internal signal of eye movements to compensate for their effects. The latter can be isolated by experimentally stabilizing the image on a moving retina, but this approach has never been adopted to study motion physiology. Using this method, we find that extraretinal signals have little influence on activity in visual cortex, whereas visually based corrections for ongoing eye movements have stronger effects and are likely most important under real-world conditions.

Context-dependence of deterministic and nondeterministic contributions to closed-loop steering control.

In natural circumstances, sensory systems operate in a closed loop with motor output, whereby actions shape subsequent sensory experiences. A prime example of this is the sensorimotor processing required to align one's direction of travel, or heading, with one's goal, a behavior we refer to as steering. In steering, motor outputs work to eliminate errors between the direction of heading and the goal, modifying subsequent errors in the process. The closed-loop nature of the behavior makes it challenging to determine how deterministic and nondeterministic processes contribute to behavior. We overcome this by applying a nonparametric, linear kernel-based analysis to behavioral data of monkeys steering through a virtual environment in two experimental contexts. In a given context, the results were consistent with previous work that described the transformation as a second-order linear system. Classically, the parameters of such second-order models are associated with physical properties of the limb such as viscosity and stiffness that are commonly assumed to be approximately constant. By contrast, we found that the fit kernels differed strongly across tasks in these and other parameters, suggesting context-dependent changes in neural and biomechanical processes. We additionally fit residuals to a simple noise model and found that the form of the noise was highly conserved across both contexts and animals. Strikingly, the fitted noise also closely matched that found previously in a human steering task. Altogether, this work presents a kernel-based analysis that characterizes the context-dependence of deterministic and non-deterministic components of a closed-loop sensorimotor task.

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."

Parietal area VIP causally influences heading perception during pursuit eye movements.

The ventral intraparietal area (VIP) of the macaque monkey brain is a multimodal area with visual, vestibular, somatosensory, and eye movement-related responses. The visual responses are strongly directional, and VIP neurons respond well to complex optic flow patterns similar to those found during self-motion. To test the hypothesis that visual responses in VIP directly contribute to the perception of self-motion direction, we used electrical microstimulation to perturb activity in VIP while animals performed a two-alternative heading discrimination task. Microstimulation systematically biased monkeys' choices in a direction consistent with neuronal preferences at the stimulation site, and these effects were larger while the animal was making smooth pursuit eye movements. From these results, we conclude that VIP is causally involved in the perception of self-motion from visual cues and that this involvement is gated by ongoing motor behavior.

The responses of VIP neurons are sufficiently sensitive to support heading judgments.

The ventral intraparietal area (VIP) of the macaque monkey is thought to be involved in judging heading direction based on optic flow. We recorded neuronal discharges in VIP while monkeys were performing a two-alternative, forced-choice heading discrimination task to relate quantitatively the activity of VIP neurons to monkeys' perceptual choices. Most VIP neurons were responsive to simulated heading stimuli and were tuned such that their responses changed across a range of forward trajectories. Using receiver operating characteristic (ROC) analysis, we found that most VIP neurons were less sensitive to small heading changes than was the monkey, although a minority of neurons were equally sensitive. Pursuit eye movements modestly yet significantly increased both neuronal and behavioral thresholds by approximately the same amount. Our results support the view that VIP activity is involved in self-motion judgments.

Extrastriate area MST and parietal area VIP similarly represent forward headings.

Many studies have documented the involvement of medial superior temporal extrastriate area (MST) in the perception of heading based on optic flow information. Furthermore, both heading perception and the responses of MST neurons are relatively stable in the presence of eye movements that distort the retinal flow information on which perception is based. Area VIP in the posterior parietal cortex also contains a robust representation of optic flow cues for heading. However, the studies in the two areas were frequently conducted using different stimuli, making quantitative comparison difficult. To remedy this, we studied MST using a family of random dot heading stimuli that we have previously used in the study of VIP. These stimuli simulate observer translation through a three-dimensional cloud of points, and a range of forward headings was presented both with and without horizontal smooth pursuit eye movements. We found that MST neurons, like VIP neurons, respond robustly to these stimuli and partially compensate for the presence of pursuit. Quantitative comparison of the responses revealed no substantial difference between the heading responses of MST and VIP neurons or in their degree of pursuit tolerance.

Parietal area VIP neuronal responses to heading stimuli are encoded in head-centered coordinates.

The ventral intraparietal area (VIP) is a multimodal parietal area, where visual responses are brisk, directional, and typically selective for complex optic flow patterns. VIP thus could provide signals useful for visual estimation of heading (self-motion direction). A central problem in heading estimation is how observers compensate for eye velocity, which distorts the retinal motion cues upon which perception depends. To find out if VIP could be useful for heading, we measured its responses to simulated trajectories, both with and without eye movements. Our results showed that most VIP neurons very strongly signal heading direction. Furthermore, the tuning of most VIP neurons was remarkably stable in the presence of eye movements. This stability was such that the population of VIP neurons represented heading very nearly in head-centered coordinates. This makes VIP the most robust source of such signals yet described, with properties ideal for supporting perception.

Zebras and Biting Flies: Quantitative Analysis of Reflected Light from Zebra Coats in Their Natural Habitat.

Experimental and comparative evidence suggests that the striped coats of zebras deter biting fly attack, but the mechanisms by which flies fail to target black-and-white mammals are still opaque. Two hypotheses have been proposed: stripes might serve either to defeat polarotaxis or to obscure the form of the animal. To test these hypotheses, we systematically photographed free-living plains zebras in Africa. We found that black and white stripes both have moderate polarization signatures with a similar angle, though the degree (magnitude) of polarization in white stripes is lower. When we modeled the visibility of these signals from different distances, we found that polarization differences between stripes are invisible to flies more than 10 m away because they are averaged out by the flies' low visual resolution. At any distance, however, a positively polarotactic insect would have a distinct signal to guide its visual approach to a zebra because we found that polarization of light reflecting from zebras is higher than from surrounding dry grasses. We also found that the stripes themselves are visible to flies at somewhat greater distances (up to 20 m) than the polarization contrast between stripes. Together, these observations support hypotheses in which zebra stripes defeat visually guided orienting behavior in flies by a mechanism independent of polarotaxis.

Clustering of selectivity for optic flow in the ventral intraparietal area.

The presence of a columnar or clustered organization for some property often denotes that this property is important to the local information processing in a cortical area. To determine whether self-motion is systematically organized in the ventral intraparietal area (VIP), we made long electrode penetrations, recording both multi-unit and single-unit tuning for horizontally varying heading stimuli at frequent intervals. Single units were well correlated with the tuning of multi-unit activity at the same location and multi-unit activity was more correlated with tuning at nearby locations than it was with tuning at locations beyond approximately 0.5 mm. From this, we conclude that heading information is represented in a clustered, and possibly columnar, fashion in VIP.

Monkey steering responses reveal rapid visual-motor feedback.

The neural mechanisms underlying primate locomotion are largely unknown. While behavioral and theoretical work has provided a number of ideas of how navigation is controlled, progress will require direct physiolgical tests of the underlying mechanisms. In turn, this will require development of appropriate animal models. We trained three monkeys to track a moving visual target in a simple virtual environment, using a joystick to control their direction. The monkeys learned to quickly and accurately turn to the target, and their steering behavior was quite stereotyped and reliable. Monkeys typically responded to abrupt steps of target direction with a biphasic steering movement, exhibiting modest but transient overshoot. Response latencies averaged approximately 300 ms, and monkeys were typically back on target after about 1 s. We also exploited the variability of responses about the mean to explore the time-course of correlation between target direction and steering response. This analysis revealed a broad peak of correlation spanning approximately 400 ms in the recent past, during which steering errors provoke a compensatory response. This suggests a continuous, visual-motor loop controls steering behavior, even during the epoch surrounding transient inputs. Many results from the human literature also suggest that steering is controlled by such a closed loop. The similarity of our results to those in humans suggests the monkey is a very good animal model for human visually guided steering.

Mechanisms of self-motion perception.

Guiding effective movement through the environment is one of the visual system's most important functions. The pattern of motion that we see allows us to estimate our heading accurately in a variety of environments, despite the added difficulty imposed by our own eye and head movements. The cortical substrates for heading perception include the medial superior temporal area (MST) and the ventral intraparietal area (VIP). This review discusses recent work on these two areas in the context of behavioral observations that establish the important problems the visual system must solve. Signals relevant to self motion are both more widespread than heretofore recognized and also more complex because they are multiplexed with other sensory signals, such as vestibular, auditory, and tactile information. The review presents recent work as a background to highlight important problems that remain unsolved.

Linear responses to stochastic motion signals in area MST.

The medial superior temporal (MST) area contains neurons with tuning for complex motion patterns, but very little is known about the generation of such responses. To explore how neuronal responses varied across complex motion pattern coherence, we recorded from single units while varying the strength of the global motion pattern in random dot stimuli. Stimuli were a family of optic flow patterns, consisting of radial motion, rotary motion, or combinations thereof ("spiral space"). We controlled the strength of the motion in the stimuli by varying the coherence--the proportion of dots carrying the signal. This allows motion strength to be varied independently of stimulus size, speed, or contrast. Most neurons' responses were well described as a linear function of stimulus coherence. Although more than half the cells possessed significant nonlinearities, these typically accounted for little additional variance. Nonlinear coherence response functions could either be compressive (e.g., saturating) or expansive and occurred in both the preferred and null direction responses. The presence of nonlinearities was not related to neuronal response properties such as preferred spiral-space direction or tuning bandwidth; however, cells with compressive nonlinearities in both the preferred and null directions tended to have higher response amplitudes and were more sensitive to weak motion signals. These cells did not appear to form a distinct subpopulation within MST. Our results suggest that MST neurons predominantly linearly encode increasing pattern motion energy within their RFs.

Contrast dependence of response normalization in area MT of the rhesus macaque.

Contrast normalization is a process whereby responses of neurons are scaled according to the total amount of contrast in a region of the image nearby the receptive field of a neuron. This process allows neurons to code for informative scene or object attributes in a manner unaffected by changes in illumination. Evidence for normalization is seen in striate and extrastriate cortex from experiments where multiple stimuli are presented with a single receptive field (RF). Neuronal responses in such experiments are smaller than that predicted by linear summation, revealing the presence of normalization. While the presence of normalization is often clear, its mechanism is less so. To study the mechanism of normalization, we measured the interaction between pairs of brief local stimuli (spatial Gabor functions) within the RFs of cells in the middle temporal (MT or V5) area of monkeys and varied both the location and contrast of the stimuli. We found response summed approximately linearly when contrast was low but rapidly became normalized as stimulus contrast increased. The rapid transition to effective normalization at low contrasts suggested cooperativity in the normalization, and a model embodying such a cooperative step provided a good account of our data.

Optic flow signals in extrastriate area MST: comparison of perceptual and neuronal sensitivity.

The medial superior temporal area of extrastriate cortex (MST) contains signals selective for nonuniform patterns of motion often termed "optic flow." The presence of such tuning, however, does not necessarily imply involvement in perception. To quantify the relationship between these selective neuronal signals and the perception of optic flow, we designed a discrimination task that allowed us to simultaneously record neuronal and behavioral sensitivities to near-threshold optic flow stimuli tailored to MST cells' preferences. In this two-alternative forced-choice task, we controlled the salience of globally opposite patterns (e.g., expansion and contraction) by varying the coherence of the motion. Using these stimuli, we could both relate the sensitivity of neuronal signals in MST to the animal's behavioral sensitivity and also measure trial-by-trial correlation between neuronal signals and behavioral choices. Neurons in MST showed a wide range of sensitivities to these complex motion stimuli. Many neurons had sensitivities equal or superior to the monkey's threshold. On the other hand, trial-by-trial correlation between neuronal discharge and choice ("choice probability") was weak or nonexistent in our data. Together, these results lead us to conclude that MST contains sufficient information for threshold judgments of optic flow; however, the role of MST activity in optic flow discriminations may be less direct than in other visual motion tasks previously described by other laboratories.

Motion adaptation in area MT.

In many sensory systems, exposure to a prolonged stimulus causes adaptation, which tends to reduce neural responses to subsequent stimuli. Such effects are usually stimulus-specific, making adaptation a powerful probe into information processing. We used dynamic random dot kinematograms to test the magnitude and selectivity of adaptation effects in the middle temporal area (MT) and to compare them to effects on human motion discrimination. After 3 s of adaptation to a random dot pattern moving in the preferred direction, MT neuronal responses to subsequent test patterns were reduced by 26% on average compared with adaptation to a static pattern. This reduction in response magnitude was largely independent of what test stimulus was presented. However, adaptation in the opposite direction changed responses less often and very inconsistently. Therefore motion adaptation systematically and profoundly affects the neurons in MT representing the adapted direction, but much less those representing the opposite direction. In human psychophysical experiments, such adapting stimuli affected direction discrimination, biasing choices away from the adaptation direction. The magnitude of this perceptual shift was consistent with the magnitude of the changes seen in area MT, if one assumes that a motion comparison step occurs after MT.

Area MST and heading perception in macaque monkeys.

The macaque medial superior temporal area (MST) is proposed to be specialized for analyzing complex 'optic flow' information. Such space-varying motion patterns provide a rich source of information about self motion, scene structure and object shape. We report the performance of rhesus macaques on a two-alternative 'heading' task, in which they reported whether horizontally varying, simulated trajectories were to left or right of center. Monkeys were sensitive to small heading angles; thresholds averaged 1.5-3 degrees. Heading estimates were stable in the face of changing stimulus location and smooth pursuit eye movements. In addition, we tested the role of area MST in heading judgements by electrically activating columns of neurons in this area while the monkeys performed the heading task. Activation of MST frequently affected performance, usually causing choice biases. These induced biases were often large and usually concordant with the preference of the neurons being activated. In addition, the induced biases were often larger in the presence of smooth pursuit eye movements. These results favor the hypothesis that MST is involved in recovering self-motion direction from optic flow cues and in the process by which heading perception is compensated for ongoing eye movements.