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.     

Neural Coding of Finger and Wrist Movements

Previous work (Schieber and Hibbard, 1993) has shown that single motor cortical neurons do not discharge specifically for a particular flexion-extension finger movement but instead are active with movements of different fingers. In addition, neuronal populations active with movements of different fingers overlap extensively in their spatial locations in the motor cortex. These data suggested that control of any finger movement utilizes a distributed population of neurons. In this study we applied the neuronal population vector analysis (Georgopoulos et al., 1983) to these same data to determine (1) whether single cells are tuned in an abstract, three-dimensional (3D) instructed finger and wrist movement space with hand-like geometry and (2) whether the neuronal population encodes specific finger movements. We found that the activity of 132/176 (75%) motor cortical neurons related to finger movements was indeed tuned in this space. Moreover, the population vector computed in this space predicted well the instructed finger movement. Thus, although single neurons may be related to several disparate finger movements, and neurons related to different finger movements are intermingled throughout the hand area of the motor cortex, the neuronal population activity does specify particular finger movements.     

Extra-retinal adaptation of cortical motion-processing areas during pursuit eye movements

Repetitive eye movement produces a compelling motion aftereffect (MAE). One mechanism thought to contribute to the illusory movement is an extra-retinal motion signal generated after adaptation. However, extra-retinal signals are also generated during pursuit. They modulate activity within cortical motion-processing area MST, helping transform retinal motion into motion in the world during an eye movement. Given the evidence that MST plays a key role in generating MAE, it may also become indirectly adapted by prolonged pursuit. To differentiate between these two extra-retinal mechanisms we examined storage of the MAE across a period of darkness. In one condition observers were told to stare at a moving pattern, an instruction that induces a more reflexive type of eye movement. In another they were told to deliberately pursue it. We found equally long MAEs when testing immediately after adaptation but not when the test was delayed by 40 s. In the case of the reflexive eye movement the delay almost completely extinguished the MAE, whereas the illusory motion following pursuit remained intact. This suggests pursuit adapts cortical motion-processing areas whereas unintentional eye movement does not. A second experiment showed that cortical mechanisms cannot be the sole determinant of pursuit-induced MAE. Following oblique pursuit, we found MAE direction changes from oblique to vertical. Perceived MAE direction appears to be influenced by a subcortical mechanism as well, one based on the relative recovery rate of horizontal and vertical eye-movement processes recruited during oblique pursuit.     

Face-infringement space: the frame of reference of the ventral intraparietal area

Experimental studies have shown that responses of ventral intraparietal area (VIP) neurons specialize in head movements and the environment near the head. VIP neurons respond to visual, auditory, and tactile stimuli, smooth pursuit eye movements, and passive and active movements of the head. This study demonstrates mathematical structure on a higher organizational level created within VIP by the integration of a complete set of variables covering face-infringement. Rather than positing dynamics in an a priori defined coordinate system such as those of physical space, we assemble neuronal receptive fields to find out what space of variables VIP neurons together cover. Section 1 presents a view of neurons as multidimensional mathematical objects. Each VIP neuron occupies or is responsive to a region in a sensorimotor phase space, thus unifying variables relevant to the disparate sensory modalities and movements. Convergence on one neuron joins variables functionally, as space and time are joined in relativistic physics to form a unified spacetime. The space of position and motion together forms a neuronal phase space, bridging neurophysiology and the physics of face-infringement. After a brief review of the experimental literature, the neuronal phase space natural to VIP is sequentially characterized, based on experimental data. Responses of neurons indicate variables that may serve as axes of neural reference frames, and neuronal responses have been so used in this study. The space of sensory and movement variables covered by VIP receptive fields joins visual and auditory space to body-bound sensory modalities: somatosensation and the inertial senses. This joining of allocentric and egocentric modalities is in keeping with the known relationship of the parietal lobe to the sense of self in space and to hemineglect, in both humans and monkeys. Following this inductive step, variables are formalized in terms of the mathematics of graph theory to deduce which combinations are complete as a multidimensional neural structure that provides the organism with a complete set of options regarding objects impacting the face, such as acceptance, pursuit, and avoidance. We consider four basic variable types: position and motion of the face and of an external object. Formalizing the four types of variables allows us to generalize to any sensory system and to determine the necessary and sufficient conditions for a neural center (for example, a cortical region) to provide a face-infringement space. We demonstrate that VIP includes at least one such face-infringement space.     

Frontal cortical control of smooth-pursuit

To maintain optimal clarity of objects moving slowly in three dimensional space, frontal eyed-primates use both smooth-pursuit and vergence (depth) eye movements to track precisely those objects and maintain their images on the foveae of left and right eyes. The caudal parts of the frontal eye fields contain neurons that discharge during smooth-pursuit. Recent results have provided a new understanding of the roles of the frontal eye field pursuit area and suggest that it may control the gain of pursuit eye movements, code predictive visual signals that drive pursuit, and code commands for smooth eye movements in a three dimensional coordinate frame.     

Operant control of human eye movements

Saccade and smooth pursuit are the eye movements used by primates to shift gaze. In this article we review evidence for the effects of reinforcement on several dimensions of these responses such as their latencies, velocities or amplitudes. We propose that these responses are operant behaviours controlled by their consequences on performance of visually guided tasks. Studying the conditions under which particular eye movement patterns might emerge from the cumulative effects of reinforcement provides critical insights about how motor responses are attuned to environmental exigencies.     

The role of the posterior parietal cortex in coordinate transformations for visual-motor integration

Lesion to the posterior parietal cortex in monkeys and humans produces spatial deficits in movement and perception. In recording experiments from area 7a, a cortical subdivision in the posterior parietal cortex in monkeys, we have found neurons whose responses are a function of both the retinal location of visual stimuli and the position of the eyes in the orbits. By combining these signals area 7 a neurons code the location of visual stimuli with respect to the head. However, these cells respond over only limited ranges of eye positions (eye-position-dependent coding). To code location in craniotopic space at all eye positions (eye-position-independent coding) an additional step in neural processing is required that uses information distributed across populations of area 7a neurons. We describe here a neural network model, based on back-propagation learning, that both demonstrates how spatial location could be derived from the population response of area 7a neurons and accurately accounts for the observed response properties of these neurons.     

Responses of Neurons of the Extrastriate Area 21b of the Cat Brain Cortex to Changes in Orientation of Moving Visual Stimuli

We studied the responses of neurons of the extrastriate cortical area 21b of the cat to changes in orientation of the movements of visual stimuli within the receptive field (RF) of the neuron under study. Our experiments demonstrated that 24 of 108 cells (22%) responded differentially to a certain extent to orientation of the movements of visual stimuli. As a whole, neurons of the area 21b did not demonstrate fine tuning on the optimum angle of orientation. In many cases, neuronal responses to different orientations of the movement of visual stimulus depended significantly on specific parameters of this stimulus (its shape, dimensions, and contrast). Some directionally sensitive neurons responded to a change in orientation of the movement of visual stimuli by modification of the index of directionality. We also studied spatial organization of the RF of neurons with the presentation of stationary visual stimuli. Comparison of the neuronal responses to a change in orientation of the movements of stimuli and to presentation of stationary stimuli showed that the correlation between the orientation sensitivity of the neuron under study and the stationary functional organization of its RF was insignificant. We hypothesize that inhibitory processes and subthreshold influences from a space surrounding the RF play a special role in the formation of the neuronal responses generated in the associative visual cortical regions to visual stimulation.     

Source of the eye-movement signal reaching real-motion cells

The stability of visual perception despite eye movements suggests the existence in the visual system of neurons able to recognize whether the movement of a retinal image is due to the actual movement of an object or is self-induced by the ocular movement. We found neurons of this type in several areas of the monkey visual cortex and named them "real-motion" cells. Extracellular recordings were carried out from single neurons of the cortical prestriate area V3A of two awake macaque monkeys. Eighty-seven neurons were studied by comparing their responses during stimulus movement across the stationary receptive field, and receptive-field movement across the stationary stimulus. This visual stimulation was presented against a uniform visual background, in darkness or against a textured background. Neurons which were not real-motion in light (45/87) maintained their behaviour in darkness, while about 40% of real-motion cells lost this behaviour in darkness. Both real-motion and non real-motion cells maintained the same behaviour when tested against a uniform or textured visual background but often, texture increased the difference in the response that real-motion cells showed between stimulus and eye movement. These data suggest that the eye-movement signal which reaches real-motion cells and is responsible for their behaviour may be either retinal or extraretinal in nature. This double innervation is in good agreement with perceptual phenomena related to the detection of movement in the visual field.     

Multisensory information facilitates reaction speed by enlarging activity difference between superior colliculus hemispheres in rats

Animals can make faster behavioral responses to multisensory stimuli than to unisensory stimuli. The superior colliculus (SC), which receives multiple inputs from different sensory modalities, is considered to be involved in the initiation of motor responses. However, the mechanism by which multisensory information facilitates motor responses is not yet understood. Here, we demonstrate that multisensory information modulates competition among SC neurons to elicit faster responses. We conducted multiunit recordings from the SC of rats performing a two-alternative spatial discrimination task using auditory and/or visual stimuli. We found that a large population of SC neurons showed direction-selective activity before the onset of movement in response to the stimuli irrespective of stimulation modality. Trial-by-trial correlation analysis showed that the premovement activity of many SC neurons increased with faster reaction speed for the contraversive movement, whereas the premovement activity of another population of neurons decreased with faster reaction speed for the ipsiversive movement. When visual and auditory stimuli were presented simultaneously, the premovement activity of a population of neurons for the contraversive movement was enhanced, whereas the premovement activity of another population of neurons for the ipsiversive movement was depressed. Unilateral inactivation of SC using muscimol prolonged reaction times of contraversive movements, but it shortened those of ipsiversive movements. These findings suggest that the difference in activity between the SC hemispheres regulates the reaction speed of motor responses, and multisensory information enlarges the activity difference resulting in faster responses.     

Sensory and behavioral properties of neurons in posterior parietal cortex of the awake, trained monkey.

Neurons in posterior parietal cortex of the awake, trained monkey respond to passive visual and/or somatosensory stimuli. In general, the receptive fields of these cells are large and nonspecific. When these neurons are studied during visually guided hand movements and eye movements, most of their activity can be accounted for by passive sensory stimulation. However, for some visual cells, the response to a stimulus is enhanced when it is to be the target for a saccadic eye movement. This enhancement is selective for eye movements into the visual receptive field since it does not occur with eye movements to other parts of the visual field. Cells that discharge in association with a visual fixation task have foveal receptive fields and respond to the spots of light used as fixation targets. Cells discharging selectively in association with different directions of tracking eye movements have directionally selective responses to moving visual stimuli. Every cell in our sample discharging in association with movement could be driven by passive sensory stimuli. We conclude that the activity of neurons in posterior parietal cortex is dependent on and indicative of external stimuli but not predictive of movement.     

Cursive writing with smooth pursuit eye movements

The eyes never cease to move: ballistic saccades quickly turn the gaze toward peripheral targets, whereas smooth pursuit maintains moving targets on the fovea where visual acuity is best. Despite the oculomotor system being endowed with exquisite motor abilities, any attempt to generate smooth eye movements against a static background results in saccadic eye movements [1, 2]. Although exceptions to this rule have been reported [3-5], volitional control over smooth eye movements is at best rudimentary. Here, I introduce a novel, temporally modulated visual display, which, although static, sustains smooth eye movements in arbitrary directions. After brief training, participants gain volitional control over smooth pursuit eye movements and can generate digits, letters, words, or drawings at will. For persons deprived of limb movement, this offers a fast, creative, and personal means of linguistic and emotional expression.     

The influence of structured visual backgrounds on smooth-pursuit initiation,steady-state pursuit and smooth-pursuit termination

 Smooth-pursuit eye movements were recorded in two rhesus monkeys in order to compare the influence of structured visual backgrounds on smooth-pursuit initiation, steady-state pursuit and pursuit termination. Different target trajectories were used in order to study smooth-pursuit initiation and termination. The influence of visual backgrounds on pursuit initiation was characterized by recording ocular responses elicited by step-ramp target displacements starting from straight ahead. Pursuit termination was characterized by analysing the transition from steady-state smooth-pursuit to fixation when a centripetally directed target ramp was terminated by a small target step in the direction of the ramp as soon as the target had come close to the straightahead position. The quantification of steady-state pursuit was based on ocular responses elicited by either paradigm. In accordance with previous work, we found that the onset of smooth-pursuit eye movements was delayed and initial eye acceleration reduced in the presence of a structured visual background. Likewise, mean eye velocity during steady-state pursuit was reduced by structured visual backgrounds. However, neither the latency nor the time course of smooth-pursuit termination was altered when the homogeneous background was replaced by a structured visual background. The lack of sensitivity of pursuit termination to the presence of visual structured backgrounds supports a previous contention that pursuit termination is mediated by a process which is different from the ones mediating smooth-pursuit initiation and steady-state pursuit. The absence of any noticeable effect of structured backgrounds on pursuit termination suggests that at least the fast component of the optokinetic reflex is suppressed during pursuit termination. Received: 24 October 1994/Accepted in revised form: 16 December 1994     

Basal Ganglia Neuronal Activity during Scanning Eye Movements in Parkinson’s Disease

The oculomotor role of the basal ganglia has been supported by extensive evidence, although their role in scanning eye movements is poorly understood. Nineteen Parkinsońs disease patients, which underwent implantation of deep brain stimulation electrodes, were investigated with simultaneous intraoperative microelectrode recordings and single channel electrooculography in a scanning eye movement task by viewing a series of colored pictures selected from the International Affective Picture System. Four patients additionally underwent a visually guided saccade task. Microelectrode recordings were analyzed selectively from the subthalamic nucleus, substantia nigra pars reticulata and from the globus pallidus by the WaveClus program which allowed for detection and sorting of individual neurons. The relationship between neuronal firing rate and eye movements was studied by crosscorrelation analysis. Out of 183 neurons that were detected, 130 were found in the subthalamic nucleus, 30 in the substantia nigra and 23 in the globus pallidus. Twenty percent of the neurons in each of these structures showed eye movement-related activity. Neurons related to scanning eye movements were mostly unrelated to the visually guided saccades. We conclude that a relatively large number of basal ganglia neurons are involved in eye motion control. Surprisingly, neurons related to scanning eye movements differed from neurons activated during saccades suggesting functional specialization and segregation of both systems for eye movement control.     

Methods for predicting cortical UP and DOWN states from the phase of deep layer local field potentials

During anesthesia, slow-wave sleep and quiet wakefulness, neuronal membrane potentials collectively switch between de- and hyperpolarized levels, the cortical UP and DOWN states. Previous studies have shown that these cortical UP/DOWN states affect the excitability of individual neurons in response to sensory stimuli, indicating that a significant amount of the trial-to-trial variability in neuronal responses can be attributed to ongoing fluctuations in network activity. However, as intracellular recordings are frequently not available, it is important to be able to estimate their occurrence purely from extracellular data. Here, we combine in vivo whole cell recordings from single neurons with multi-site extracellular microelectrode recordings, to quantify the performance of various approaches to predicting UP/DOWN states from the deep-layer local field potential (LFP). We find that UP/DOWN states in deep cortical layers of rat primary auditory cortex (A1) are predictable from the phase of LFP at low frequencies (< 4 Hz), and that the likelihood of a given state varies sinusoidally with the phase of LFP at these frequencies. We introduce a novel method of detecting cortical state by combining information concerning the phase of the LFP and ongoing multi-unit activity.     

A new visual area on the inferior wall of the cat cruciate sulcus

Properties of 187 neurons in the inferior wall of the cruciate sulcus, in an area where electrical stimulation evoked unidirectional saccadic eye movements, were investigated in waking cats. Of the total number 172 responded to visual stimulation. Neurons in the surface layers of the cortex responded to simple visual stimuli: light or dark spots or bars, both stationary and moving at speeds of around 30 deg/sec. These neurons showed no selectivity as regards stimulus orientation but sometimes behaved selectively toward the direction of their movements. In the intermediate layers the maximal neuronal response was obtained to a model of a bird flaping its wings. Neuronal responses in the depth of the cortex were characterized by selectivity to movement of stimuli toward or away from the animal in a certain part of the visual field, irrespective of whether a light stimulus was presented against a dark background or a dark stimulus against the light background. Responses to visual stimulation were exhibited only if the animal was in a state of activation, when the EEG showed desynchronization, and they were absent in a state of quite wakefulness. No responses were obtained to auditory or somatic stimulation. Responses to visual stimulation were not found in neurons of the medial wall of the brain beneath the cruciate sulcus, but responses were recorded to eye movements of definite size or orientation. It is postulated that at least two contiguous retinotopically organized zones exist in this part of the brain. Activity of one of them is connected with visual function, that of the other with eye movements.Institute for Problems in Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 16, No. 6, pp. 766–773, November–December, 1984.     

Optimizing visual motion perception during eye movements.

We usually perceive a stationary, stable world and we are able to correctly estimate the direction of heading from optic flow despite coherent visual motion induced by eye movements. This astonishing example of perceptual invariance results from a comparison of visual information with internal reference signals predicting the visual consequences of an eye movement. Here we demonstrate that the reference signal predicting the consequences of smooth-pursuit eye movements is continuously calibrated on the basis of direction-selective interactions between the pursuit motor command and the rotational flow induced by the eye movement, thereby minimizing imperfections of the reference signal and guaranteeing an ecologically optimal interpretation of visual motion.     

Learned timing of motor behavior in the smooth eye movement region of the frontal eye fields

Proper timing is a critical aspect of motor learning. We report a relationship between a representation of time and an expression of learned timing in neurons in the smooth eye movement region of the frontal eye fields (FEF(SEM)). During prelearning pursuit of target motion at a constant velocity, each FEF(SEM) neuron is most active at a distinct time relative to the onset of pursuit tracking. In response to an instructive change in target direction, a neuron expresses the most learning when the instruction occurs near the time of its maximal participation in prelearning pursuit. Different neurons are most active, and undergo the most learning, at distinct times during pursuit. We suggest that the representation of time in the FEF(SEM) drives learning that is temporally linked to an instructive change in target motion, and that this may be a general function of motor areas of the cortex.     

Reward-dependent gain and bias of visual responses in primate superior colliculus

Eye movements are often influenced by expectation of reward. Using a memory-guided saccade task with an asymmetric reward schedule, we show that visual responses of monkey SC neurons increase when the visual stimulus indicates an upcoming reward. The increase occurred in two distinct manners: (1) reactively, as an increase in the gain of the visual response when the stimulus indicated an upcoming reward; (2) proactively, as an increase in anticipatory activity when reward was expected in the neuron's response field. These effects were observed mostly in saccade-related SC neurons in the deeper layer which would receive inputs from the cortical eye fields and the basal ganglia. These results, together with recent findings, suggest that the gain modulation may be determined by the inputs from both the cortical eye fields and the basal ganglia, whereas the anticipatory bias may be derived mainly from the basal ganglia.     

Frame of reference transformations in motion perception during smooth pursuit eye movements

Smooth pursuit eye movements change the retinal image velocity of objects in the visual field. In order to change from a retinocentric frame of reference into a head-centric one, the visual system has to take the eye movements into account. Studies on motion perception during smooth pursuit eye movements have measured either perceived speed or perceived direction during smooth pursuit to investigate this frame of reference transformation, but never both at the same time. We devised a new velocity matching task, in which participants matched both perceived speed and direction during fixation to that during pursuit. In Experiment 1, the velocity matches were determined for a range of stimulus directions, with the head-centric stimulus speed kept constant. In Experiment 2, the retinal stimulus speed was kept approximately constant, with the same range of stimulus directions. In both experiments, the velocity matches for all directions were shifted against the pursuit direction, suggesting an incomplete transformation of the frame of reference. The degree of compensation was approximately constant across stimulus direction. We fitted the classical linear model, the model of Turano and Massof (2001) and that of Freeman (2001) to the velocity matches. The model of Turano and Massof fitted the velocity matches best, but the differences between de model fits were quite small. Evaluation of the models and comparison to a few alternatives suggests that further specification of the potential effect of retinal image characteristics on the eye movement signal is needed.