Processing of Egomotion-Consistent Optic Flow in the Rhesus Macaque Cortex.

The cortical network that processes visual cues to self-motion was characterized with functional magnetic resonance imaging in 3 awake behaving macaques. The experimental protocol was similar to previous human studies in which the responses to a single large optic flow patch were contrasted with responses to an array of 9 similar flow patches. This distinguishes cortical regions where neurons respond to flow in their receptive fields regardless of surrounding motion from those that are sensitive to whether the overall image arises from self-motion. In all 3 animals, significant selectivity for egomotion-consistent flow was found in several areas previously associated with optic flow processing, and notably dorsal middle superior temporal area, ventral intra-parietal area, and VPS. It was also seen in areas 7a (Opt), STPm, FEFsem, FEFsac and in a region of the cingulate sulcus that may be homologous with human area CSv. Selectivity for egomotion-compatible flow was never total but was particularly strong in VPS and putative macaque CSv. Direct comparison of results with the equivalent human studies reveals several commonalities but also some differences.

Fast ventral stream neural activity enables rapid visual categorization.

Primates can recognize objects embedded in complex natural scenes in a glimpse. Rapid categorization paradigms have been extensively used to study our core perceptual abilities when the visual system is forced to operate under strong time constraints. However, the neural underpinning of rapid categorization remains to be understood, and the incredible speed of sight has yet to be reconciled with modern ventral stream cortical theories of object recognition. Here we recorded multichannel subdural electrocorticogram (ECoG) signals from intermediate areas (V4/PIT) of the ventral stream of the visual cortex while monkeys were actively engaged in a rapid animal/non-animal categorization task. A traditional event-related potential (ERP) analysis revealed short visual latencies (<50-70ms) followed by a rapidly developing visual selectivity (within ~20-30ms) for most electrodes. A multi-variate pattern analysis (MVPA) technique further confirmed that reliable animal/non-animal category information was possible from this initial ventral stream neural activity (within ~90-100ms). Furthermore, this early category-selective neural activity was (a) unaffected by the presentation of a backward (pattern) mask, (b) generalized to novel (unfamiliar) stimuli and (c) co-varied with behavioral responses (both accuracy and reaction times). Despite the strong prevalence of task-related information on the neural signal, task-irrelevant visual information could still be decoded independently of monkey behavior. Monkey behavioral responses were also found to correlate significantly with human behavioral responses for the same set of stimuli. Together, the present study establishes that rapid ventral stream neural activity induces a visually selective signal subsequently used to drive rapid visual categorization and that this visual strategy may be shared between human and non-human primates.

Contextual Congruency Effect in Natural Scene Categorization: Different Strategies in Humans and Monkeys (Macaca mulatta).

Rapid visual categorization is a crucial ability for survival of many animal species, including monkeys and humans. In real conditions, objects (either animate or inanimate) are never isolated but embedded in a complex background made of multiple elements. It has been shown in humans and monkeys that the contextual background can either enhance or impair object categorization, depending on context/object congruency (for example, an animal in a natural vs. man-made environment). Moreover, a scene is not only a collection of objects; it also has global physical features (i.e phase and amplitude of Fourier spatial frequencies) which help define its gist. In our experiment, we aimed to explore and compare the contribution of the amplitude spectrum of scenes in the context-object congruency effect in monkeys and humans. We designed a rapid visual categorization task, Animal versus Non-Animal, using as contexts both real scenes photographs and noisy backgrounds built from the amplitude spectrum of real scenes but with randomized phase spectrum. We showed that even if the contextual congruency effect was comparable in both species when the context was a real scene, it differed when the foreground object was surrounded by a noisy background: in monkeys we found a similar congruency effect in both conditions, but in humans the congruency effect was absent (or even reversed) when the context was a noisy background.

Humans and monkeys share visual representations.

Conceptual abilities in animals have been shown at several levels of abstraction, but it is unclear whether the analogy with humans results from convergent evolution or from shared brain mechanisms inherited from a common origin. Macaque monkeys can access "non-similarity-based concepts," such as when sorting pictures containing a superordinate target category (animal, tree, etc.) among other scenes. However, such performances could result from low-level visual processing based on learned regularities of the photographs, such as for scene categorization by artificial systems. By using pictures of man-made objects or animals embedded in man-made or natural contexts, the present study clearly establishes that macaque monkeys based their categorical decision on the presence of the animal targets regardless of the scene backgrounds. However, as is found with humans, monkeys performed better with categorically congruent object/context associations, especially when small object sizes favored background information. The accuracy improvements and the response-speed gains attributable to superordinate category congruency in monkeys were strikingly similar to those of human subjects tested with the same task and stimuli. These results suggest analogous processing of visual information during the activation of abstract representations in both humans and monkeys; they imply a large overlap between superordinate visual representations in humans and macaques as well as the implicit use of experienced associations between object and context.

Rapid visual categorization of natural scene contexts with equalized amplitude spectrum and increasing phase noise.

This study aimed to determine the extent to which rapid visual context categorization relies on global scene statistics, such as diagnostic amplitude spectrum information. We measured performance in a Natural vs. Man-made context categorization task using a set of achromatic photographs of natural scenes equalized in average luminance, global contrast, and spectral energy. Results suggest that the visual system might use amplitude spectrum characteristics of the scenes to speed up context categorization processes. In a second experiment, we measured performance impairments with a parametric degradation of phase information applied to power spectrum averaged scenes. Results showed that performance accuracy was virtually unaffected up to 50% of phase blurring, but then rapidly fell to chance level following a sharp sigmoid curve. Response time analysis showed that subjects tended to make their fastest responses based on the presence of diagnostic man-made information; if no man-made characteristics enable to reach rapidly a decision threshold, because of a natural scene display or a high level of noise, the alternative decision for a natural response became increasingly favored. This two-phase strategy could maximize categorization performance if the diagnostic features of man-made environments tolerate higher levels of noise than natural features, as proposed recently.

Early interference of context congruence on object processing in rapid visual categorization of natural scenes.

Whereas most scientists agree that scene context can influence object recognition, the time course of such object/context interactions is still unknown. To determine the earliest interactions between object and context processing, we used a rapid go/no-go categorization task in which natural scenes were briefly flashed and subjects required to respond as fast as possible to animal targets. Targets were pasted on congruent (natural) or incongruent (urban) contexts. Experiment 1 showed that pasting a target on another congruent background induced performance impairments, whereas segregation of targets on a blank background had very little effect on behavior. Experiment 2 used animals pasted on congruent or incongruent contexts. Context incongruence induced a 10% drop of correct hits and a 16-ms increase in median reaction times, affecting even the earliest behavioral responses. Experiment 3 replicated the congruency effect with other subjects and other stimuli, thus demonstrating its robustness. Object and context must be processed in parallel with continuous interactions possibly through feed-forward co-activation of populations of visual neurons selective to diagnostic features. Facilitation would be induced by the customary co-activation of "congruent" populations of neurons whereas interference would take place when conflictual populations of neurons fire simultaneously.

Processing scene context: fast categorization and object interference.

The extent to which object identification is influenced by the background of the scene is still controversial. On the one hand, the global context of a scene might be considered as an ultimate representation, suggesting that object processing is performed almost systematically before scene context analysis. Alternatively, the gist of a scene could be extracted sufficiently early to be able to influence object categorization. It is thus essential to assess the processing time of scene context. In the present study, we used a go/no-go rapid visual categorization task in which subjects had to respond as fast as possible when they saw a "man-made environment", or a "natural environment", that was flashed for only 26 ms. "Man-made" and "natural" scenes were categorized with very high accuracy (both around 96%) and very short reaction times (median RT both around 390 ms). Compared with previous results from our group, these data demonstrate that global context categorization is remarkably fast: (1) it is as fast as object categorization [Fabre-Thorpe, M., Delorme, A., Marlot, C., & Thorpe, S. (2001). A limit to the speed of processing in ultra-rapid visual categorization of novel natural scenes. Journal of Cognitive Neuroscience, 13(2), 171-180]; (2) it is faster than contextual categorization at more detailed levels such as sea, mountain, indoor or urban contexts [Rousselet, G. A., Joubert, O. R., & Fabre-Thorpe, M. (2005). How long to get to the "gist" of real-world natural scenes? Visual Cognition, 12(6), 852-877]. Further analysis showed that the efficiency of contextual categorization was impaired by the presence of a salient object in the scene especially when the object was incongruent with the context. Processing of natural scenes might thus involve in parallel the extraction of the global gist of the scene and the concurrent object processing leading to categorization. These data also suggest early interactions between scene and object representations compatible with contextual influences on object categorization in a parallel network.

Rapid categorization of foveal and extrafoveal natural images: associated ERPs and effects of lateralization.

Humans are fast and accurate at performing an animal categorization task with natural photographs briefly flashed centrally. Here, this central categorization task is compared to a three position task in which photographs could appear randomly either centrally, or at 3.6 degrees eccentricity (right or left) of the fixation point. A mild behavioral impairment was found with peripheral stimuli with no evidence in support of hemispheric superiority; but enlarging the window of spatial attention to three possible stimuli locations had no behavioral cost on the processing of central images. Performance in the central categorization task has been associated with a large difference between the potentials evoked to target and non-target correct trials, starting about 150 ms after stimulus onset on frontal sites. Present results show that this activity originates within extrastriate visual cortices and probably reflects perceptual stimuli differences processed within areas involved in object recognition. Latencies, slopes, and peak amplitudes of this differential activity were invariant to stimulus position and attentional load. Stimulus location uncertainty and lateralization did not affect speed of visual processing.

Visual activation in prefrontal cortex is stronger in monkeys than in humans.

The prefrontal cortex supports many cognitive abilities, which humans share to some degree with monkeys. The specialized functions of the prefrontal cortex depend both on the nature of its inputs from other brain regions and on distinctive aspects of local processing. We used functional MRI to compare prefrontal activity between monkey and human subjects when they viewed identical images of objects, either intact or scrambled. Visual object-related activation of the lateral prefrontal cortex was observed in both species, but was stronger in monkeys than in humans, both in magnitude (factors 2-3) and in spatial extent (fivefold or more as a percentage of prefrontal volume). This difference was observed for two different stimulus sets, at two field strengths, and over a range of tasks. These results suggest that there may be more volitional control over visual processing in humans than in monkeys.

The processing of visual shape in the cerebral cortex of human and nonhuman primates: a functional magnetic resonance imaging study.

We compared neural substrates of two-dimensional shape processing in human and nonhuman primates using functional magnetic resonance (MR) imaging in awake subjects. The comparison of MR activity evoked by viewing intact and scrambled images of objects revealed shape-sensitive regions in occipital, temporal, and parietal cortex of both humans and macaques. Intraparietal cortex in monkeys was relatively more two-dimensional shape sensitive than that of humans. In both species, there was an interaction between scrambling and type of stimuli (grayscale images and drawings), but the effect of stimulus type was much stronger in monkeys than in humans. Shape- and motion-sensitive regions overlapped to some degree. However, this overlap was much more marked in humans than in monkeys. The shape-sensitive regions can be used to constrain the warping of monkey to human cortex and suggest a large expansion of lateral parietal and superior temporal cortex in humans compared with monkeys.

Similarities and differences in motion processing between the human and macaque brain: evidence from fMRI.

The present report reviews a series of functional magnetic resonance imaging (fMRI) activation studies conducted in parallel in awake monkeys and humans using the same motion stimuli in both species. These studies reveal that motion stimuli engage largely similar cortical regions in the two species. These common regions include MT/V5 and its satellites, of which FST contributes more to the human motion complex than is generally assumed in human imaging. These results also establish a direct link between selectivity of MT/V5 neurons for speed gradients and functional activation of human MT/V5 by three-dimensional (3D) structure from motion stimuli. On the other hand, striking functional differences also emerged: in humans V3A and several regions in the intraparietal sulcus (IPS) are much more motion sensitive than their simian counterparts.

Stereopsis activates V3A and caudal intraparietal areas in macaques and humans.

Stereopsis, the perception of depth from small differences between the images in the two eyes, provides a rich model for investigating the cortical construction of surfaces and space. Although disparity-tuned cells have been found in a large number of areas in macaque visual cortex, stereoscopic processing in these areas has never been systematically compared using the same stimuli and analysis methods. In order to examine the global architecture of stereoscopic processing in primate visual cortex, we studied fMRI activity in alert, fixating human and macaque subjects. In macaques, we found strongest activation to near/far compared to zero disparity in areas V3, V3A, and CIPS. In humans, we found strongest activation to the same stimuli in areas V3A, V7, the V4d topolog (V4d-topo), and a caudal parietal disparity region (CPDR). Thus, in both primate species a small cluster of areas at the parieto-occipital junction appears to be specialized for stereopsis.

The retinotopic organization of primate dorsal V4 and surrounding areas: A functional magnetic resonance imaging study in awake monkeys.

Using functional magnetic resonance imaging (fMRI), we mapped the retinotopic organization throughout the visual cortex of fixating monkeys. The retinotopy observed in areas V1, V2, and V3 was completely consistent with the classical view. V1 and V3 were bordered rostrally by a vertical meridian representation, and V2 was bordered by a horizontal meridian. More anterior in occipital cortex, both areas V3A and MT-V5 had lower and upper visual field representations split by a horizontal meridian. The rostral border of dorsal V4 was characterized by the gradual transition of a representation of the vertical meridian (dorsally) to a representation of the horizontal meridian (more ventrally). Central and ventral V4, on the other hand, were rostrally bordered by a representation of the horizontal meridian. The eccentricity lines ran perpendicular to the ventral V3-V4 border but were parallel to the dorsal V3-V4 border. These results indicate different retinotopic organizations within dorsal and ventral V4, suggesting that the latter regions may not be merely the lower and upper visual field representations of a single area. Moreover, because the present fMRI data are in agreement with previously published electrophysiological results, reported distinctions in the retinotopic organization of human and monkey dorsal V4 reflect genuine species differences that cannot be attributed to technical confounds. Finally, aside from dorsal V4, the retinotopic organization of macaque early visual cortex (V1, V2, V3, V3A, and ventral V4) is remarkably similar to that observed in human fMRI studies. This finding indicates that early visual cortex is mostly conserved throughout hominid evolution.

Repeated fMRI using iron oxide contrast agent in awake, behaving macaques at 3 Tesla.

Iron oxide contrast agents have been employed extensively in anesthetized rodents to enhance fMRI sensitivity and to study the physiology of cerebral blood volume (CBV) in relation to blood oxygen level-dependent (BOLD) signal following neuronal activation. This study quantified the advantages of exogenous agent for repeated neuroimaging in awake, nonhuman primates using a clinical 3 Tesla scanner. A monocrystalline iron oxide nanoparticle (MION) solution was injected at iron doses of 8 to 10 mg/kg in two macaque monkeys. Adverse behavioral effects due to contrast agent were not observed in either monkey using cumulative doses in excess of 60 mg/kg. Relative to BOLD imaging at 3 Tesla, MION increased functional sensitivity by an average factor of 3 across the brain for a stimulus of long duration. Rapid stimulus presentation attenuated MION signal changes more than BOLD signal changes, due to the slower time constant of the blood volume response relative to BOLD signal. Overall, the contrast agent produced a dramatic improvement in functional brain imaging results in the awake, behaving primate at this field strength. (c) 2002 Elsevier Science (USA).