Space coding by premotor cortex

Summary Many neurons in inferior area 6, a cortical premotor area, respond to visual stimuli presented in the space around the animal. We were interested to learn whether the receptive fields of these neurons are coded in retinotopic or in body-centered coordinates. To this purpose we recorded single neurons from inferior area 6 (F4 sector) in a monkey trained to fixate a light and detect its dimming. During fixation visual stimuli were moved towards the monkey both within and outside the neurons's receptive field. The fixation point was then moved and the neuron retested with the monkey's gaze deviated to the new location. The results showed that most inferior area 6 visual neurons code the stimulus position in spatial and not in retinal coordinates. It is proposed that these visual neurons are involved in generating the stable body-centered frame of reference necesary for programming visually guided movements.     

Feedback of visual object information to foveal retinotopic cortex

The mammalian visual system contains an extensive web of feedback connections projecting from higher cortical areas to lower areas, including primary visual cortex. Although multiple theories have been proposed, the role of these connections in perceptual processing is not understood. We found that the pattern of functional magnetic resonance imaging response in human foveal retinotopic cortex contained information about objects presented in the periphery, far away from the fovea, which has not been predicted by prior theories of feedback. This information was position invariant, correlated with perceptual discrimination accuracy and was found only in foveal, but not peripheral, retinotopic cortex. Our data cannot be explained by differential eye movements, activation from the fixation cross, or spillover activation from peripheral retinotopic cortex or from lateral occipital complex. Instead, our findings indicate that position-invariant object information from higher cortical areas is fed back to foveal retinotopic cortex, enhancing task performance.     

Neural responses in the macaque v1 to bar stimuli with various lengths presented on the blind spot

Although there is no retinal input within the blind spot, it is filled with the same visual attributes as its surround. Earlier studies showed that neural responses are evoked at the retinotopic representation of the blind spot in the primary visual cortex (V1) when perceptual filling-in of a surface or completion of a bar occurs. To determine whether these neural responses correlate with perception, we recorded from V1 neurons whose receptive fields overlapped the blind spot. Bar stimuli of various lengths were presented at the blind spots of monkeys while they performed a fixation task. One end of the bar was fixed at a position outside the blind spot, and the position of the other end was varied. Perceived bar length was measured using a similar set of bar stimuli in human subjects. As long as one end of the bar was inside the blind spot, the perceived bar length remained constant, and when the bar exceeded the blind spot, perceptual completion occurred, and the perceived bar length increased substantially. Some V1 neurons of the monkey exhibited a significant increase in their activity when the bar exceeded the blind spot, even though the amount of the retinal stimulation increased only slightly. These response increases coincided with perceptual completion observed in human subjects and were much larger than would be expected from simple spatial summation and could not be explained by contextual modulation. We conclude that the completed bar appearing on the part of the receptive field embedded within the blind spot gave rise to the observed increase in neuronal activity.     

Spatially specific FMRI repetition effects in human visual cortex

The functional MRI (fMRI) response to a pair of identical, successively presented stimuli can result in a smaller signal than the presentation of two nonidentical stimuli. This "repetition effect" has become a frequently used tool to make inferences about neural selectivity in specific cortical areas. However, little is known about the mechanism(s) underlying the effect. In particular, despite many successful applications of the technique in higher visual areas, repetition effects in lower visual areas [e.g., primary visual cortex (V1)] have been more difficult to characterize. One property that is well understood in early visual areas is the mapping of visual field locations to specific areas of the cortex (i.e., retinotopy). We used the retinotopic organization of V1 to activate progressively different populations of neurons in a rapid fMRI experimental design. We observed a repetition effect (reduced signal) when localized stimulus elements were repeated in identical locations. We show that this effect is spatially tuned and largely independent of both interstimulus interval (100-800 ms) and the focus of attention. Using the same timing parameters for which we observed a large effect of spatial position, we also examined the response to orientation changes and observed no effect of an orientation change on the response to repeated stimuli in V1 but significant effects in other retinotopic areas. Given these results, we discuss the possible causes of these repetition effects as well as the implications for interpreting other experiments that use this potentially powerful imaging technique.     

Visual responses of the human superior colliculus: a high-resolution functional magnetic resonance imaging study

The superior colliculus (SC) is a multimodal laminar structure located on the roof of the brain stem. The SC is a key structure in a distributed network of areas that mediate saccadic eye movements and shifts of attention across the visual field and has been extensively studied in nonhuman primates. In humans, it has proven difficult to study the SC with functional MRI (fMRI) because of its small size, deep location, and proximity to pulsating vascular structures. Here, we performed a series of high-resolution fMRI studies at 3 T to investigate basic visual response properties of the SC. The retinotopic organization of the SC was determined using the traveling wave method with flickering checkerboard stimuli presented at different polar angles and eccentricities. SC activations were confined to stimulation of the contralateral hemifield. Although a detailed retinotopic map was not observed, across subjects, the upper and lower visual fields were represented medially and laterally, respectively. Responses were dominantly evoked by stimuli presented along the horizontal meridian of the visual field. We also measured the sensitivity of the SC to luminance contrast, which has not been previously reported in primates. SC responses were nearly saturated by low contrast stimuli and showed only small response modulation with higher contrast stimuli, indicating high sensitivity to stimulus contrast. Responsiveness to stimulus motion in the SC was shown by robust activations evoked by moving versus static dot stimuli that could not be attributed to eye movements. The responses to contrast and motion stimuli were compared with those in the human lateral geniculate nucleus. Our results provide first insights into basic visual responses of the human SC and show the feasibility of studying subcortical structures using high-resolution fMRI.     

Integration of retinal disparity and fixation-distance related signals toward an egocentric coding of distance in the posterior parietal cortex of primates

For those movements that are directed toward objects located in extrapersonal space, it is necessary that visual inputs are first remapped from a retinal coordinate system to a body-centered one. The posterior parietal cortex (PPC) most likely integrates retinal and extraretinal information to determine the egocentric distance of an object located in three-dimensional (3-D) space. This determination requires both a retinal disparity signal and a parallel estimate of the fixation distance. We recorded from the lateral intraparietal area (LIP) to see if single neurons respond to both vergence angle and retinal disparity and if these two signals are integrated to encode egocentric distance. Monkeys were trained to make saccades to real targets in 3-D space. When both fixation distance and disparity of visual stimuli were varied, the disparity tuning of individual neurons display a fixation-distance modulation. We propose that the observed modulation contributes to a spatial coding domain intermediate between retinal and egocentric because the disparity tuning shifts in a systematic way with changes in fixation distance.     

Differential contribution of early visual areas to the perceptual process of contour processing

We investigated contour processing and figure-ground detection within human retinotopic areas using event-related functional magnetic resonance imaging (fMRI) in 6 healthy and na?ve subjects. A figure (6 degrees side length) was created by a 2nd-order texture contour. An independent and demanding foveal letter-discrimination task prevented subjects from noticing this more peripheral contour stimulus. The contour subdivided our stimulus into a figure and a ground. Using localizers and retinotopic mapping stimuli we were able to subdivide each early visual area into 3 eccentricity regions corresponding to 1) the central figure, 2) the area along the contour, and 3) the background. In these subregions we investigated the hemodynamic responses to our stimuli and compared responses with or without the contour defining the figure. No contour-related blood oxygenation level-dependent modulation in early visual areas V1, V3, VP, and MT+ was found. Significant signal modulation in the contour subregions of V2v, V2d, V3a, and LO occurred. This activation pattern was different from comparable studies, which might be attributable to the letter-discrimination task reducing confounding attentional modulation. In V3a, but not in any other retinotopic area, signal modulation corresponding to the central figure could be detected. Such contextual modulation will be discussed in light of the recurrent processing hypothesis and the role of visual awareness.     

Responses of a looming-sensitive neuron to compound and paired object approaches

The lobula giant movement detector (LGMD) and its target neuron, the descending contralateral movement detector (DCMD), constitute a motion-sensitive pathway in the locust visual system that responds preferentially to objects approaching on a collision course. LGMD receptive field properties, anisotropic distribution of local retinotopic inputs across the visual field, and localized habituation to repeated stimuli suggest that this pathway should be sensitive to approaches of individual objects within a complex visual scene. We presented locusts with compound looming objects while recording from the DCMD to test the effects of nonuniform edge expansion on looming responses. We also presented paired objects approaching from different regions of the visual field at nonoverlapping, closely timed and simultaneous approach intervals to study DCMD responses to multiple looming stimuli. We found that looming compound objects evoked characteristic responses in the DCMD and that the time of peak firing was consistent with predicted values based on a weighted ratio of the half size of each distinct object edge and the absolute approach velocity. We also found that the azimuthal position and interval of paired approaches affected DCMD firing properties and that DCMDs responded to individual objects approaching within 106 ms of each other. Moreover, comparisons between individual and paired approaches revealed that overlapping approaches are processed in a strongly sublinear manner. These findings are consistent with biophysical mechanisms that produce nonlinear integration of excitatory and feed-forward inhibitory inputs onto the LGMD that have been shown to underlie responses to looming stimuli.     

Parietal representation of object-based saccades

When monkeys make saccadic eye movements to simple visual targets, neurons in the lateral intraparietal area (LIP) display a retinotopic, or eye-centered, coding of the target location. However natural saccadic eye movements are often directed at objects or parts of objects in the visual scene. In this paper we investigate whether LIP represents saccadic eye movements differently when the target is specified as part of a visually displayed object. Monkeys were trained to perform an object-based saccade task that required them to make saccades to previously cued parts of an abstract object after the object reappeared in a new orientation. We recorded single neurons in area LIP of two macaque monkeys and analyzed their activity in the object-based saccade task, as well as two control tasks: a standard memory saccade task and a fixation task with passive object viewing. The majority of LIP neurons that were tuned in the memory saccade task were also tuned in the object-based saccade task. Using a hierarchical generalized linear model analysis, we compared the effects of three different spatial variables on the firing rate: the retinotopic location of the target, the object-fixed location of the target, and the orientation of the object in space. There was no evidence of an explicit object-fixed representation in the activity in LIP during either of the object-based tasks. In other words, no cells had receptive fields that rotated with the object. While some cells showed a modulation of activity due to the location of the target on the object, these variations were small compared to the retinotopic effects. For most cells, firing rates were best accounted for by either the retinotopic direction of the movement, the orientation of the object, or both spatial variables. The preferred direction of these retinotopic and object orientation effects were found to be invariant across tasks. On average, the object orientation effects were consistent with the retinotopic coding of potential target locations on the object. This interpretation is supported by the fact that the magnitude of these two effects were roughly equal in the early portions of the trial, but around the time of the motor response, the retinotopic effects dominated. We conclude that LIP uses the same retinotopic coding of saccade target whether the target is specified as an absolute point in space or as a location on a moving object.     

The time course of perisaccadic receptive field shifts in the lateral intraparietal area of the monkey

Neurons in the lateral intraparietal area of the monkey (LIP) have visual receptive fields in retinotopic coordinates when studied in a fixation task. However, in the period immediately surrounding a saccade these receptive fields often shift, so that a briefly flashed stimulus outside the receptive field will drive the neurons if the eye movement will bring the spatial location of that vanished stimulus into the receptive field. This is equivalent to a transient shift of the retinal receptive field. The process enables the monkey brain to process a stimulus in a spatially accurate manner after a saccade, even though the stimulus appeared only before the saccade. We studied the time course of this receptive field shift by flashing a task-irrelevant stimulus for 100 ms before, during, or after a saccade. The stimulus could appear in receptive field as defined by the fixation before the saccade (the current receptive field) or the receptive field as defined by the fixation after the saccade (the future receptive field). We recorded the activity of 48 visually responsive neurons in LIP of three hemispheres of two rhesus monkeys. We studied 45 neurons in the current receptive field task, in which the saccade removed the stimulus from the receptive field. Of these neurons 29/45 (64%) showed a significant decrement of response when the stimulus appeared 250 ms or less before the saccade, as compared with their activity during fixation. The average response decrement was 38% for those cells showing a significant (P < 0.05 by t-test) decrement. We studied 39 neurons in the future receptive field task, in which the saccade brought the spatial location of a recently vanished stimulus into the receptive field. Of these 32/39 (82%) had a significant response to stimuli flashed for 100 ms in the future receptive field, even 400 ms before the saccade. Neurons never responded to stimuli moved by the saccade from a point outside the receptive field to another point outside the receptive field. Neurons did not necessarily show any saccadic suppression for stimuli moved from one part of the receptive field to another by the saccade. Stimuli flashed <250 ms before the saccade-evoked responses in both the presaccadic and the postsaccadic receptive fields, resulting in an increase in the effective receptive field size, an effect that we suggest is responsible for perisaccadic perceptual inaccuracies.     

Perceptual characteristics of peripheral vision in children with autism

The present study examined the recognition of numerical stimuli briefly presented in the peripheral and the central (foveal) visual fields of children with autism. The participants were 5 children with high-functioning Autism Spectrum Disorder (ASD) and 10 typically developing (TD) children of similar chronological age. The stimuli were number strings presented on a personal computer screen for 160 msec in the position of the fixation point (foveal condition) or in the peripheral visual field (retinal eccentricity of 16 degrees) in one of the eight radial positions selected randomly (peripheral condition). The participants' task was to report the number of stimuli. The results showed that there were no significant differences in the mean response times between the TD and ASD groups. However, the mean percentage of correct answers in the ASD group was significantly higher than in the TD group for the peripheral condition. These results suggest that the effective visual field of the ASD group is expanded compared with the TD group. We discussed the relationships between perceptual characteristics and cognitive processes particular to ASD children.     

Rapid and precise retinotopic mapping of the visual cortex obtained by voltage-sensitive dye imaging in the behaving monkey

Retinotopy is a fundamental organizing principle of the visual cortex. Over the years, a variety of techniques have been used to examine it. None of these techniques, however, provides a way to rapidly characterize retinotopy, at the submillimeter range, in alert, behaving subjects. Voltage-sensitive dye imaging (VSDI) can be used to monitor neuronal population activity at high spatial and temporal resolutions. Here we present a VSDI protocol for rapid and precise retinotopic mapping in the behaving monkey. Two monkeys performed a fixation task while thin visual stimuli swept periodically at a high speed in one of two possible directions through a small region of visual space. Because visual space is represented systematically across the cortical surface, each moving stimulus produced a traveling wave of activity in the cortex that could be precisely measured with VSDI. The time at which the peak of the traveling wave reached each location in the cortex linked this location with its retinotopic representation. We obtained detailed retinotopic maps from a region of about 1 cm(2) over the dorsal portion of areas V1 and V2. Retinotopy obtained during <4 min of imaging had a spatial precision of 0.11-0.19 mm, was consistent across experiments, and reliably predicted the locations of the response to small localized stimuli. The ability to rapidly obtain precise retinotopic maps in behaving monkeys opens the door for detailed analysis of the relationship between spatiotemporal dynamics of population responses in the visual cortex and perceptually guided behavior.     

Pulvinar nuclei of the behaving rhesus monkey: visual responses and their modulation

We have examined the properties of neurons in three subdivisions of the pulvinar of alert, trained rhesus monkeys 1) an inferior, retinotopically mapped area (PI), 2) a lateral, retinotopically organized region (PL), and 3) a dorsomedial visual portion of the lateral pulvinar (Pdm), which has a crude retinotopic organization. We tested the neurons for visual responses to stationary and moving stimuli and for changes in these responses produced by behavioral manipulations. All areas contain cells sensitive to stimulus orientation as well as neurons selective for the direction of stimulus movement; however, the majority of cells in all three regions are either broadly tuned or nonselective for these attributes. Nearly all cells respond to stimulus onset, a significant number also give a response to stimulus termination, and rarely a cell gives only off responses. Nearly all cells increase their discharge rate to visual stimuli. Receptive fields in the two retinotopically mapped regions, PI and PL, have well-defined borders. The sizes of these receptive fields show a positive correlation with the eccentricity of the receptive fields. The receptive fields in the remaining region, Pdm, are frequently very large, but with these large fields excluded, show a similar correlation with eccentricity. All pulvinar cells tested (n = 20) were mapped in retinal coordinates; the receptive fields are positioned in relation to the retina. We found no cells with gaze-gated characteristics (2), nor cells mapped in a spatial coordinate system. The response latencies in PI and PL are shorter and less variable than the latencies in Pdm. Active use of a stimulus can produce an enhancement or attenuation of the visual response. Eye-movement modulation was found in all three subdivisions in about equal frequencies. Attentional modulation was common in Pdm and was rare in PI and PL. The modulation is spatially selective in Pdm and nonselective in PI for a small number of tested cells. These data demonstrate functional differences between Pdm and the other two areas and suggest that Pdm plays a role in selective visual attention, whereas PI and PL probably contribute to other aspects of visual perception.     

Cognitive mechanisms of transitive inference

Objects in natural scenes are rarely seen in isolation, but are usually overlapping or partially occluding other objects. To recognize individual objects, the visual system must be able to segregate overlapping objects from one another. Evidence from lesions in humans and monkeys suggest that perceptual segregation of occluded or overlapping objects involves extrastriate visual cortex. In monkeys, area V4 has been shown to play an important role in recognizing occluded or poorly salient shapes. In humans, a retinotopic homologue of ventral V4 (V4v) has been described, but it is not known whether this area is also functionally homologous to area V4 in monkeys. In this study, we tried to localize the visual cortical regions involved in perceptual segregation of overlapping shapes using positron emission tomography (PET). Regional cerebral blood flow (rCBF) was measured in seven subjects while they discriminated the relative areas of simultaneously presented rectangular shapes. In the control condition, the shapes were displayed without overlaps; in a second condition, the shapes overlapped each other partially. In a third condition, the shapes did not overlap but had been reduced in salience by adding random noise to the stimuli. Contrasting the overlapping shape condition with the control condition identified a single region in the left posterior lateral occipital cortex. The rCBF in this region also increased, though more weakly, during discrimination of shapes embedded in noise, relative to the control condition. The region activated by segregation of overlapping shapes was located in the posterior occipital cortex close to the anterior border of area V2, near the average location of human V4v as determined by retinotopic mapping studies. The activation of this region of extrastriate visual cortex by a task that involved segregation of overlapping shapes is consistent with monkey V4 and human V4v being functionally homologous. We conclude that discrimination of overlapping shapes involves in particular a region of extrastriate visual cortex located in the left lateral occipital cortex and that this region may correspond to human V4v.     

The orthographic sensitivity to written Chinese in the occipital-temporal cortex

Previous studies have identified an area in the left lateral fusiform cortex that is highly responsive to written words and has been named the visual word form area (VWFA). However, there is disagreement on the specific functional role of this area in word recognition. Chinese characters, which are dramatically different from Roman alphabets in the visual form and in the form to phonological mapping, provide a unique opportunity to investigate the properties of the VWFA. Specifically, to clarify the orthographic sensitivity in the mid-fusiform cortex, we compared fMRI response amplitudes (Exp. 1) as well as the spatial patterns of response across multiple voxels (Exp. 2) between Chinese characters and stimuli derived from Chinese characters with different orthographic properties. The fMRI response amplitude results suggest the existence of orthographic sensitivity in the VWFA. The results from multi-voxel pattern analysis indicate that spatial distribution of the responses across voxels in the occipitotemporal cortex contained discriminative information between the different types of character-related stimuli. These results together suggest that the orthographic rules are likely represented in a distributed neural network with the VWFA containing the most specific information regarding a stimulus’ orthographic regularity.     

The representation of perceived angular size in human primary visual cortex

Two objects that project the same visual angle on the retina can appear to occupy very different proportions of the visual field if they are perceived to be at different distances. What happens to the retinotopic map in primary visual cortex (V1) during the perception of these size illusions? Here we show, using functional magnetic resonance imaging (fMRI), that the retinotopic representation of an object changes in accordance with its perceived angular size. A distant object that appears to occupy a larger portion of the visual field activates a larger area in V1 than an object of equal angular size that is perceived to be closer and smaller. These results demonstrate that the retinal size of an object and the depth information in a scene are combined early in the human visual system.     

A body-centred frame of reference drives spatial priming in visual search

Spatial priming in visual search is a well-documented phenomenon. If the target of a visual search is presented at the same location in subsequent trials, the time taken to find the target at this repeated target location is significantly reduced. Previous studies did not determine which spatial reference frame is used to code the location. At least two reference frames can be distinguished: an observer-related frame of reference (egocentric) or a scene-based frame of reference (allocentric). While past studies suggest that an allocentric reference frame is more effective, we found that an egocentric reference frame is at least as effective as an allocentric one (Ball et al. Neuropsychologia 47(6):1585–1591, 2009). Our previous study did not identify which specific egocentric reference frame was used for the priming: participants could have used a retinotopic or a body-centred frame of reference. Here, we disentangled the retinotopic and body-centred reference frames. In the retinotopic condition, the position of the target stimulus, when repeated, changed with the fixation position, whereas in the body-centred condition, the position of the target stimulus remained the same relative to the display, and thus to the body-midline, but was different relative to the fixation position. We used a conjunction search task to assess the generality of our previous findings. We found that participants relied on body-centred information and not retinotopic cues. Thus, we provide further evidence that egocentric information, and specifically body-centred information, can persist for several seconds, and that these effects are not specific to either a feature or a conjunction search paradigm.     

Retinotopy and color sensitivity in human visual cortical area V8

Prior studies suggest the presence of a color-selective area in the inferior occipital-temporal region of human visual cortex. It has been proposed that this human area is homologous to macaque area V4, which is arguably color selective, but this has never been tested directly. To test this model, we compared the location of the human color-selective region to the retinotopic area boundaries in the same subjects, using functional magnetic resonance imaging (fMRI), cortical flattening and retinotopic mapping techniques. The human color-selective region did not match the location of area V4 (neither its dorsal nor ventral subdivisions), as extrapolated from macaque maps. Instead this region coincides with a new retinotopic area that we call 'V8', which includes a distinct representation of the fovea and both upper and lower visual fields. We also tested the response to stimuli that produce color afterimages and found that these stimuli, like real colors, caused preferential activation of V8 but not V4.     

Short‐term trained lexical categories affect preattentive shape perception: Evidence from vMMN

Perceptual processing of colors and shapes in the right visual field is modulated by the lexical category information of the stimuli, a phenomenon known as the lateralized Whorfian effect. For color stimuli, lateralized Whorfian effect is characterized by preattentive occurrence and dependency on acquired lexical information, but it remains unknown whether these key features are generalizable to other domains of perceptual processing. Here, we investigated whether lateralized Whorfian effect in the shape perception domain also depends on acquired lexical category and occurs preattentively using ERPs. Participants were trained to associate novel, irregular polygons with lexical category labels via short‐term intensive training. Using the visual oddball paradigm, we found stronger visual mismatch negativity (vMMN) component elicited by the deviant stimuli whose lexical category differed from the standard stimuli when the deviant was presented in the right visual field, indicating higher perceptual conspicuity for between‐category stimuli. These findings provide direct evidence of similar preattentive lexical category‐contingent modulation on shape perception akin to color perception, suggesting that the lateralized Whorfian effect is not epiphenomenal but rather might reflect the interaction between higher‐level lexical processing and the lower‐level perceptual processing more broadly.     

Cortical synchronization suggests neural principles of visual feature grouping

Compositions of visual scenes are related here to neural signals in visual cortex and to cortical circuit models to understand neural mechanisms of perceptual feature grouping. Starting from the hypothesis that synchronization and decoupling of cortical gamma-activities (35-90 Hz) define the relations among visual objects, we concentrate on synchronization related to (1) static retinal stimulation during ocular fixation, and (2) transient stimulation by sudden shifts in object position. The synchronization hypothesis has been tested by analyzing signal correlations in visual cortex of monkeys with the following results: Static retinal stimuli induce loosely phase-coupled gamma-activities among neurons of an object's cortical representation. Patches of gamma-synchronization become decoupled across the representation of an object's contour, and thereby can code figure-ground segregation. Transient stimuli evoke synchronized volleys of stimulus-locked activities that are typically non-rhythmic and include low frequency components in addition to those in the gamma-range. It is argued that stimulus-induced and stimulus-locked synchronizations may play different roles in perceptual feature grouping.