Michele Furlan

A Representation of Changing Heading Direction in Human Cortical Areas pVIP and CSv

When we move around in the environment, we continually change direction. Much work has examined how the brain extracts instantaneous direction of heading from optic flow but how changes in heading are encoded is unknown. Change could simply be inferred cognitively from successive instantaneous heading values, but we hypothesize that heading change is represented as a low-level signal that feeds into motor control with minimal need for attention or cognition. To test this, we first used functional MRI to measure activity in several predefined visual areas previously associated with processing optic flow (hMST, hV6, pVIP, and CSv) while participants viewed flow that simulated either constant heading or changing heading. We then trained a support vector machine (SVM) to distinguish the multivoxel activity pattern elicited by rightward versus leftward changes in heading direction. Some motion-sensitive visual cortical areas, including hMST, responded well to flow but did not appear to encode heading change. However, visual areas pVIP and, particularly, CSv responded with strong selectivity to changing flow and also allowed direction of heading change to be decoded. This suggests that these areas may construct a representation of heading change from instantaneous heading directions, permitting rapid and accurate preattentive detection and response to change.

Cortical hyperexcitability and sensitivity to discomfort glare.

It is well established that there are two main aspects to glare, the visual impairment and the discomfort, known as disability and discomfort glare, respectively. In contrast to the case of disability glare we understand very little about the underlying mechanisms or physiology of discomfort glare. This study attempts to elucidate the neural mechanisms involved using fMRI and glare sources with controlled levels of retinal illuminance. Prior to carrying out the fMRI experiment, we determined each participants discomfort glare threshold. The participants were then divided into two groups of equal size based on their ranked sensitivity to discomfort glare, a low and high sensitivity group. In the fMRI experiment each participant was presented with three levels of glare intensity whilst simultaneously required to carry out a simple behavioral task. We compared BOLD responses between the two groups and found that the group more sensitive to glare had an increased response that was localized at three discrete, bilateral cortical locations: one in the cunei, one in the lingual gyri and one in the superior parietal lobules. This increased response was present for all light levels tested, whether or not they were intense enough to cause discomfort glare. Based on the results, we present the case that discomfort glare may be a response to hyperexcitability or saturation of visual neurons.

Neural Correlates of Finger Gnosis

Neuropsychological studies have described patients with a selective impairment of finger identification in association with posterior parietal lesions. However, evidence of the role of these areas in finger gnosis from studies of the healthy human brain is still scarce. Here we used functional magnetic resonance imaging to identify the brain network engaged in a novel finger gnosis task, the intermanual in-between task (IIBT), in healthy participants. Several brain regions exhibited a stronger blood oxygenation level-dependent (BOLD) response in IIBT than in a control task that did not explicitly rely on finger gnosis but used identical stimuli and motor responses as the IIBT. The IIBT involved stronger signal in the left inferior parietal lobule (IPL), bilateral precuneus (PCN), bilateral premotor cortex, and left inferior frontal gyrus. In all regions, stimulation of nonhomologous fingers of the two hands elicited higher BOLD signal than stimulation of homologous fingers. Only in the left anteromedial IPL (a-mIPL) and left PCN did signal strength decrease parametrically from nonhomology, through partial homology, to total homology with stimulation delivered synchronously to the two hands. With asynchronous stimulation, the signal was stronger in the left a-mIPL than in any other region, possibly indicating retention of task-relevant information. We suggest that the left PCN may contribute a supporting visuospatial representation via its functional connection to the right PCN. The a-mIPL may instead provide the core substrate of an explicit bilateral body structure representation for the fingers that when disrupted can produce the typical symptoms of finger agnosia.

Connectivity of the Cingulate Sulcus Visual Area (CSv) in the Human Cerebral Cortex.

The human cingulate sulcus visual area (CSv) responds selectively to visual and vestibular cues to self-motion. Although it is more selective for visual self-motion cues than any other brain region studied, it is not known whether CSv mediates perception of self-motion. An alternative hypothesis, based on its location, is that it provides sensory information to the motor system for use in guiding locomotion. To evaluate this hypothesis we studied the connectivity pattern of CSv, which is completely unknown, with a combination of diffusion MRI and resting-state functional MRI. Converging results from the 2 approaches suggest that visual drive is provided primarily by areas hV6, pVIP (putative intraparietal cortex) and PIC (posterior insular cortex). A strong connection with the medial portion of the somatosensory cortex, which represents the legs and feet, suggests that CSv may receive locomotion-relevant proprioceptive information as well as visual and vestibular signals. However, the dominant connections of CSv are with specific components of the motor system, in particular the cingulate motor areas and the supplementary motor area. We propose that CSv may provide a previously unknown link between perception and action that serves the online control of locomotion.

Global Motion Processing in Human Visual Cortical Areas V2 and V3.

Global motion perception entails the ability to extract the central direction tendency from an extended area of visual space containing widely disparate local directions. A substantial body of evidence suggests that local motion signals generated in primary visual cortex (V1) are spatially integrated to provide perception of global motion, beginning in the middle temporal area (MT) in macaques and its counterpart in humans, hMT. However, V2 and V3 also contain motion-sensitive neurons that have larger receptive fields than those found in V1, giving the potential for spatial integration of motion signals. Despite this, V2 and V3 have been overlooked as sites of global motion processing. To test, free of local-global confounds, whether human V2 and V3 are important for encoding global motion, we developed a visual stimulus that yields a global direction yet includes all possible local directions and is perfectly balanced at the local motion level. We then attempted to decode global motion direction in such stimuli with multivariate pattern classification of fMRI data. We found strong sensitivity to global motion in hMT, as expected, and also in several higher visual areas known to encode optic flow. Crucially, we found that global motion direction could be decoded in human V2 and, particularly, in V3. The results suggest the surprising conclusion that global motion processing is a key function of cortical visual areas V2 and V3. A possible purpose is to provide global motion signals to V6. SIGNIFICANCE STATEMENT Humans can readily detect the overall direction of movement in a flock of birds despite large differences in the directions of individual birds at a given moment. This ability to combine disparate motion signals across space underlies many aspects of visual motion perception and has therefore received considerable research attention. The received wisdom is that spatial integration of motion signals occurs in the cortical motion complex MT+ in both human and nonhuman primates. We show here that areas V2 and V3 in humans are also able to perform this function. We suggest that different cortical areas integrate motion signals in different ways for different purposes.

Activity in the human superior colliculus relating to endogenous saccade preparation and execution.

In recent years a small number of studies have applied functional imaging techniques to investigate visual responses in the human superior colliculus (SC), but few have investigated its oculomotor functions. Here, in two experiments, we examined activity associated with endogenous saccade preparation. We used 3-T fMRI to record the hemodynamic activity in the SC while participants were either preparing or executing saccadic eye movements. Our results showed that not only executing a saccade (as previously shown) but also preparing a saccade produced an increase in the SC hemodynamic activity. The saccade-related activity was observed in the contralateral and to a lesser extent the ipsilateral SC. A second experiment further examined the contralateral mapping of saccade-related activity with a larger range of saccade amplitudes. Increased activity was again observed in both the contralateral and ipsilateral SC that was evident for large as well as small saccades. This suggests that the ipsilateral component of the increase in BOLD is not due simply to small-amplitude saccades producing bilateral activity in the foveal fixation zone. These studies provide the first evidence of presaccadic preparatory activity in the human SC and reveal that fMRI can detect activity consistent with that of buildup neurons found in the deeper layers of the SC in studies of nonhuman primates.

Measuring response saturation in human MT and MST as a function of motion density

The human brain areas MT and MST have been studied in great detail using fMRI with regards to their motion processing properties; however, to what extent this corresponds with single cell recordings remains to be fully described. Average response over human MT+ has been shown to increase linearly with motion coherence, similar to single cell responses. In response to motion density some single cell data however suggest a rapid saturation. We ask how the combination of these responses is reflected in the population response. We measured the blood oxygen level dependent (BOLD) response function of MT and MST using a motion density signal, comparing with area V1. We used spatially fixed apertures containing motion stimuli to manipulate the area covered by motion. We found that MT and MST responded above baseline to a very minimal amount of motion and showed a rather flat response to motion density, indicative of saturation. We discuss how this may be related to the size of the receptive fields and inhibitory interactions, although necessarily residual attention effects also need to be considered. We then compared different types of motion and found no difference between coherent and random motion at any motion density, suggesting that when combining response over several motion stimuli covering the visual field, a linear relationship of MT and MST population response as a function of motion coherence might not hold.

Cortical responses to congruent and incongruent stereo cues for objects on a collision path with the observer

Abstract We explored the cortical responses to visual collision events that were presented via stimuli that changed in size (looming) or stereo-depth (binocular motion), or both. In particular we examined the differences in cortical response when the looming and binocular cues were congruent or incongruent in the collision information they provided. A stereoscopic goggle system was used within the fMRI environment and allowed us to present looming and disparity cues in isolation, or in congruent or incongruent combinations. Comparison across conditions showed that incongruent cues elicited additional activation in cortical areas know to both process error and locate objects in spatio-topic coordinates. Results are discussed in terms of cognitive and motor responses to seeing incongruent cues.

An fMRI Investigation of Preparatory Set in the Human Cerebral Cortex and Superior Colliculus for Pro- and Anti-Saccades.

Previous studies have identified several cortical regions that show larger BOLD responses during preparation and execution of anti-saccades than pro-saccades. We confirmed this finding with a greater BOLD response for anti-saccades than pro-saccades during the preparation phase in the FEF, IPS and DLPFC and in the FEF and IPS in the execution phase. We then applied multi-voxel pattern analysis (MVPA) to establish whether different neural populations are involved in the two types of saccade. Pro-saccades and anti-saccades were reliably decoded during saccade execution in all three cortical regions (FEF, DLPFC and IPS) and in IPS during saccade preparation. This indicates neural specialization, for programming the desired response depending on the task rule, in these regions. In a further study tailored for imaging the superior colliculus in the midbrain a similar magnitude BOLD response was observed for pro-saccades and anti-saccades and the two saccade types could not be decoded with MVPA. This was the case both for activity related to the preparation phase and also for that elicited during the execution phase. We conclude that separate cortical neural populations are involved in the task-specific programming of a saccade while in contrast, the SC has a role in response preparation but may be less involved in high-level, task-specific aspects of the control of saccades.

Decoding rule search domain in the left inferior frontal gyrus

Traditionally, the left hemisphere has been thought to extract mainly verbal patterns of information, but recent evidence has shown that the left Inferior Frontal Gyrus (IFG) is active during inductive reasoning in both the verbal and spatial domains. We aimed to understand whether the left IFG supports inductive reasoning in a domain-specific or domain-general fashion. To do this we used Multi-Voxel Pattern Analysis to decode the representation of domain during a rule search task. Thirteen participants were asked to extract the rule underlying streams of letters presented in different spatial locations. Each rule was either verbal (letters forming words) or spatial (positions forming geometric figures). Our results show that domain was decodable in the left prefrontal cortex, suggesting that this region represents domain-specific information, rather than processes common to the two domains. A replication study with the same participants tested two years later confirmed these findings, though the individual representations changed, providing evidence for the flexible nature of representations. This study extends our knowledge on the neural basis of goal-directed behaviors and on how information relevant for rule extraction is flexibly mapped in the prefrontal cortex.