Cortical area MSTd combines visual cues to represent 3-D self-movement

As arboreal primates move through the jungle, they are immersed in visual motion that they must distinguish from the movement of predators and prey. We recorded dorsal medial superior temporal (MSTd) cortical neuronal responses to visual motion stimuli simulating self-movement and object motion. MSTd neurons encode the heading of simulated self-movement in three-dimensional (3-D) space. 3-D heading responses can be evoked either by the large patterns of visual motion in optic flow or by the visual object motion seen when an observer passes an earth-fixed landmark. Responses to naturalistically combined optic flow and object motion depend on their relative directions: an object moving as part of the optic flow field has little effect on neuronal responses. In contrast, an object moving separately from the optic flow field has large effects, decreasing the amplitude of the population response and shifting the population's heading estimate to match the direction of object motion as the object moves toward central vision. These effects parallel those seen in human heading perception with minimal effects of objects moving with the optic flow and substantial effects of objects violating the optic flow. We conclude that MSTd can contribute to navigation by supporting 3-D heading estimation, potentially switching from optic flow to object cues when a moving object passes in front of the observer.     

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.     

Neuronal responses to optic flow in the monkey parietal area PEc

Area PEc, a high order association area, is located in the dorsocaudal portion of the superior parietal cortex. PEc neurons encode visual motion signals, especially the direction of stimulus motion. The present study tested if PEc neurons also process visual correlates of self-motion. The extracellular activity of single neurons in response to optic flow stimuli was recorded in two monkeys (Macaca fascicularis) trained in a fixation task. The stimuli were produced by random dots simulating planar motion, radial expansion and radial contraction. A substantial number of PEc neurons were specifically activated by radial optic flow and were selective for the position of the focus of expansion with respect to the fovea. Eccentric positions of the focus of expansion were preferred. Almost all neurons showed opponent excitatory-inhibitory activity to expanding-contracting visual fields. Planar motion elicited very weak responses. Optic flow responsiveness is not entirely explained by classical bar sensitivity in PEc neurons, suggesting that optic flow and classical bar responses could serve different mechanisms in the integration of visuo-motor signals to prepare body movements.     

Vestibular inputs to human motion-sensitive visual cortex

Two crucial sources of information available to an organism when moving through an environment are visual and vestibular stimuli. Macaque cortical area MSTd processes visual motion, including cues to self-motion arising from optic flow and also receives information about self-motion from the vestibular system. In humans, whether human MST (hMST) receives vestibular afferents is unknown. We have combined 2 techniques, galvanic vestibular stimulation and functional MRI (fMRI), to show that hMST is strongly activated by vestibular stimulation in darkness, whereas adjacent area MT is unaffected. The activity cannot be explained in terms of somatosensory stimulation at the electrode site. Vestibular input appears to be confined to the anterior portion of hMST, suggesting that hMST as conventionally defined may contain 2 subregions. Vestibular activity was also seen in another area previously implicated in processing visual cues to self-motion, namely the cingulate sulcus visual area (CSv), but not in visual area V6. The results suggest that cross-modal convergence of cues to self-motion occurs in both hMST and CSv.     

Cortical neuronal responses to optic flow are shaped by visual strategies for steering

We hypothesized that neuronal responses to virtual self-movement would be enhanced during steering tasks. We recorded the activity of medial superior temporal (MSTd) neurons in monkeys trained to steer a straight-ahead course, using optic flow. We found smaller optic flow responses during active steering than during the passive viewing of the same stimuli. Behavioral analysis showed that the monkeys had learned to steer using local motion cues. Retraining the monkeys to use the global pattern of optic flow reversed the effects of the active-steering task: active steering then evoked larger responses than passive viewing. We then compared the responses of neurons during active steering by local motion and by global patterns: Local motion trials promoted the use of local dot movement near the center of the stimulus by occluding the peripheral visual field midway through the trial. Global pattern trials promoted the use of radial pattern movement by occluding the central visual field midway through the trial. In this study, identical full-field optic-flow stimuli evoked larger responses in global-pattern trials than in local motion trials. We conclude that the selection of specific visual cues reflects strategies for active steering and alters MSTd neuronal responses to optic flow.     

Eye-hand coordination during reaching. II. An analysis of the relationships between visuomanual signals in parietal cortex and parieto-frontal association projections

The relationships between the distribution of visuomanual signals in parietal cortex and that of parieto-frontal projections are the subject of the present study. Single cell recording was performed in areas PEc and V6A, where different anatomical tracers were also injected. The monkeys performed a variety of behavioral tasks, aimed at studying the visual and motor properties of parietal cells, as well as the potential combination of retinal-, eye- and hand-related signals on cell activity. The activity of most cells was related to the direction of movement and the active position of the hand. Many of these reach-related cells were influenced by eye position information. Fewer cells displayed relationships to saccadic eye movements. The activity of most neurons related to a combination of both hand and eye signals. Many cells were also modulated during preparation for hand movement. Light-dark differences of activity were common and interpreted as related to the sight and monitoring of hand motion and/or position in the visual field. Most cells studied were very sensitive to moving visual stimuli and also responded to optic flow stimulation. Visual receptive fields were generally large and extended to the periphery of the visual field. For most neurons, the orientation of the preferred directions computed across different epochs and tasks conditions clustered within a limited sector of space, the field of global tuning. This can be regarded as an ideal frame to combine spatially congruent eye- and hand-related information for different forms of visuomanual behavior. All these properties were common to both PEc and V6A. Retinal, eye- and hand-related activity types, as well as parieto-frontal association cells, were distributed in a periodic fashion across the tangential domain of areas PEc and V6A. These functional and anatomical distributions were characterized and compared through a spectral and coherency analysis, which revealed the existence of a selective 'match' between activity types and parieto-frontal connections. This match depended on where each individual efferent projection was addressed. The results of the present and of the companion study can be relevant for a re-interpretation of optic ataxia as the consequence of the breakdown of the combination of retinal-, eye- and hand-related directional signals within the global tuning fields of parietal neurons.     

Functional sub-regions for optic flow processing in the posteromedial lateral suprasylvian cortex of the cat.

During locomotion, an observer sees a large and complex pattern of visual motion called optic flow. This phenomenon is characterized by elements in the environment accelerating and expanding as they move peripherally. In cats, previous studies have indicated that the posteromedial part of the lateral suprasylvian (PMLS) cortex may be involved in the processing of optic flow fields. We further addressed this issue by studying the importance of specific parameters of the optic flow patterns and investigating whether cell responses to these stimuli depend on receptive field (RF) location in the visual field. Results can be summarized as follows: approximately two-thirds of PMLS cells responded to optic flow fields and a subset of these (84/153) showed a clear direction selectivity for motion along the frontal axis. Of these units, the majority responded preferentially to expansion rather than contraction of the pattern. Cells' responses depend on RF location in the visual field. For centrally located RFs, tested both when the origin of motion was within the RF or at the area centralis, responses were generally comparable whether or not size or speed gradients were removed from the optic flow pattern. A different tendency was observed for peripherally located RFs. In general, these cells exhibited a preferred direction almost exclusively when the origin of motion was placed at the area centralis, and neuronal discharges and direction selectivity for many of them were reduced when the optic flow cues were removed from the pattern. The results of this study suggest that there may be functional differences in response properties between PMLS cells located in the central and peripheral parts of the visual field that may reflect a specialization of the PMLS cortex in optic flow processing.     

Modulation of responses to optic flow in area 7a by retinotopic and oculomotor cues in monkey

Perception of two- and three-dimensional optic flow critically depends upon extrastriate cortices that are part of the 'dorsal stream' for visual processing. Neurons in area 7a, a sub-region of the posterior parietal cortex, have a dual sensitivity to visual input and to eye position. The sensitivity and selectivity of area 7a neurons to three sensory cues - optic flow, retinotopic stimulus position and eye position - were studied. The visual response to optic flow was modulated by the retinotopic stimulus position and by the eye position in the orbit. The position dependence of the retinal and eye position modulation (i.e. gain field) were quantified by a quadratic regression model that allowed for linear or peaked receptive fields. A local maximum (or minimum) in both the retinotopic fields and the gain fields was observed, suggesting that these sensory qualities are not necessarily linearly represented in area 7a. Neurons were also found that simply encoded the eye position in the absence of optic flow. The spatial tuning for the eye position signals upon stationary stimuli and optic flow was not the same, suggesting multiple anatomical sources of the signals. These neurons can provide a substrate for spatial representation while primates move in the environment.      

A model of movement coordinates in the motor cortex: posture-dependent changes in the gain and direction of single cell tuning curves.

This article outlines a methodology for investigating the coordinate systems by which movement variables are encoded in the firing rates of individual motor cortical neurons. Recent neurophysiological experiments have probed the issue of underlying coordinates by examining how cellular preferred directions (as determined by the center-out task) change with posture. Several key experimental findings have resulted that constrain hypotheses about how motor cortical cells encode movement information. But while the significance of shifts in preferred direction is well known and widely accepted, posture-dependent changes in the depth of modulation of a cell's tuning curve--that is, gain changes--have not been similarly identified as a means of coordinate inference. This article develops a vector field framework in which the preferred direction and the gain of a cell's tuning curve are viewed as dual components of a unitary response vector. The formalism can be used to compute how each aspect of cell response covaries with posture as a function of the coordinate system in which a given cell is hypothesized to encode its movement information. Such an integrated approach leads to a model of motor cortical cell activity that codifies the following four observations: (i) cell activity correlates with hand movement direction; (ii) cell activity correlates with hand movement speed; (iii) preferred directions vary with posture; and (iv) the modulation depth of tuning curves varies with posture. Finally, the model suggests general methods for testing coordinate hypotheses at the single-cell level and simulates an example protocol for three possible coordinate systems: Cartesian spatial, shoulder-centered, and joint angle.     

Eye position signals modulate early dorsal and ventral visual areas

An internal sense of eye position is necessary to maintain the constancy of the visual world in spite of movements of the eyes. Neuroimaging studies have localized human homologs of monkey visual motion processing areas in MT/MST and also in the collateral sulcus (V4), an area that codes features within objects. We show that these two areas have a baseline fMRI signal that is modulated by eye position and that the preferred direction of the eye position signal is different in the two areas; increasing for ipsiversive eye positions in MT/MST and increasing for contraversive eye positions within the collateral sulcus. This baseline modulation is a true eye position signal; one that is present in the absence of visual motion stimuli. The difference in the preferred direction of the eye position signal may reflect the different transformations in these two areas; a transformation from a retinotopic (eye-centered) to an egocentric coordinate frame necessary for guiding action and to an object-centered frame for object recognition.     

Behavioral influences on cortical neuronal responses to optic flow

Optic flow selectively activates neurons in medial superior temporal (MST) cortex. We find that many MST neurons yield larger and more selective responses when the optic flow guides a subsequent eye movement. Smaller, less selective responses are seen when optic flow is preceded by a flashed precue that guides eye movements. Selectivity can decrease by a third (32%) after a flashed precue is presented at a peripheral location as a small spot specifying the target location of the eye movement. Smaller decreases in selectivity (18%) occur when the precue is presented centrally with its shape specifying the target location. Shape precues presented centrally, but not linked to specific target locations, do not appear to alter optic flow selectivity. The effects of spatial precueing can be reversed so that the precue leads to larger and more selective optic flow responses: A flashed precue presented as a distracter before behaviorally relevant optic flow is associated with larger optic flow responses and a 45% increase in selectivity. Together, these findings show that spatial precues can decrease or increase the size and selectivity of optic flow responses depending on the associated behavioral contingencies.     

Recoding arm position to learn visuomotor transformations.

There is strong experimental evidence that guiding the arm toward a visual target involves an initial vectorial transformation from direction in visual space to direction in motor space. Constraints on this transformation are imposed (i) by the neural codes for incoming information: the desired movement direction is thought to be signalled by populations of broadly tuned neurons and arm position by populations of monotonically tuned neurons; and (ii) by the properties of outgoing information: the actual movement direction results from the collective action of broadly tuned neurons whose preferred directions rotate with the position of the arm. A neural network model is presented that computes the visuomotor mapping, given these constraints. Appropriate operations are learned by the network in an unsupervised fashion through repeated action- perception cycles by recoding the arm-related proprioceptive information. The resulting solution has two interesting properties: (i) the required transformation is executed accurately over a large part of the reaching space, although few positions are actually learned; and (ii) properties of single neurons and populations in the network closely resemble those of neurons and populations in parietal and motor cortical regions. This model thus suggests a realistic scenario for the calculation of coordinate transformations and initial motor command for arm reaching movements.     

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 Alzheimer's disease patients with navigational deficits.     

Robust persistent neural activity in a model integrator with multiple hysteretic dendrites per neuron

Short-term memory is often correlated with persistent changes in neuronal firing rates in response to transient inputs. We model the persistent maintenance of an analog eye position signal by an oculomotor neural integrator receiving transient eye movement commands. Previous models of this network rely on precisely tuned positive feedback with <1% tolerance to mistuning, or use neurons that exhibit large discontinuities in firing rate with small changes in eye position. We show analytically how using neurons with multiple bistable dendritic compartments can enhance the robustness of eye fixations to mistuning while reproducing the approximately linear and continuous relationship between neuronal firing rates and eye position, and the dependence of neuron pair firing rate relationships on the direction of the previous saccade. The response of the model to continuously varying inputs makes testable predictions for the performance of the vestibuloocular reflex. Our results suggest that dendritic bistability could stabilize the persistent neural activity observed in working memory systems.     

Directional information flows between brain hemispheres during presleep wake and early sleep stages

Neuroscientists' efforts to better understand the underlying processes of human consciousness are growing in a variety of multidisciplinary approaches. Relevant within these are the studies aimed at exploring the physiological substratum of the propagation and reduction of cerebral-namely, corticocortical-communication flows. However, the preferential direction of the information flow between brain hemispheres is as yet largely unknown. It is the aim of the present research to study the communication flows between brain hemispheres, their directionality, and their regional variations across wake-sleep states. A second aim is to investigate the possibility of an association between different brain rhythms and different preferred directions of the information flow. Scalp electroencephalograms (EEGs) were recorded in 10 normal volunteers from wakefulness to early sleep stages (viz., resting wakefulness, sleep stages 2 and 4, and rapid eye movement [REM] of the first sleep cycle). EEG rhythms of interest were delta (1-4 Hz), theta (5-7 Hz), alpha (8-11 Hz), sigma (12-15 Hz), and beta (16-30 Hz). The direction of the interhemispheric information flow was evaluated by computing directed transformation function from these EEG rhythms. Interhemispheric directional flows varied as a function of the state of consciousness (wake and early sleep stages) and in relation to different cerebral areas. Across wake to sleep states, we found that delta and beta rhythms convey interhemispheric signals with opposite directions: preferred right to left hemisphere direction for delta and left to right for beta rhythms. A log correlation confirmed that the trend of low to high EEG frequencies-traditionally associated with an increasing state of vigilance-was significantly related to the direction of the communication flow from the left to right hemisphere. This evidence might open the way for a variety of research lines on different psychophysiological and pathological conditions.     

Neuronal activity in the caudal frontal eye fields of monkeys during memory-based smooth pursuit eye movements: comparison with the supplementary eye fields

Recently, we examined the neuronal substrate of predictive pursuit during memory-based smooth pursuit and found that supplementary eye fields (SEFs) contain signals coding assessment and memory of visual motion direction, decision not-to-pursue ("no-go"), and preparation for pursuit. To determine whether these signals were unique to the SEF, we examined the discharge of 185 task-related neurons in the caudal frontal eye fields (FEFs) in 2 macaques. Visual motion memory and no-go signals were also present in the caudal FEF but compared with those in the SEF, the percentage of neurons coding these signals was significantly lower. In particular, unlike SEF neurons, directional visual motion responses of caudal FEF neurons decayed exponentially. In contrast, the percentage of neurons coding directional pursuit eye movements was significantly higher in the caudal FEF than in the SEF. Unlike SEF inactivation, muscimol injection into the caudal FEF did not induce direction errors or no-go errors but decreased eye velocity during pursuit causing an inability to compensate for the response delays during sinusoidal pursuit. These results indicate significant differences between the 2 regions in the signals represented and in the effects of chemical inactivation suggesting that the caudal FEF is primarily involved in generating motor commands for smooth-pursuit eye movements.     

Speed selectivity for optic flow in area 7a of the behaving macaque

Area 7a, in the inferior parietal lobe, has been implicated in optic flow processing to obtain spatial information about the environment. Optic flow, angle-of-gaze and center-of-motion dependencies are already documented, but the selectivity of area 7a to speed is unknown. Such information is crucial as area 7a provides the final step in visual motion analysis that begins at the lateral geniculate nucleus and passes through MT, MST and LIP/VIP. Macaque area 7a neurons were tested with optic flows with speeds of 0.5-128 degrees /s. Of 161 neurons tested in four hemispheres of two adult male macaques, 53% (86/161) were speed selective at either the time of stimulus onset, at the end of the trial, or at both times. Speed selec- tivities resembling the basic filter types (band-pass, band-reject, high-pass, low-pass, broadband) were found. Area 7a neurons exhibited two novel properties not previously reported elsewhere. Speed selectivity was found to be dynamic in that many cells gained, lost or changed speed tuning over the course of a trial. In addition, speed dependence and optic flow selectivity interacted. For example, a cell could preferentially respond to one type of naviga- tional optic flow at a slow speed and a different navigational optic flow at a fast speed. The presence of speed selectivity combined with other properties of area 7a neurons indicates that these neurons may have a role in the concurrent representation of heading as well as multiple object speeds and directions.     

Persistent neural activity in head direction cells

Many neurons throughout the rat limbic system discharge in relation to the animal's directional heading with respect to its environment. These so-called head direction (HD) cells exhibit characteristics of persistent neural activity. This article summarizes where HD cells are found, their major properties, and some of the important experiments that have been conducted to elucidate how this signal is generated. The number of HD and angular head velocity cells was estimated for several brain areas involved in the generation of the HD signal, including the postsubiculum, anterior dorsal thalamus, lateral mammillary nuclei and dorsal tegmental nucleus. The HD cell signal has many features in common with what is known about how neural integration is accomplished in the oculomotor system. The nature of the HD cell signal makes it an attractive candidate for using neural network models to elucidate the signal's underlying mechanisms. The conditions that any network model must satisfy in order to accurately represent how the nervous system generates this signal are highlighted and areas where key information is missing are discussed.     

Retinotopy and attention in human occipital, temporal, parietal, and frontal cortex

Novel mapping stimuli composed of biological motion figures were used to study the extent and layout of multiple retinotopic regions in the entire human brain and to examine the independent manipulation of retinotopic responses by visual stimuli and by attention. A number of areas exhibited retinotopic activations, including full or partial visual field representations in occipital cortex, the precuneus, motion-sensitive temporal cortex (extending into the superior temporal sulcus), the intraparietal sulcus, and the vicinity of the frontal eye fields in frontal cortex. Early visual areas showed mainly stimulus-driven retinotopy; parietal and frontal areas were driven primarily by attention; and lateral temporal regions could be driven by both. We found clear spatial specificity of attentional modulation not just in early visual areas but also in classical attentional control areas in parietal and frontal cortex. Indeed, strong spatiotopic activity in these areas could be evoked by directed attention alone. Conversely, motion-sensitive temporal regions, while exhibiting attentional modulation, also responded significantly when attention was directed away from the retinotopic stimuli.     

Natural vision reveals regional specialization to local motion and to contrast-invariant, global flow in the human brain

Visual changes in feature movies, like in real-live, can be partitioned into global flow due to self/camera motion, local/differential flow due to object motion, and residuals, for example, due to illumination changes. We correlated these measures with brain responses of human volunteers viewing movies in an fMRI scanner. Early visual areas responded only to residual changes, thus lacking responses to equally large motion-induced changes, consistent with predictive coding. Motion activated V5+ (MT+), V3A, medial posterior parietal cortex (mPPC) and, weakly, lateral occipital cortex (LOC). V5+ responded to local/differential motion and depended on visual contrast, whereas mPPC responded to global flow spanning the whole visual field and was contrast independent. mPPC thus codes for flow compatible with unbiased heading estimation in natural scenes and for the comparison of visual flow with nonretinal, multimodal motion cues in it or downstream. mPPC was functionally connected to anterior portions of V5+, whereas laterally neighboring putative homologue of lateral intraparietal area (LIP) connected with frontal eye fields. Our results demonstrate a progression of selectivity from local and contrast-dependent motion processing in V5+ toward global and contrast-independent motion processing in mPPC. The function, connectivity, and anatomical neighborhood of mPPC imply several parallels to monkey ventral intraparietal area (VIP).