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.     

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.     

The multiple roles of visual cortical areas MT/MST in remembering the direction of visual motion

Although the role of cortical areas MT and MST (MT/MST) in the processing of directional motion information is well established, little is known about the way these areas contribute to the execution of complex behavioral tasks requiring the use of such information. We tested monkeys with unilateral lesions of these areas on a visual working memory task in which motion signals not only had to be encoded, but also stored for brief periods of time and then retrieved. The monkeys compared the directions of motion of two random-dot stimuli, sample and test, separated by a temporal delay. By increasing the temporal delay and spatially separating the two stimuli, placing one in the affected visual field and the other in the intact visual field, we were able to assess the contribution of MT/MST to specific components of the task: encoding (sample), retention (delay) and encoding/retrieval/comparison (test). We found that the effects of MT/MST lesions on specific components depended upon the demands of the task and the nature of the visual motion stimuli. Whenever stimuli consisted of random dots moving in a broad range of directions, MT/MST lesions appeared to affect encoding. Furthermore, when the lesions affected encoding of the sample, retention of the direction of stimulus motion was also affected. However, when the stimulus was coherent and the emphasis of the task was on the comparison of small direction differences, the absence of MT/MST had major impact on the retrieval/comparison component of the task and not on encoding or storage.     

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).     

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.     

Functional MRI studies of human visual motion perception: texture,luminance, attention and after-effects

Motion of an object is thought to be perceived independently of the object's surface properties. However, theoretical, neuropsychological and psychophysical observations have suggested that motion of textures, called 'second-order motion', may be processed by a separate system from luminance-based, or 'first-order', motion. Functional magnetic resonance imaging (fMRI) responses during passive viewing, attentional modulation and post-adaptation motion after-effects (MAE) of these stimuli were measured in seven retinotopic visual areas (labeled V1, V2, V3, VP, V4v, V3A and LO) and the motion-sensitive area MT/MST (V5). In all visual areas, responses were strikingly similar to motion of first- and second-order stimuli. These results differ from a prior investigation, because here the motion-specific responses were isolated. Directing attention towards and away from the motion elicited equivalent response modulation for the two types. Dramatic post-adaptation (MAE) differences in perception of the two stimuli were observed and fMRI activation mimicked perceptual changes, but did not reveal the processing differences. In fact, no visual area was found to respond selectively to the motion of second-order stimuli, suggesting that motion perception arises from a unified motion detection system.     

Double dissociation of V1 and V5/MT activity in visual awareness

The critical time windows of the contribution of V1 and V5/MT to visual awareness of moving visual stimuli were compared by administering transcranial magnetic stimulation (TMS) to V1 or V5/MT in various time intervals from stimulus offset during performance of a simple motion detection task. Our results show a double dissociation in which the critical period of V1 both predates and postdates that of V5/MT, and where stimulation of either V1 at V5/MT's critical period or V5/MT at V1's critical period does not impair performance. These findings demonstrate the importance of back-projections from V5/MT to V1 in awareness of real motion stimuli.     

Transient and permanent deficits in motion perception after lesions of cortical areas MT and MST in the macaque monkey

We examined the nature and the selectivity of the motion deficitsproduced by lesions of extrastriate areas MT and MST. Lesionswere made by injecting ibotenic acid into the representationof the left visual field in two macaque monkeys. The monkeysdiscriminated two stimuli that differed either in stimulus directionor orientation. Direction and orientation discrimination wereassessed by measuring thresholds with gratings and random-dotsplaced in the intact or lesioned visual fields. At the startof behavioral testing, we found pronounced, motion-specificdeficits in thresholds for all types of moving stimuli, includingpronounced elevations in contrast thresholds and in signal-to-noisethresholds measured with moving gratings, as well as deficitsin direction range thresholds and motion coherence measuredwith random-dot stimuli. In addition, the accuracy of directiondiscrimination was reduced at smaller spatial displacements(i.e. step sizes), suggesting an increase in spatial scale ofthe residual directional mechanism. Subsequent improve- mentsin thresholds were seen with all motion stimuli, as behavioraltraining progressed, and these improvements occurred only withextensive behavioral testing in the lesioned visual field. Theseimprovements were particularly pronounced for stimuli not maskedby noise. On the other hand, deficits in the ability to extractmotion from noisy stimuli and in the accuracy of direction discriminationpersisted despite extensive behavioral training. These resultsdemonstrate the importance of areas MT and MST for the perceptionof motion direction, particularly in the presence of noise.In addition, they provide evidence for the importance of behavioraltraining for functional recovery after cortical lesions. Thedata also strongly support the idea of functional specializationof areas MT and MST for motion processing.     

Posterior cingulate cortex: sensory and oculomotor properties of single neurons in behaving cat.

The posterior cingulate cortex of the cat is strongly linked to cortical areas with sensory and oculomotor functions. We have now recorded from feline posterior cingulate neurons in order to determine whether they are active in conjunction with sensory events and eye movements. The results described here are based on monitoring the electrical activity of 195 single neurons in the posterior cingulate cortex of three cats equipped with surgically implanted scleral search coils and trained to fixate visual targets. Posterior cingulate neurons carry tonic orbital position signals and are phasically active in conjunction with saccadic eye movements. Activity related to eye movements and gaze is attenuated but not abolished by the elimination of visual feedback. Posterior cingulate neurons also are responsive to visual, auditory, and somatosensory stimulation. Systematic testing with visual stimuli revealed that responses are sharply reduced due to refractoriness at rates of stimulation greater than a few per second. These results conform to the theory that posterior cingulate cortex is involved in processes underlying visuospatial cognition.     

Priming of motion direction and area V5/MT: a test of perceptual memory

Presentation of supraliminal or subliminal visual stimuli that can (or cannot) be detected or identified can improve the probability of the same stimulus being detected over a subsequent period of seconds, hours or longer. The locus and nature of this perceptual priming effect was examined, using suprathreshold stimuli, in subjects who received repetitive pulse transcranial magnetic stimulation over the posterior occipital cortex, the extrastriate motion area V5/MT or the right posterior parietal cortex during the intertrial interval of a visual motion direction discrimination task. Perceptual priming observed in a control condition was abolished when area V5/MT was stimulated but was not affected by magnetic stimulation over striate or parietal sites. The effect of transcranial magnetic stimulation (TMS) on priming was specific to site (V5/MT) and to task - colour priming was unaffected by TMS over V5/MT. The results parallel, in the motion domain, recent demonstrations of the importance of macaque areas V4 and TEO for priming in the colour and form domains.     

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.     

Cortical input to the nucleus of the optic tract and dorsal terminal nucleus (NOT-DTN) in macaques: a retrograde tracing study

Using retrograde tracing methods, we investigated the cortical projection to the nucleus of the optic tract and dorsal terminal nucleus of the accessory optic system (NOT-DTN) in macaque monkeys. Tracer injections at electrophysiologically identified recording sites in the NOT-DTN resulted in retrogradely labelled neurons in layer V of various cortical areas. The strongest projection always arose from the middle temporal area (MT) and the adjoining cortex anterior to MT in the superior temporal sulcus. A less dense projection came from the middle superior temporal area (MST). In addition, retrogradely labelled cells were consistently found in areas V1 and V2 at moderate to high density. Furthermore, sparse to moderate labelling occurred in prestriate area V3. These findings were compared with the label resulting from control injections into the superior colliculus in two additional cases. Our results indicate that the cortical input to the NOT-DTN as the sensorimotor interface for the pathway subserving stabilizing eye movements during the optokinetic reflex and smooth pursuit mainly arises from the motion-sensitive areas MT and MST in the superior temporal sulcus, as well as from areas V1 and V2. Clearly the projection to the NOT-DTN does not arise from a single cortical area.     

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.     

Maps of complex motion selectivity in the superior temporal cortex of the alert macaque monkey: a double-label 2-deoxyglucose study

The superior temporal sulcus (STS) of the macaque monkey contains multiple visual areas. Many neurons within these regions respond selectively to motion direction and to more complex motion patterns, such as expansion, contraction and rotation. Single-unit recording and optical recording studies in MT/MST suggest that cells with similar tuning properties are clustered into columns extending through multiple cortical layers. In this study, we used a double-label 2-deoxyglucose technique in awake, behaving macaque monkeys to clarify this functional organization. This technique allowed us to label, in a single animal, two populations of neurons responding to two different visual stimuli. In one monkey we compared expansion with contraction; in a second monkey we compared expansion with clockwise rotation. Within the STS we found a patchy arrangement of cortical columns with alternating stimulus selectivity: columns of neurons preferring expansion versus contraction were more widely separated than those selective for expansion versus rotation. This mosaic of interdigitating columns on the floor and posterior bank of the STS included area MT and some neighboring regions of cortex, perhaps including area MST.      

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.     

Temporal relation of population activity in visual areas MT/MST and in primary motor cortex during visually guided tracking movements

There is growing evidence that in primate cerebral cortex the areas along the 'dorsal pathway' are involved in the transformation of visual motion information towards a motor command. To pursue this cortical flow of information from visual motion areas to the motor cortex, single-cell activity was recorded from visual areas MT/MST (middle temporal area/medial superior temporal area) and from primary motor cortex (M1) while monkeys tracked moving targets with their right hand. Spike activity of 353 directionally tuned motor cortex cells was combined to a time-varying population vector, and similarly a time-resolved visual population vector was calculated from 252 MT/MST cells. Both population vectors code faithfully for the direction of the collinear motion of target and hand. For a given direction, the length of the population vectors varied over time during the performance of the task. The temporal evolution of both population responses reflects the different relationship between the early visual responses to the moving target and the directional motor command controlling the hand movement. The results indicate that during the visual tracking task visual and motor populations which code for similar directions of movement are co-activated with considerable temporal overlap. Despite this co-activation in both modalities, we failed to observe any significant synchronization between areas MT/MST and M1.     

Areas PMLS and 21 a of Cat Visual Cortex: Two Functionally Distinct Areas

We have compared the receptive field properties of neurons recordedfrom visuotopically corresponding regions of area 21a and theposteromedial lateral suprasylvian area (PMLS) of cat visualcortex. In both areas, the great majority of neurons were orientation-selectiveand binocular, and their responses to moving contours were modulatedby simultaneous in-phase or anti-phase motion of large texturedbackground stimuli (‘visual noise’). However, despitethe great hodological similarity between the two areas, PMLSneurons had on average significantly higher peak discharge rates,exhibited substantially greater direction selectivity indices,and preferred substantially higher stimulus velocities thanarea 21a neurons. Furthermore, the majority of binocular neuronsin the PMLS area and in area 21a were dominated respectivelyby the contralateral and the ipsilateral eyes. Finally, while46% of PMLS neurons were excited by movement of visual noiseper Se. only 25% of area 21 a neurons could be excited by suchstimuli. We argue that the PMLS area, like its presumed primatehomologue the middle-temporal (MT) area, is mainly involvedin motion analysis. By contrast, area 21a appears to be involvedin pattern analysis rather than motion analysis. It is likelythat phylogenetically area 21a derives from the PMLS area.     

Activation of area MT/V5 and the right inferior parietal cortex during the discrimination of transient direction changes in translational motion

The perception of changes in the direction of objects that translate in space is an important function of our visual system. Here we investigate the brain electrical phenomena underlying such a function by using a combination of magnetoencephalography (MEG) and magnetic resonance imaging. We recorded MEG-evoked responses in 9 healthy human subjects while they discriminated the direction of a transient change in a translationally moving random dot pattern presented either to the right or to the left of a central fixation point. We found that responses reached their maximum in 2 main regions corresponding to motion processing area middle temporal (MT)/V5 contralateral to the stimulated visual field, and to the right inferior parietal lobe (rIPL). The activation latencies were very similar in both regions ( approximately 135 ms) following the direction change onset. Our findings suggest that area MT/V5 provides the strongest sensory signal in response to changes in the direction of translational motion, whereas area rIPL may be involved either in the sensory processing of transient motion signals or in the processing of signals related to orienting of attention.     

A possible regulatory role of glyoxalase I in cell viability of human prostate cancer

The medial parieto-occipital cortex is a central node in the dorsomedial visual stream. Recent physiological studies in the macaque monkey have demonstrated that the medial parieto-occipital cortex contains two areas, the visual area V6 and the visuomotor area V6A. Area V6 is a retinotopically organized visual area that receives form and motion information directly from V1 and is heavily connected with the other areas of the dorsal visual stream, including V6A. Area V6A is a bimodal visual/somatosensory area that elaborates visual information such as form, motion and space suitable for the control of both reaching and grasping movements. Somatosensory and skeletomotor activities in V6A affect the upper limbs and involve both the transport phase of reaching and grasping movements. Finally, V6A is strongly and reciprocally connected with the dorsal premotor cortex controlling arm movements. The picture emerging from these data is that the medial parieto-occipital cortex is well equipped to control both proximal and distal movements in the online visuomotor guidance of prehension. In agreement with this view, selective V6A lesions in monkey produce misreaching and misgrasping with the arm contralateral to the lesion in visually guided movements. These deficits are similar to those observed in optic ataxia patients and suggest that human and monkey superior parietal lobules are homologous structures, and that optic ataxia syndrome is the result of the lesion of a 'human' area V6A.     

Shape selectivity for camouflage-breaking dynamic stimuli in dorsal V4 neurons

Motion is a potent cue for breaking camouflage in the natural world. To understand the neural basis of this phenomenon, one must utilize moving shapes defined by coherent motion of random texture elements against a similar, but stationary texture. To investigate how well neurons in area V4 process this novel, ecologically relevant stimulus and to compare shape selectivity for these shapes with static and other moving shapes, we tested V4 neurons with 5 static or moving shapes defined either by luminance or kinetic cues. The kinetic cues included a temporal frequency cue due to the difference in temporal frequencies of the moving dots inside the shape boundary and stationary dots outside the boundary. Therefore, static opponent motion-defined shapes without this cue were tested as an additional control. Approximately 44% (95/216) of V4 neurons showed shape selectivity. Analyses of these selective neurons both at single-neuron and population levels revealed that the shape-selective V4 neurons responded selectively to the moving kinetic shapes and that these neurons demonstrated robust invariance for shape preference across different shape conditions. Cue-invariant shape selectivity was more pronounced when kinetic shapes included the temporal frequency cue. This invariance may be rooted in nonlinearities occurring early in the visual pathway.