Temporal limitations in object processing across the human ventral visual pathway

Behavioral studies have shown that object recognition becomes severely impaired at fast presentation rates, indicating a limitation in temporal processing capacity. Here, we studied whether this behavioral limit in object recognition reflects limitations in the temporal processing capacity of early visual areas tuned to basic features or high-level areas tuned to complex objects. We used functional MRI (fMRI) to measure the temporal processing capacity of multiple areas along the ventral visual pathway progressing from the primary visual cortex (V1) to high-level object-selective regions, specifically the fusiform face area (FFA) and parahippocampal place area (PPA). Subjects viewed successive images of faces or houses at presentation rates varying from 2.3 to 37.5 items/s while performing an object discrimination task. Measures of the temporal frequency response profile of each visual area revealed a systematic decline in peak tuning across the visual hierarchy. Areas V1-V3 showed peak activity at rapid presentation rates of 18-25 items/s, area V4v peaked at intermediate rates (9 items/s), and the FFA and PPA peaked at the slowest temporal rates (4-5 items/s). Our results reveal a progressive loss in the temporal processing capacity of the human visual system as information is transferred from early visual areas to higher areas. These data suggest that temporal limitations in object recognition likely result from the limited processing capacity of high-level object-selective areas rather than that of earlier stages of visual processing.     

Perceptual continuity and the emergence of perceptual persistence in the ventral visual pathway

Perceptual continuity is an important aspect of our experience of the visual world. In this study, we focus on an example of perceptual continuity involving the maintenance of figure-ground segregation despite the removal of binding cues that initiated the segregation. Fragmented line drawings of objects were superimposed on a background of randomly oriented lines. Global forms could be discriminated from the background based on differences in motion or differences in color/brightness. Furthermore, perception of a global form persisted after the binding cue had been removed. A comparison between the persistence of forms constructed from motion or color demonstrated that both forms produced persistence after the object defining cues were removed. Functional imaging showed a gradual increase in the persistence of brain activity in the lower visual areas (V1, V2, VP), which reached significance in V4v and peaked in the lateral occipital area. There was no difference in the location of persistence for color- or motion-defined forms. These results suggest that the retention of a global percept is an emerging property of the ventral visual processing stream and the maintenance of grouped visual elements is independent of cue type. We postulated that perceptual persistence depends on a system of perceptual memory reflecting the state of perceptual organization.     

Asymmetry and ventral course of the human geniculostriate pathway as determined by hippocampal visual evoked potentials and subsequent visual field defects after temporal lobectomy

Summary Twenty-two patients with psychomotor epilepsy were implanted with depth electrodes along the axis of the mesial temporal lobe to identify an operable unilateral epileptic focus. Neuronal and field potentials were recorded in response to diffuse retinal illumination and clear short-latency responses were found in parahippocampal gyrus. These visual afferents in the mesial temporal lobe are assumed to be both from subcortical and cortical visual areas. There was a clear asymmetry in the ventral trajectory of the geniculostriate pathway as evidenced by asymmetric neuronal and field potential responses to brief flashes in right vs. left hippocampal gyrus and confirmed by a corresponding partial visual field deficit following therapeutic anterior temporal lobectomy. These results demonstrate that there is a retinotopic organization of fibers in the human geniculostriate pathway and that this pathway may have considerable variability in the anterior and ventral course these fibers take through the temporal lobe. These findings adequately account for the presence of direct projections from geniculate to hippocampal cortex and for unexpected hemianopsias with standard resections of the temporal lobe when there is a deviant detour of the geniculostriate pathway.Supported by grant no. NS 02808 and the Ralph Smith Foundation     

The visual cortico-striato-nigral pathway in the rat

The organization of the visual cortico-striato-nigral pathway in the rat has been investigated in two sets of experiments using anterograde autoradiographic tracing techniques. First, in one group of animals, injections of tritiated amino acids were placed throughout the visual cortex to demonstrate the visual corticostriatal pathway. The results indicate that visual corticostriatal fibres terminate in a distinctive clustered pattern throughout the entire length of the ipsilateral dorsomedial striatum. The projection shows a longitudinal topographic organization with cortical loci projecting onto narrow longitudinal regions of the dorsomedial striatum. In addition to the ipsilateral projection, a substantially smaller contralateral visual corticostriatal projection was also demonstrated. In the second set of experiments, the visual corticorecipient region of the striatum demonstrated in the first set of experiments was injected with tritiated amino acids to demonstrate the "visual" striatonigral projection. The results indicate that striatonigral fibres from the dorsomedial striatum project throughout the rostrocaudal extent of the ventral region of the pars reticulata. As with the visual corticostriatal pathway, the projection shows a longitudinal topographic organization with striatal loci projecting onto longitudinal regions of the ventral pars reticulata; the most rostral regions of the dorsal striatum project to the most medial regions of the ventral pars reticulata and, likewise, successively more caudal regions of the dorsal striatum project to successively more lateral regions of the ventral pars reticulata. In addition to the main projection to the ventral pars reticulata, a second smaller component of the striatonigral pathway was traced to adjacent regions of the dorsal pars reticulata and ventral pars compacta. These findings provide evidence of a visual cortico-striato-nigral pathway to both the pars reticulata and pars compacta in the rat. It is suggested that the major projection onto the ventral pars reticulata may provide an input onto nigrotectal neurons and thereby complete an indirect visual corticotectal connection mediated via links in the basal ganglia.     

A tectocortical visual pathway in the rat

Injections of tritiated leucine into the superior colliculus of the rat were used to study the efferents of the colliculus. The superficial layers of the colliculus project to the lateral posterior nucleus, the lateral geniculate nucleus and the pretectum. Two distinct subdivisions of the lateral posterior nucleus were found, a caudomedial region which receives a bilateral projection from the superior colliculus and an anterolateral region which receives a unilateral projection from the superior colliculus. Injections of horseradish peroxidase into the lateral prestriate visual cortex showed that the lateral posterior nucleus sends a dense projection to this area. There was no evidence that the caudomedial and anterolateral parts of the lateral posterior nucleus project to different regions of the lateral prestriate cortex.The tectothalamocortical pathway in the rat provides a major route outside the geniculostriate projection by which visual information from the retina can reach the cortex.     

Pantomimed actions may be controlled by the ventral visual stream

Several studies have demonstrated that while perceptual judgements of object size can be biased by visual illusions, actions remain more closely scaled to true object properties. This dissociation is often cited in support of a two-stream model of visual processing, in which visual perception is thought to be mediated by a ventral stream, while goal-directed actions are controlled by a dorsal stream. Evidence suggests that pantomimed actions (i.e., actions directed toward remembered targets) are controlled differently to natural actions; indeed, it has been proposed that pantomimed actions are mediated by the ventral rather than the dorsal stream. To test this hypothesis, we examined the effect of a visual size illusion (a variation of the Müller-Lyer figure) on manual aperture formation during natural and pantomimed prehension (i.e., action) and aperture scaling (i.e., perception). As found in earlier studies, mean peak aperture (MPA) was significantly affected by the illusion in the perception task but not the natural action task. In the pantomime condition, action and perception were equally affected by the illusion as reflected by MPA. These results provide support for the hypothesis that pantomimed actions are mediated by the ventral visual processing stream, while natural actions depend on the dorsal stream.     

Role of the extra-geniculate pathway in visual guidance

Summary We investigated the effect of superior colliculus lesions on the performance of a visually guided paw movement. Six cats were trained to perform a paw movement toward a lever moving in front of them at an adjustable speed. The target was visible and accessible for approximately 700 ms, corresponding to the time needed to traverse the aperture situated in front of the animal. To receive a food pellet reward the cat had to press on the lever during this presentation period. Efficient and misguided movements were recorded, and their relative proportions calculated. For each rewarded movement, the response time (delay between the appearance of the lever in the aperture and the cat's press) was automatically computed. After stabilization of their performance, each cat underwent a bilateral electrolytic lesion of the superior colliculi. In all cases it markedly affected precision. The cats first recovered their ability to reach an immobile lever and later on their ability to point to the lever while it was moving. However, even after two months of postoperative training, two cats had still not completely recovered their preoperative precision. All lesioned animals displayed a perturbation in their response time distribution. Anterior lesions, involving area centralis projection, were more effective in producing the deficits than more posterior ones. The results are discussed in relation to the involvement of the superior colliculus in the analysis of peripheral fixed or moving stimuli.     

Concordance between perceptual and categorical repetition effects in the ventral visual stream

The process of object categorization is an integral part of human cognition. In the present study, we have used a repetition suppression paradigm to determine the degree to which the ventral visual cortex is sensitive to categorical relationships. By using images of animals and tools, suppression across perceptual (stimulus level) and categorical repetitions (basic level and domain level) was compared and contrasted across the domain-selective and hierarchical organization of the ventral visual stream. Both perceptual and categorical repetition effects were insensitive to domain-selective tuning, with suppression most prominent in regions responding maximally to images, irrespective of stimulus domain. Likewise, both perceptual and categorical repetition produced overlapping suppression across multiple regions of the visual hierarchy. Some divergent patterns were observed. The right superior temporal sulcus demonstrated repetition suppression only at the basic level (different examples of the same basic object), and the right anterior fusiform gyrus was sensitive to direct stimulus repetition but not basic-level categorical repetition. Because of the high concordance between the response profiles of perceptual and categorical repetition effects, we conclude they arise from a common cognitive mechanism.     

An underestimated visual pathway in reptiles

Field potentials evoked in the turtle general cortex by electric stimulation of the optic tectum were analyzed. Cathodal polarization and subtotal lesions of n. rotundus led to either facilitation or depression of later components of the cortical potential. On the contrary, cathodal polarization and lesions of n.geniculatus lateralis dorsalis similarly affected the initial component. After 21-23 months following eye enucleation or optic nerve section, the conduction of fast tectal volleys to the general cortex via n. geniculatus lateralis dorsalis was blocked, though the conduction of tectal impulses to the dorsal ventricular ridge via n.rotundus survived. It is concluded that in turtles one more visual channel, i.e., retino-tecto-geniculo-cortical, is functioning, in addition to well-known retino-tecto-rotundo-telencephalic and retino-geniculo-cortical channels.     

Glial activation in the spinal ventral horn caudal to cervical injury

Microglia and astrocytes play complex roles following spinal cord injury (SCI), contributing to inflammatory processes that both exacerbate injury and promote functional recovery by supporting neuro-protection and neuroplasticity. The crossed phrenic phenomenon (CPP) is an example of respiratory plasticity in which C₂ cervical hemisection (C₂HS) strengthens crossed-spinal synaptic pathways to phrenic motor neurons ipsilateral to injury. We hypothesized that microglia and astrocytes are activated in the phrenic motor nucleus caudal and ipsilateral to C₂HS, suggesting their potential for involvement in the CPP. To test this hypothesis, an incomplete cervical spinal hemisection (C₂ lateral injury; C₂LI) was performed, and rats were allowed to recover for 1, 3, 14 or 28 days before collecting perfused spinal tissues. Microglia (via OX42) and astrocytes [via glial fibrillary acidic protein (GFAP)] were visualized with immunofluorescence microscopy in the C₄-C₅ ventral horn, the region encompassing most of the phrenic motor nucleus. OX42-occupied fractional area ipsilateral to injury increased with C₂LI (vs. sham) at 1 (12.5 ± 1.8%, p < 0.001), 3 (29.0 ± 1.9%, p < 0.001), 14 (26.1 ± 3.1%, p < 0.001) and 28 (19.2 ± 2.0%, p < 0.001) days post-C₂LI. GFAP-occupied fractional area also increased with C₂LI at 3 (24.4 ± 3.2%, p < 0.001) and 14 (16.8 ± 8.3%, p = 0.012) days, but not at 1 (6.2 ± 3.9%, p = 0.262) or 28 (10.6 ± 3.9%, p = 0.059) days post-C₂LI. Thus, microglia and astrocytes are activated in the phrenic motor nucleus caudal to C₂LI, suggesting that they play a role in functional deficits and/or recovery following spinal injury.     

Inherited abnormalities in the protein C activation pathway

The protein C (PC) anticoagulant pathway plays a crucial role in the regulation of fibrin formation via proteolytic degradation of the procoagulant cofactors factor Va and VIIIa by activated PC (APC). PC circulates in plasma as a zymogen, which is activated, on the surface of endothelial cells by the thrombin-thrombomodulin complex. Another endothelial cell-specific protein, the endothelial cell PC/APC receptor (EPCR), binds PC on the endothelial cell surface and further enhances the rate of PC activation. Normal APC generation depends on the precise assemblage, on the surface of endothelial cells, of at least four proteins: thrombin, thrombomodulin (TM), PC and EPCR. Therefore, any change in the efficiency of this assemblage may cause reduced APC generation and an increase in the risk of thrombosis. In the last years, several reports have suggested the association between mutations in TM and EPCR genes and venous and arterial thrombosis. Surprisingly, no studies have been reported linking mutations with levels of circulating APC, the final product of the interaction between thrombin, TM, PC and EPCR. Here, we describe the previously reported mutations in the TM and EPCR genes, and present the design and evaluation of a new strategy to investigate TM, EPCR, PC and prothrombin gene mutations in arterial and venous thrombosis.     

Amblyopia decreases activation of the corticogeniculate pathway and visual thalamic reticularis in attentive rats: a 'focal attention' hypothesis.

In rats which were rendered monocular amblyopic by lid suturing one eye during a critical period, the intensity of neuronal activation in parts of the monocular segments of the striate cortex (layers 4 and 6) and lateral geniculate nucleus, and in the visual segment of the thalamic reticular nucleus, was determined after exploration of a novel-complex environment. Quantitative analysis of the number of Fos-labelled neurons per unit area showed that, in comparison to the structures contralateral to the normal eye, in the side contralateral to the deprived amblyopic eye there is a gradient of diminished activation. The strongest activation asymmetry was observed in the visual reticular segment, while in layers 6 and 4 of the visual cortex the activation asymmetry was less strong and weakest, respectively. In the lateral geniculate there was no Fos-detectable activation asymmetry. Furthermore, there was a positive correlation between the time rats spent in exploration and the degree of activation asymmetry in the visual reticular segment. From these results it is concluded: (1) Activation of the visual segment of the thalamic reticular nucleus in the alert, attentive animal is predominantly under visual cortical control via the cortico-reticulo-geniculate pathway originating in layer 6, because this layer showed activation asymmetry while the other visual input to reticularis, the geniculate, did not show this asymmetry. (2) Activation of the visual reticularis is a function of attention to the environment because its activation asymmetry was correlated to the amount of exploratory attentional behaviour. (3) Diminished activity in the cortico-reticulo-geniculate pathway originating in layer 6, and of visual reticularis, caused by visual deprivation during the critical period should be considered as additional etiological factors of the resulting amblyopia. The functional significance of these results is explained by a 'focal attention' hypothesis postulating that the observed activation of visual reticularis in exploring animals is necessarily a reflection of activation of the corticogeniculate pathway, because these axons innervate both the geniculate and the visual reticular segment. Mechanistically, a focus of animal's attention is transmitted in a top-down fashion from the extrastriate cortex, and from upper cortical layers, into striate cortex layer 6. In turn, activation of layer 6 cells corresponding to attentional foci generates a core of excitation in the geniculate by the direct glutamatergic corticogeniculate axons, and a surround inhibition by the disynaptic cortico-reticulo-geniculate (ultimately GABAergic) pathway. In the temporal domain, in light of recent results, activation of thalamic reticular nucleus visual segment will contribute to the induction of gamma oscillations in geniculocortical pathways and in their cortical targets. All together, these interactions result in increased effectiveness of thalamocortical transmission of features from the focalized visual scene. The postulated attention-dependent spatiotemporal influences on thalamocortical transmission would be a main function of the corticothalamic pathways in the awake, attentive animal.     

Comparison of shape encoding in primate dorsal and ventral visual pathways

Ventral and dorsal visual pathways perform fundamentally different functions. The former is involved in object recognition, whereas the latter carries out spatial localization of stimuli and visual guidance of motor actions. Despite the association of the dorsal pathway with spatial vision, recent studies have reported shape selectivity in the dorsal stream. We compared shape encoding in anterior inferotemporal cortex (AIT), a high-level ventral area, with that in lateral intraparietal cortex (LIP), a high-level dorsal area, during a fixation task. We found shape selectivities of individual neurons to be greater in anterior inferotemporal cortex than in lateral intraparietal cortex. At the neural population level, responses to different shapes were more dissimilar in AIT than LIP. Both observations suggest a greater capacity in AIT for making finer shape distinctions. Multivariate analyses of AIT data grouped together similar shapes based on neural population responses, whereas such grouping was indistinct in LIP. Thus in a first comparison of shape response properties in late stages of the two visual pathways, we report that AIT exhibits greater capability than LIP for both object discrimination and generalization. These differences in the two visual pathways provide the first neurophysiological evidence that shape encoding in the dorsal pathway is distinct from and not a mere duplication of that formed in the ventral pathway. In addition to shape selectivity, we observed stimulus-driven cognitive effects in both areas. Stimulus repetition suppression in LIP was similar to the well-known repetition suppression in AIT and may be associated with the "inhibition of return" memory effect observed during reflexive attention.     

Synchronization between the end stages of the dorsal and the ventral visual stream

The end stage areas of the ventral (IT) and the dorsal (AIP) visual streams encode the shape of disparity-defined three-dimensional (3D) surfaces. Recent anatomical tracer studies have found direct reciprocal connections between the 3D-shape selective areas in IT and AIP. Whether these anatomical connections are used to facilitate 3D-shape perception is still unknown. We simultaneously recorded multi-unit activity (MUA) and local field potentials in IT and AIP while monkeys discriminated between concave and convex 3D shapes and measured the degree to which the activity in IT and AIP synchronized during the task. We observed strong beta-band synchronization between IT and AIP preceding stimulus onset that decreased shortly after stimulus onset and became modulated by stereo-signal strength and stimulus contrast during the later portion of the stimulus period. The beta-coherence modulation was unrelated to task-difficulty, regionally specific, and dependent on the MUA selectivity of the pairs of sites under study. The beta-spike-field coherence in AIP predicted the upcoming choice of the monkey. Several convergent lines of evidence suggested AIP as the primary source of the AIP-IT synchronized activity. The synchronized beta activity seemed to occur during perceptual anticipation and when the system has stabilized to a particular perceptual state but not during active visual processing. Our findings demonstrate for the first time that synchronized activity exists between the end stages of the dorsal and ventral stream during 3D-shape discrimination.     

Complement activation after lumbosacral ventral root avulsion injury

A lumbosacral ventral root avulsion (VRA) injury results in a pronounced loss of motoneurons, in part due to apoptosis. Caspase inhibitors may rescue motoneurons after a VRA in neonatal rats, but this treatment approach has been unsuccessful to protect motoneurons subjected to the same injury in adult rats. Other mechanisms may contribute to the retrograde motoneuron death encountered in adult animals. Here, we study whether the complement system, a part of the innate immune system, contributes to motoneuron death after a lumbosacral VRA. Adult Sprague-Dawley rats underwent a unilateral L5-S2 VRA injury. At 10 days postoperatively, quantitative immunohistochemical studies demonstrated that the lytic membrane attack complex (MAC) targeted approximately 38% of axotomized motoneurons. The MAC inhibitor Clusterin was concurrently expressed at significantly higher levels in astrocytes and de novo in 30% of the remaining motoneurons. Our data suggest that complement activation and necrosis contribute to motoneuron death after lumbosacral VRA injuries. We speculate that inhibition of MAC may constitute a potential neuroprotective strategy following cauda equina injuries.     

Deferred imitation of object-related actions in human-reared juvenile chimpanzees and orangutans

Deferred imitation of object-related actions (e.g., picking up a cloth with a set of tongs) was assessed in 3 enculturated juvenile orangutans (Pongo pygmaeus) and 3 enculturated juvenile chimpanzees (Pan troglodytes). For each task, animals were given 4 min to explore the objects (baseline), followed by a demonstration of the target behavior, and 10 min later, were re-presented the objects (deferred phase). Each animal displayed deferred imitation on at least one trial, with each species demonstrating deferred imitation on approximately half of all possible trials. The findings were interpreted as reflecting cognitive abilities in juvenile great apes that permit deferred imitation under humanlike rearing conditions.     

Quantitative characterization of disparity tuning in ventral pathway area V4

We performed a quantitative characterization of binocular disparity-tuning functions in the ventral (object-processing) pathway of the macaque visual cortex. We measured responses of 452 area V4 neurons to stimuli with disparities ranging from -1.0 to +1.0 degrees. Asymmetric Gaussian functions fit the raw data best (median R = 0.90), capturing both the modal components (local peaks in the -1.0 to +1.0 degrees range) and the monotonic components (linear or sigmoidal dependency on disparity) of the tuning patterns. Values derived from the asymmetric Gaussian fits were used to characterize neurons on a modal x monotonic tuning domain. Points along the modal tuning axis correspond to classic tuned excitatory and inhibitory patterns; points along the monotonic axis correspond to classic near and far patterns. The distribution on this domain was continuous, with the majority of neurons exhibiting a mixed modal/monotonic tuning pattern. The distribution in the modal dimension was shifted toward excitatory patterns, consistent with previous results in other areas. The distribution in the monotonic dimension was shifted toward tuning for crossed disparities (corresponding to stimuli nearer than the fixation plane). This could reflect a perceptual emphasis on objects or object parts closer to the observer. We also found that disparity-tuning strength was positively correlated with orientation-tuning strength and color-tuning strength, and negatively correlated with receptive field eccentricity.