Cortical connections of the macaque anterior intraparietal (AIP) area

We traced the cortical connections of the anterior intraparietal (AIP) area, which is known to play a crucial role in visuomotor transformations for grasping. AIP displayed major connections with 1) areas of the inferior parietal lobule convexity, the rostral part of the lateral intraparietal area and the SII region; 2) ventral visual stream areas of the lower bank of the superior temporal sulcus and the middle temporal gyrus; and 3) the premotor area F5 and prefrontal areas 46 and 12. Additional connections were observed with the caudal intraparietal area and the ventral part of the frontal eye field. This study suggests that visuomotor transformations for object-oriented actions, processed in AIP, rely not only on dorsal visual stream information related to the object's physical properties but also on ventral visual stream information related to object identity. The identification of direct anatomical connections with the inferotemporal cortex suggests that AIP also has a unique role in linking the parietofrontal network of areas involved in sensorimotor transformations for grasping with areas involved in object recognition. Thus, AIP could represent a crucial node in a cortical circuit in which hand-related sensory and motor signals gain access to representations of object identity for tactile object recognition.     

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.     

Experience-dependent sharpening of visual shape selectivity in inferior temporal cortex

Whereas much is known about the visual shape selectivity of neurons in the inferior temporal cortex (ITC), less is known about the role of visual learning in the development and refinement of ITC shape selectivity. To address this, we trained monkeys to perform a visual categorization task with a parametric set of highly familiar stimuli. During training, the stimuli were always presented at the same orientation. In this experiment, we recorded from ITC neurons while monkeys viewed the trained stimuli in addition to image-plane rotated versions of those stimuli. We found that, concomitant with the monkeys' behavioral performance, neuronal stimulus selectivity was stronger for stimuli presented at the trained orientation than for rotated versions of the same stimuli. We also recorded from ITC neurons while monkeys viewed sets of novel and familiar (but not explicitly trained) randomly chosen complex stimuli. We again found that ITC stimulus selectivity was sharper for familiar than novel stimuli, suggesting that enhanced shape tuning in ITC can arise for both passively experienced and explicitly trained stimuli.     

Cortical projections of area V2 in the macaque

To determine the locus, extent and topograhic organization of cortical projections of area V2, we injected tritiated amino acids under electrophysiological control into 15 V2 sites in 14 macaques. The injection sites included the foveal representation and representations ranging from central to far peripheral eccentricities in both the upper and lower visual fields. The results indicated that all V2 sites project topographically back to V1 and forward to V3, V4 and MT. There is also a topographically organized projection from V2 to V4t, but this projection is limited to the lower visual field representation. V2 thus appears to project to virtually all the visual cortex within the occipital lobe. In addition to these projections to occipital visual areas, V2 sites representing eccentricities of approximately 30 degrees and greater project to three visual areas in parietal cortex-the medial superior temporal (MST), parieto-occipital (PO) and ventral intraparietal (VIP) areas. This peripheral field representation of V2 also projects to area VTF, a visual area located in area TF on the posterior parahippocampal gyrus. Projections from the peripheral field representation of V2 of parietal areas could provide a direct route for rapid activation of circuits serving spatial vision and spatial attention.      

Frontal-temporal disconnection abolishes object discrimination learning set in macaque monkeys

Two previous studies have shown that frontal-temporal disconnection in monkeys, produced by unilateral ablation of frontal cortex in one hemisphere and of visual inferior temporal cortex in the opposite hemisphere is entirely without effect on visual object-reward association learning in concurrent discrimination tasks. This is a surprising finding in light of the severe impairments that follow frontal-temporal disconnection in many other tests of visual learning and memory, including delayed matching-to-sample and several conditional learning tasks. To explore the limits of this preserved object-reward association learning, we trained monkeys on visual object discrimination learning set (DLS) prior to frontal-temporal disconnection. As a result of training with single object-reward associations, the monkeys acquired a proficient learning set, evidenced by the rapid learning of new single object-reward association problems. This rapid learning was not affected by unilateral ablations of either inferior temporal cortex alone or frontal cortex alone but was severely impaired after final surgery to complete the disconnection. Moreover, each individual monkey now learned single object-reward association problems at the slow rate at which that individual had learned such problems before the formation of learning set. This result shows that frontal-temporal disconnection abolishes visual learning set.     

Mental visual synthesis is originated in the fronto-temporal network of the left hemisphere

Mental visual synthesis is the capacity for experiencing, constructing, or manipulating 'mental imagery'. To investigate brain networks involved in mental visual synthesis, brain activity was measured in right-handed healthy volunteers during mental imagery tasks, in which the subjects were instructed to imagine a novel object, that does not exist in the real world, by composing it from two visually presented words associated with a real object or two achromatic line drawings of a real object, using functional magnetic resonance imaging (fMRI). Both tasks activated the same areas in the inferior frontal and inferior temporal cortices of the left hemisphere. Our results indicate that the source of mental visual synthesis may be formed by activity of a brain network consisting of these areas, which are also involved in semantic operations and visual imagery.     

Cortical connections of the inferior parietal cortical convexity of the macaque monkey

We traced the cortical connections of the 4 cytoarchitectonic fields--Opt, PG, PFG, PF--forming the cortical convexity of the macaque inferior parietal lobule (IPL). Each of these fields displayed markedly distinct sets of connections. Although Opt and PG are both targets of dorsal visual stream and temporal visual areas, PG is also target of somatosensory and auditory areas. Primary parietal and frontal connections of Opt include area PGm and eye-related areas. In contrast, major parietal and frontal connections of PG include IPL, caudal superior parietal lobule (SPL), and agranular frontal arm-related areas. PFG is target of somatosensory areas and also of the medial superior temporal area (MST) and temporal visual areas and is connected with IPL, rostral SPL, and ventral premotor arm- and face-related areas. Finally, PF is primarily connected with somatosensory areas and with parietal and frontal face- and arm-related areas. The present data challenge the bipartite subdivision of the IPL convexity into a caudal and a rostral area (7a and 7b, respectively) and provide a new anatomical frame of reference of the macaque IPL convexity that advances our present knowledge on the functional organization of this cortical sector, giving new insight into its possible role in space perception and motor control.     

Laminar specificity of intrinsic connections in Broca's area

Broca's area and its right hemisphere homologue comprise 2 cytoarchitectonic subdivisions, FDgamma and FCBm of von Economo C and Koskinas GN (1925, Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. Vienna/Berlin [Germany]: Springer). We report here on intrinsic connections within these areas, as revealed with biotinylated dextran amine and 1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate tracing in postmortem human brains. Injections limited to supragranular layers revealed a complex intrinsic network of horizontal connections within layers II and III spreading over several millimeters and to a lesser extent within layers IV, V, and VI. Ninety percent of the retrogradely labeled neurons (n = 734) were in supragranular layers, 4% in layer IV, and 6% in infragranular layers; most were pyramids and tended to be grouped into clusters of approximately 500 microm in diameter. Injections involving layer IV revealed extended horizontal connections within layers I-IV (up to 3.7 mm) and to a lesser extent in layers V and VI. Injections limited to the infragranular layers revealed horizontal connections mainly limited to these layers. Thus, intrinsic connections within Broca's area display a strong laminar specificity. This pattern is very similar in areas FDgamma and FCBm and in the 2 hemispheres.     

Single cell integration of animate form, motion and location in the superior temporal cortex of the macaque monkey

This study investigated the cellular mechanisms in the anterior part of the superior temporal sulcus (STSa) that underlie the integration of different features of the same visually perceived animate object. Three visual features were systematically manipulated: form, motion and location. In 58% of a population of cells selectively responsive to the sight of a walking agent, the location of the agent significantly influenced the cell's response. The influence of position was often evident in intricate two- and three-way interactions with the factors form and/or motion. For only one of the 31 cells tested, the response could be explained by just a single factor. For all other cells at least two factors, and for half of the cells (52%) all three factors, played a significant role in controlling responses. Our findings support a reformulation of the Ungerleider and Mishkin model, which envisages a subdivision of the visual processing into a ventral 'what' and a dorsal 'where' stream. We demonstrated that at least part of the temporal cortex ('what' stream) makes ample use of visual spatial information. Our findings open up the prospect of a much more elaborate integration of visual properties of animate objects at the single cell level. Such integration may support the comprehension of animals and their actions.     

Impaired filtering of distracter stimuli by TE neurons following V4 and TEO lesions in macaques

Directing attention to a behaviorally relevant visual stimulus can overcome the distracting effects of other nearby stimuli. Correspondingly, physiological studies indicate that attention serves to filter distracting stimuli from receptive fields (RFs) in several extrastriate areas. Moreover, a recent study demonstrated that lesions of extrastriate areas V4 and TEO produce impairments in attentional filtering. A critical remaining question concerns why lesions of ventral stream areas cause attentional filtering impairments. To address this question, we tested the effects of restricted area V4 and TEO lesions on both behavioral performance and the responses of downstream neurons in area TE. The lesions impaired behavioral discrimination thresholds and altered neuronal selectivity for target stimuli in the presence of distracters. With attention to the target, but in the absence of V4 and/or TEO inputs, TE neurons responded as though attentional inputs could no longer be used to filter distracters from their RFs. This presumably occurred because top-down attentional signals were no longer able to filter distracters from the RFs of the cells that provide TE with major input. Consistent with this interpretation, increasing the spatial separation between targets and distracters, such that they no longer fell within a typical V4 RF dimension, restored both behavioral performance and neuronal selectivity in the portion of TE RFs affected by the V4 lesion.     

Organization of horizontal axons in the inferior temporal cortex and primary visual cortex of the macaque monkey

We investigated the organization of horizontal connections at two distinct hierarchical levels in the ventral visual cortical pathway of the monkey, the inferior temporal (TE) and primary visual (V1) cortices. After injections of anterograde tracers into layers 2 and 3, clusters of terminals ('patches') of labeled horizontal collaterals in TE appeared at various distances up to 8 mm from the injection site, while in V1 clear patches were distributed only within 2 mm. The size and spacing of these patches in TE were larger and more irregular than those observed in V1. The labeling intensity of patches in V1 declined sharply with distance from the injection site. This tendency was less obvious in TE; a number of densely labeled patches existed at distant sites beyond weakly labeled patches. While injections into both areas resulted in an elongated pattern of patches, the anisotropy was greater in TE than in V1 for injections of a similar size. Dual tracer injections and larger-sized injections further revealed that the adjacent sites in TE had spatially distinct horizontal projections, compared to those in V1. These area-specific characteristics of the horizontal connections may contribute to the differences in visual information processing of TE and V1.     

A motion-sensitive area in ferret extrastriate visual cortex: an analysis in pigmented and albino animals

In search of the neuronal substrate for motion analysis in the ferret (Mustela putorius furo), we extracellularly recorded from extrastriate visual cortex in five pigmented and two albino ferrets under general anaesthesia and paralysis. Visual stimulation consisted of large area random dot patterns moving either on a circular path in the frontoparallel plane or expanding and contracting radially. Strongly direction-selective neurons were recorded in a circumscribed area in and just posterior to the suprasylvian sulcus, thus named by us the posterior suprasylvian area (area PSS). Altogether, we recorded 210 (90%) and 95 (72%) PSS neurons in pigmented and albino ferrets, respectively, that were direction selective. In these neurons responses during random dot pattern stimulation in the preferred direction were at least twice as strong than stimulation in the non-preferred direction. Response strength in preferred direction and tuning sharpness of PSS neurons in albinos were significantly reduced when compared to pigmented animals (median values: 34.1 versus 14.8 spikes/s and 142 versus 165 degrees for pigmented and albino ferrets, respectively). Inter-spike-intervals during visual stimulation were significantly shorter in pigmented (median 9 ms) than in albino PSS neurons (median 14 ms). Our data indicate that area PSS may play a crucial role in motion perception in the ferret.     

A comparative study of shape representation in macaque visual areas v2 and v4

We compared aspects of shape representation in extrastriate visual areas V2 and V4, which are both implicated in shape processing and belong to different hierarchical levels. We recorded responses of cells in awake, fixating monkeys to matched sets of contour and grating stimuli of low or intermediate complexity. These included simple stimuli (bars and sinusoids) and more complex stimuli (angles, intersections, arcs, and non-Cartesian gratings), all scaled to receptive field size. The responses of cells within each area were substantially modulated by each shape characteristic tested, with substantial overlap between areas by many response measures. Our analyses revealed many clear and reliable differences between areas in terms of the effectiveness of, and response modulation by, various shape characteristics. Grating stimuli were on average more effective than contour stimuli in V2 and V4, but the difference was more pronounced in V4. As a population, V4 showed greater response modulation by some shape characteristics (including simple shape characteristics) and V2 showed greater response modulation by many others (including complex shape characteristics). Recordings from area V1 demonstrated complex shape selectivity in some cells and relatively modest population differences in comparison with V2. Altogether, the representation of 2-dimensional shape characteristics revealed by this analysis varies substantially among the 3 areas. But surprisingly, the differences revealed by our analyses, individually or collectively, do not parallel the stepwise organization of the anatomical hierarchy. Commonalities of visual shape representation across hierarchical levels may reflect the replication of neural circuits used in generating complex shape representations at multiple spatial scales.     

Functional architecture of retinotopy in visual association cortex of behaving monkey

While the receptive field properties of single neurons in the inferior parietal cortex have been quantitatively described from numerous electrical measurements, the visual topography of area 7a and the adjacent dorsal prelunate area (DP) remains unknown. This lacuna may be a technical byproduct of the difficulty of reconstructing tens to hundreds of penetrations, or may be the result of varying functional retinotopic architectures. Intrinsic optical imaging, performed in behaving monkey for extended periods of time, was used to evaluate retinotopy simultaneously at multiple positions across the cortical surface. As electrical recordings through an implanted artificial dura are difficult, the measurement and quantification of retinotopy with long-term recordings was validated by imaging early visual cortex (areas V1 and V2). Retinotopic topography was found in each of the three other areas studied within a single day's experiment. However, the ventral portion of DP (DPv) had a retinotopic topography that varied from day to day, while the more dorsal aspects (DPd) exhibited consistent retinotopy. This suggests that the dorsal prelunate gyrus may consist of more than one visual area. The retinotopy of area 7a also varied from day to day. Possible mechanisms for this variability across days are discussed as well as its impact upon our understanding of the representation of extrapersonal space in the inferior parietal cortex.     

Long-range clustered connections within extrastriate visual area V5/MT of the rhesus macaque

Visual area V5/MT in the rhesus macaque has a distinct functional organization, where neurons with specific preferences for direction of motion and binocular disparity are co-organized in columns or clusters. Here, we analyze the pattern of intrinsic connectivity within cortical area V5/MT in both parasagittal sections of the intact brain and tangential sections from flatmounted cortex using small injections of the retrograde tracer cholera toxin subunit b. Labeled cells were predominantly found in cortical layers 2, 3, and 6. Going along the cortical layers, labeled cells were concentrated in regularly spaced clusters. The clusters nearest to the injection site were approximately 2 mm from its center. In flatmounted cortex, along the dorsoventral axis of V5/MT, we identified further clusters of labeled cells up to 10 mm from the injection site. Quantitative analysis of parasagittal sections estimated average cluster spacing at 2.2 mm; in cortical flatmounts, spacing was 2.3 mm measured radially from the injection site. The results suggest a regular pattern of intrinsic connectivity within V5/MT, which is consistent with connectivity between sites with a common preference for both direction of motion and binocular depth. The long-range connections can potentially account for the large suppressive surrounds of V5/MT neurons.     

Shape discrimination deficits during reversible deactivation of area V4 in the macaque monkey

The role of area V4 in the primate extrastriate cortex has received much attention in recent years. However, the deficit specificity following area V4 ablations has been difficult to determine due to the ablations including area V4 and additional adjacent areas, deficit attenuation and the numerous variations in the results of different research teams. In order to address these issues, we examined the role of area V4 during reversible deactivation of the lower visual field representation within this area while macaque monkeys performed simple pattern discriminations and their eye position was monitored. Specifically, the monkeys were trained to perform a match-to-sample task with the sample stimulus placed within or outside the visual field quadrant represented within the deactivated region of area V4. The sample and match stimuli had the same salience (same size or luminance). Using this approach, we identified significant simple shape discrimination deficits during deactivation of area V4 that did not attenuate with time. Deficits were also identified when the discriminanda were the same figure viewed at different orientations (rotated shapes). In contrast, no deficits were identified during simple hue discriminations. Furthermore, no saccadic eye movement deficits were identified during deactivation of area V4. Therefore, we conclude that deactivation of area V4 yields specific deficits on simple and rotated shape discriminations. These results show that area V4 is an important step in shape and form processing along the ventral visual stream leading to the inferotemporal cortex.     

Three-dimensional structure-from-motion selectivity in the anterior superior temporal polysensory area, STPa, of the behaving monkey

Human and non-human primates are able to perceive three-dimensional structure from motion displays. Three-dimensional structure-from-motion (object-motion) displays were used to test the hypothesis that neurons in the anterior division of the superior temporal polysensory area (STPa) of monkeys can selectively respond to three-dimensional structure-from-motion. Monkeys performed a reaction time task that required the detection of a change in the fraction of structure in three-dimensional transparent sphere displays. Neurons were able to distinguish structured and unstructured three-dimensional optic flow. These cells could differentiate the change in structure-from-motion at stimulus presentation and when the animal was detecting the amount of structure in the display. Some of these neurons were also tuned for characteristics of the sphere stimuli. Cells were also tested with navigational motion and many were found to respond both to three-dimensional structure-from-motion and navigational motion. These results suggest that STPa neurons represent specific aspects of three-dimensional surface structure and that neurons within STPa contribute to the perception of three-dimensional structure-from-motion.     

Responses of neurons in macaque area V4 during memory-guided visual search.

In a typical scene with many different objects, attentional mechanisms are needed to select relevant objects for visual processing and control over behavior. To test the role of area V4 in the selection of objects based on non-spatial features, we recorded from V4 neurons in the monkey, using a visual search paradigm. A cue stimulus was presented at the center of gaze, followed by a blank delay period. After the delay, a two-stimulus array was presented extrafoveally, and the monkey was rewarded for detecting the target stimulus matching the cue. The array was composed of one 'good' stimulus (effective in driving the cell when presented alone) and one 'poor' stimulus (ineffective in driving the cell when presented alone). When the choice array was presented in the receptive field (RF) of the neuron, many cells showed suppressive interactions between the stimuli as well as strong attention effects. Within 150--200 ms of array onset, responses to the array were determined by the target stimulus. If the target was the good stimulus, the response to the array became equal to the response to the good stimulus presented alone. If the target was the poor stimulus, the response approached the response to that stimulus presented alone. Thus the influence of the nontarget stimulus was filtered out. These effects were reduced or eliminated when the poor stimulus was located outside the RF and, therefore, no longer competing for the cell's response. Overall, the results support a 'biased competition' model of attention, according to which objects in the visual field compete for representation in the cortex, and this competition is biased in favor of the behaviorally relevant object.     

Degradation of signal timing in cortical areas V1 and V2 of senescent monkeys

Senescence in monkeys results in a degradation of the functional properties of cortical cells as well as prolonged hyperactivity. We have now compared the spontaneous and visually evoked activity levels, as well as the visual response latencies of cells in cortical areas V1 and V2 of young and very old monkeys. We found that V1 cells within layer 4 exhibit normal latencies. In contrast, in other parts of V1 and throughout V2 hyperactivity in old monkeys is accompanied by dramatic delays in both the intracortical and intercortical transfer of information. Extrastriate cortex (area V2) is affected more severely than striate cortex (V1). Delayed information processing in cerebral cortex should contribute to the declines in cortical function that accompany old age.