Denis Fize

Visual Motion Processing Investigated Using Contrast Agent-Enhanced fMRI in Awake Behaving Monkeys

To reduce the information gap between human neuroimaging and macaque physiology and anatomy, we mapped fMRI signals produced by moving and stationary stimuli (random dots or lines) in fixating monkeys. Functional sensitivity was increased by a factor of approximately 5 relative to the BOLD technique by injecting a contrast agent (monocrystalline iron oxide nanoparticle [MION]). Areas identified as motion sensitive included V2, V3, MT/V5, vMST, FST, VIP, and FEF (with moving dots), as well as V4, TE, LIP, and PIP (with random lines). These regions sensitive for moving dots are largely in agreement with monkey single unit data and (except for V3A) with human fMRI results. Moving lines activate some regions that have not been previously implicated in motion processing. Overall, the results clarify the relationship between the motion pathway and the dorsal stream in primates.

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 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.

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).

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.

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.

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 23) 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.

Brain areas involved in rapid categorization of natural images: an event-related fMRI study.

Event-related fMRI was used to investigate brain activation during a visual go/no-go categorization task based on colored photographs of natural scenes, similar to a previous ERP study by Thorpe et al. (1996, Nature 381: 520-522). Subjects had to press a key when an animal was present in the display. Stimuli were flashed for 33 ms using an intertrial interval of 5 s and a design that carefully balanced targets and distractors in a pseudo-random sequence. Activation produced by targets and distractors was compared with two different techniques, one based on correlations with the stimulation pattern, the other using simple t score statistics to compare selected scans. The contralateral primary motor cortex and the ipsilateral cerebellum were both more active following target trials than following distractors, thus confirming the sensitivity of the method. Differential activity was also seen in the posterior cingulate cortex, the fusiform, and the parahippocampic gyri. Activity in such structures could underlie the differential evoked-potentials reported previously in the same task. Surprisingly, in these visual structures, the signal was stronger following distractor trials than target ones. This result could be due to more prolonged processing on distractor trials. Alternatively, it could be that target detection induces strong activation of a small proportion of neurons, which, because of competitive inhibitory mechanisms, could result in a decrease in activity for the population as a whole. We suggest that this kind of mechanism could also account for the decreases in signal observed in perceptual priming experiments.

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 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.