Integration of visual motion and pursuit signals in areas V3A and V6+ across cortical depth using 9.4T fMRI

Neural mechanisms underlying a stable perception of the world during pursuit eye movements are not fully understood. Both, perceptual stability as well as perception of real (i.e. objective) motion are the product of integration between motion signals on the retina and efference copies of eye movements. Human areas V3A and V6 have previously been shown to have strong objective ('real') motion responses. Here we used high-resolution laminar fMRI at ultra-high magnetic field (9.4T) in human subjects to examine motion integration across cortical depths in these areas. We found an increased preference for objective motion in areas V3A and V6+ i.e. V6 and possibly V6A towards the upper layers. When laminar responses were detrended to remove the upper-layer bias present in all responses, we found a unique, condition-specific laminar profile in V6+, showing reduced mid-layer responses for retinal motion only. The results provide evidence for differential, motion-type dependent laminar processing in area V6+. Mechanistically, the mid-layer dip suggests a special contribution of retinal motion to integration, either in the form of a subtractive (inhibitory) mid-layer input, or in the form of feedback into extragranular or infragranular layers. The results show that differential laminar signals can be measured in high-level motion areas in human occipitoparietal cortex, opening the prospect of new mechanistic insights using non-invasive brain imaging.

Brain state and cortical layer-specific mechanisms underlying perception at threshold

Identical stimuli can be perceived or go unnoticed across successive presentations, producing divergent behavioral readouts despite similarities in sensory input. We hypothesized that fluctuations in neurophysiological states in the sensory neocortex, which could alter cortical processing at the level of neural subpopulations, underlies this perceptual variability. We analyzed cortical layer-specific electrophysiological activity in visual area V4 during a cued attention task. We find that hit trials are characterized by a larger pupil diameter and lower incidence of microsaccades, indicative of a behavioral state with increased arousal and perceptual stability. Target stimuli presented at perceptual threshold evoke elevated multi-unit activity in V4 neurons in hit trials compared to miss trials, across all cortical layers. Putative excitatory and inhibitory neurons are strongly positively modulated in the input (IV) and deep (V & VI) layers of the cortex during hit trials. Excitatory neurons in the superficial cortical layers exhibit lower variability in hit trials. Deep layer neurons are less phase-locked to low frequency rhythms in hits. Hits are also characterized by greater interlaminar coherence between the superficial and deep layers in the pre-stimulus period, and a complementary pattern between the input layer and both the superficial and deep layers in the stimulus-evoked period. Taken together, these results indicate that a state of elevated levels of arousal and perceptual stability allow enhanced processing of sensory stimuli, which contributes to hits at perceptual threshold.

Cortex-independent open-loop control of a voluntary orofacial motor action

Whether using our eyes or our hands, we interact with our environment through mobile sensors. The efficient use of these sensory organs implies the ability to track their position; otherwise, perceptual stability and prehension would be profoundly impeded. The nervous system may be informed about the position of a sensory organ via two complementary feedback mechanisms: peripheral reafference (external, sensory feedback) and efference copy (internal feedback). Yet, the potential contributions of these mechanisms remain largely unexplored. By training rats to place their vibrissae within a predetermined angular range without contact, a task that depends on knowledge of vibrissa position relative to their face, we found that peripheral reafference is not required. The presence of motor cortex is not required either, even in the absence of peripheral reafference. On the other hand, the red nucleus, which receives descending inputs from motor cortex and the cerebellum and projects to facial motoneurons, is critical for the execution of the vibrissa task. All told, our results demonstrate the existence of an open-loop control by an internal model that is sufficient to drive voluntary motion. The internal model is independent of motor cortex and likely contains the cerebellum and associated nuclei.

Cortex-independent open-loop control of a voluntary orofacial motor action

Whether using our eyes or our hands, we interact with our environment through mobile sensors. The efficient use of these sensory organs implies the ability to track their position; otherwise, perceptual stability and prehension would be profoundly impeded. The nervous system may be informed about the position of a sensory organ via two complementary feedback mechanisms: peripheral reafference (external, sensory feedback) and efference copy (internal feedback). Yet, the potential contributions of these mechanisms remain largely unexplored. By training rats to place their vibrissae within a predetermined angular range without contact, a task that depends on knowledge of vibrissa position relative to their face, we found that peripheral reafference is not required. The presence of motor cortex is not required either, even in the absence of peripheral reafference. On the other hand, the red nucleus, which receives descending inputs from motor cortex and the cerebellum and projects to facial motoneurons, is critical for the execution of the vibrissa task. All told, our results demonstrate the existence of an open-loop control by an internal model that is sufficient to drive voluntary motion. The internal model is independent of motor cortex and likely contains the cerebellum and associated nuclei.

FUNCTIONAL SPECIFICITY IN EYE GAZE PROCESSING: EVIDENCE FROM DEVELOPMENTAL PROSOPAGNOSIA

<p>The eyes of other people subserve two core functions in human social cognition: gaze perception and face identity recognition. This thesis reports two psychophysical studies that examine the degree of functional specificity between eye gaze processing and face identity processing by testing if various aspects of gaze processing are intact in people with developmental prosopagnosia (DP) – the lifelong inability to recognise face identity. Study 1 investigates spatial integration in eye gaze perception using two tasks. DP and control participants completed one task that measured perception of gaze direction from the two eyes and another that measured the Wollaston illusion (whereby perceived eye gaze is pulled by head rotation; requiring the integration of eye and head direction). Study 2 investigates temporal integration in eye gaze perception using two tasks. The first task measured adaptation effects in eye gaze perception, which reflects sensitivity to gaze direction and its sensory representations. The second task measured serial dependence in gaze perception, which reflects temporal integration of gaze direction and its perceptual stability. Despite their deficits in recognising face identity, DP participants showed normal gaze processing across all studies. These results demonstrate the functional specificity of gaze processing and imply that gaze perception is carried out by dedicated mechanisms not used for processing identity. Our findings align with models of face processing that posit distinct pathways for gaze and identity analysis, and further clarify the selectivity of face processing dysfunctions in developmental prosopagnosia.</p>

FUNCTIONAL SPECIFICITY IN EYE GAZE PROCESSING: EVIDENCE FROM DEVELOPMENTAL PROSOPAGNOSIA

<p>The eyes of other people subserve two core functions in human social cognition: gaze perception and face identity recognition. This thesis reports two psychophysical studies that examine the degree of functional specificity between eye gaze processing and face identity processing by testing if various aspects of gaze processing are intact in people with developmental prosopagnosia (DP) – the lifelong inability to recognise face identity. Study 1 investigates spatial integration in eye gaze perception using two tasks. DP and control participants completed one task that measured perception of gaze direction from the two eyes and another that measured the Wollaston illusion (whereby perceived eye gaze is pulled by head rotation; requiring the integration of eye and head direction). Study 2 investigates temporal integration in eye gaze perception using two tasks. The first task measured adaptation effects in eye gaze perception, which reflects sensitivity to gaze direction and its sensory representations. The second task measured serial dependence in gaze perception, which reflects temporal integration of gaze direction and its perceptual stability. Despite their deficits in recognising face identity, DP participants showed normal gaze processing across all studies. These results demonstrate the functional specificity of gaze processing and imply that gaze perception is carried out by dedicated mechanisms not used for processing identity. Our findings align with models of face processing that posit distinct pathways for gaze and identity analysis, and further clarify the selectivity of face processing dysfunctions in developmental prosopagnosia.</p>

Functional Specificity In Eye Gaze Processing: Evidence From Developmental Prosopagnosia

<p>The eyes of other people subserve two core functions in human social cognition: gaze perception and face identity recognition. This thesis reports two psychophysical studies that examine the degree of functional specificity between eye gaze processing and face identity processing by testing if various aspects of gaze processing are intact in people with developmental prosopagnosia (DP) – the lifelong inability to recognise face identity. Study 1 investigates spatial integration in eye gaze perception using two tasks. DP and control participants completed one task that measured perception of gaze direction from the two eyes and another that measured the Wollaston illusion (whereby perceived eye gaze is pulled by head rotation; requiring the integration of eye and head direction). Study 2 investigates temporal integration in eye gaze perception using two tasks. The first task measured adaptation effects in eye gaze perception, which reflects sensitivity to gaze direction and its sensory representations. The second task measured serial dependence in gaze perception, which reflects temporal integration of gaze direction and its perceptual stability. Despite their deficits in recognising face identity, DP participants showed normal gaze processing across all studies. These results demonstrate the functional specificity of gaze processing and imply that gaze perception is carried out by dedicated mechanisms not used for processing identity. Our findings align with models of face processing that posit distinct pathways for gaze and identity analysis, and further clarify the selectivity of face processing dysfunctions in developmental prosopagnosia.</p>

Conscious Seeing and Invariant Recognition

This chapter explains fundamental differences between seeing and recognition, notably how and why our brains use conscious seeing to control actions like looking and reaching, while we learn both view-, size-, and view-specific object recognition categories, and view-, size-, and position-invariant object recognition categories, as our eyes search a scene during active vision. The dorsal Where cortical stream and the ventral What cortical stream interact to regulate invariant category learning by solving the View-to-Object Binding problem whereby inferotemporal, or IT, cortex associates only views of a single object with its learned invariant category. Feature-category resonances between V2/V4 and IT support category recognition. Symptoms of visual agnosia emerge when IT is lesioned. V2 and V4 interact to enable amodal completion of partially occluded objects behind their occluders, without requiring that all occluders look transparent. V4 represents the unoccluded surfaces of opaque objects and triggers a surface-shroud resonance with posterial parietal cortex, or PPC, that renders surfaces consciously visible, and enables them to control actions. Clinical symptoms of visual neglect emerge when PPC is lesioned. A unified explanation is given of data about visual crowding, situational awareness, change blindness, motion-induced blindness, visual search, perceptual stability, and target swapping. Although visual boundaries and surfaces obey computationally complementary laws, feedback between boundaries and surfaces ensure their consistency and initiate figure-ground separation, while commanding our eyes to foveate sequences of salient features on object surfaces, and thereby triggering invariant category learning. What-to-Where stream interactions enable Where’s Waldo searches for desired objects in cluttered scenes.

Learning to silence saccadic suppression

Perceptual stability is facilitated by a decrease in visual sensitivity during rapid eye movements, called saccadic suppression. While a large body of evidence demonstrates that saccadic programming is plastic, little is known about whether the perceptual consequences of saccades can be modified. Here, we demonstrate that saccadic suppression is attenuated during learning on a standard visual detection-in-noise task, to the point that it is effectively silenced. Across a period of 7 days, 44 participants were trained to detect brief, low-contrast stimuli embedded within dynamic noise, while eye position was tracked. Although instructed to fixate, participants regularly made small fixational saccades. Data were accumulated over a large number of trials, allowing us to assess changes in performance as a function of the temporal proximity of stimuli and saccades. This analysis revealed that improvements in sensitivity over the training period were accompanied by a systematic change in the impact of saccades on performance—robust saccadic suppression on day 1 declined gradually over subsequent days until its magnitude became indistinguishable from zero. This silencing of suppression was not explained by learning-related changes in saccade characteristics and generalized to an untrained retinal location and stimulus orientation. Suppression was restored when learned stimulus timing was perturbed, consistent with the operation of a mechanism that temporarily reduces or eliminates saccadic suppression, but only when it is behaviorally advantageous to do so. Our results indicate that learning can circumvent saccadic suppression to improve performance, without compromising its functional benefits in other viewing contexts.

Discrimination of Complex Odor Mixtures: A Study Using Wine Aroma Models

There are key unanswered questions when it comes to multi-component odor discrimination. This study was designed to assess discrimination of odorant mixtures that elicit a singular percept. We collected data to address the following two questions: 1) What odor features do humans notice when attempting to discriminate between subtly different odor mixtures? 2) Are odor mixtures easier to discriminate when an odorant is added, compared to when a component is removed? Using modern aroma chemistry techniques, an odor mixture resembling a generic white wine was constructed. This wine odor mixture was modified using a series of 3 esters which are commonly found in white wines that vary in chain length and branching. Participants performed a sequence of discrimination tasks for the addition / subtraction of modifiers to the base wine at different concentrations. Only one of the esters (ethyl-propanoate) led to a discriminable odor mixture. As concentration of the modifying odorant was increased, discrimination of odor mixtures was first reported because of changes in odor mixture familiarity and then intensity. We found similar sensitivity to changes in odor mixtures regardless whether the modifying compound was added or subtracted, suggesting that perceptual stability of odor mixtures is equally dependent on both imputing missing information (pattern completion) and disregarding extraneous information.