Multiple components of surround modulation in primary visual cortex: Multiple neural circuits with multiple functions?

pre-printThe responses of neurons in primary visual cortex (V1) to stimulation of their receptive field (RF) are modulated by stimuli in the RF surround. This modulation is suppressive when the stimuli in the RF and surround are of similar orientation, but less suppressive or facilitatory when they are cross-oriented. Similarly, in human vision surround stimuli selectively suppress the perceived contrast of a central stimulus. Although the properties of surround modulation have been thoroughly characterized in many species, cortical areas and sensory modalities, its role in perception remains unknown. Here we argue that surround modulation in V1 consists of multiple components having different spatio-temporal and tuning properties, generated by different neural circuits and serving different visual functions. One component arises from LGN afferents, is fast, untuned for orientation, and spatially restricted to the surround region nearest to the RF (the near-surround); its function is to normalize V1 cell responses to local contrast. Intra-V1 horizontal connections contribute a slower, narrowly orientation-tuned component to near-surround modulation, whose function is to increase the coding efficiency of natural images in manner that leads to the extraction of object boundaries. The third component is generated by topdown feedback connections to V1, is fast, broadly orientation-tuned, and extends into the far-surround; its function is to enhance the salience of behaviorally relevant visual features. Far- and near-surround modulation, thus, act as parallel mechanisms: the former quickly detects and guides saccades/attention to salient visual scene locations, the latter segments object boundaries in the scene

Border-ownership-dependent tilt aftereffect in incomplete figures

A recent physiological finding of neural coding for border ownership (BO) that defines the direction of a figure with respect to the border has provided a possible basis for figure-ground segregation. To explore the underlying neural mechanisms of BO, we investigated stimulus configurations that activate BO circuitry through psychophysical investigation of the BO-dependent tilt aftereffect (BO-TAE). Specifically, we examined robustness of the border ownership signal by determining whether the BO-TAE is observed when gestalt factors are broken. The results showed significant BO-TAEs even when a global shape was not explicitly given due to the ambiguity of the contour, suggesting a contour-independent mechanism for BO coding.This paper was published in Journal of the Optical Society of America. A and is made available as an electronic reprint with the permission of OSA. The paper can be found at the following URL on the OSA website: http://www.opticsinfobase.org/abstract.cfm?URI=josaa-24-1-18. Systematic or multiple reproduction or distribution to multiple locations via electronic or other means is prohibited and is subject to penalties under law

Doctor of Philosophy

dissertationThe primary visual cortex (V1) receives feedback projections from extrastriate visual cortical areas of a magnitude comparable to the feedforward projections it sends to them. Classically, this input has been thought to subserve "top-down" cognitive functions such as visual attention. Recently, it has been suggested that feedback could play role in more basic computations like surround modulation - the modulation of neuronal response by stimuli outside its receptive field (RF). The neural circuits and mechanisms generating such modulation remain unknown. A guiding hypothesis of this work is that feedback connections play an important role in this contextual computation. Using single unit electrophysiological recordings we have investigated the modulatory effects arising from the surround region of V1 neurons thought to be subserved by feedback connections, a region we term the ‘far' surround. We find that such modulation can be very specifically influence the response of the neuron to a stimulus inside its RF. First, by recording V1 neuron responses to an optimally oriented grating inside the neuron's RF while changing the orientation of a grating in the surround, we find that far-surround modulation is orientation-tuned, suggesting orientation specificity of the feedback connections themselves. Second, using grating stimuli confined to the ‘near' or ‘far' surround region, we find that the far surround is more broadly orientation-tuned than the near surround, perhaps indicating lesser specificity of feedback than horizontal connections. Third, using center and surround iv gratings both changing in orientation, we find that the surround is tuned to the stimulus presented to the V1 cells' receptive field, rather than to the neuron's preferred orientation. Specifically, the response of the neuron becomes maximally suppressed when the stimuli in the center and the surround are of the same orientation, irrespective of the preferred orientation of the neuron, and becomes less suppressed as the orientation difference increases, switching to facilitation in some instances. Thus, V1 neurons adapt their response to represent the orientation difference between the stimuli in the RF and the surround, and this is true across the range of the neuron's orientation tuning curve. Using computational modeling, we find that this mechanism can emerge from the dynamic interaction of orientation-specific horizontal and/or feedback connections with strong local recurrent connections. We suggest that such a mechanism may serve to enhance V1 responses to local orientation contrast, therefore increasing visual target saliency

Neural Models of Motion Integration, Segmentation, and Probablistic Decision-Making

When brain mechanism carry out motion integration and segmentation processes that compute unambiguous global motion percepts from ambiguous local motion signals? Consider, for example, a deer running at variable speeds behind forest cover. The forest cover is an occluder that creates apertures through which fragments of the deer's motion signals are intermittently experienced. The brain coherently groups these fragments into a trackable percept of the deer in its trajectory. Form and motion processes are needed to accomplish this using feedforward and feedback interactions both within and across cortical processing streams. All the cortical areas V1, V2, MT, and MST are involved in these interactions. Figure-ground processes in the form stream through V2, such as the seperation of occluding boundaries of the forest cover from the boundaries of the deer, select the motion signals which determine global object motion percepts in the motion stream through MT. Sparse, but unambiguous, feauture tracking signals are amplified before they propogate across position and are intergrated with far more numerous ambiguous motion signals. Figure-ground and integration processes together determine the global percept. A neural model predicts the processing stages that embody these form and motion interactions. Model concepts and data are summarized about motion grouping across apertures in response to a wide variety of displays, and probabilistic decision making in parietal cortex in response to random dot displays.National Science Foundation (SBE-0354378); Office of Naval Research (N00014-01-1-0624

Cortical Surround Interactions and Perceptual Salience via Natural Scene Statistics

Spatial context in images induces perceptual phenomena associated with salience and modulates the responses of neurons in primary visual cortex (V1). However, the computational and ecological principles underlying contextual effects are incompletely understood. We introduce a model of natural images that includes grouping and segmentation of neighboring features based on their joint statistics, and we interpret the firing rates of V1 neurons as performing optimal recognition in this model. We show that this leads to a substantial generalization of divisive normalization, a computation that is ubiquitous in many neural areas and systems. A main novelty in our model is that the influence of the context on a target stimulus is determined by their degree of statistical dependence. We optimized the parameters of the model on natural image patches, and then simulated neural and perceptual responses on stimuli used in classical experiments. The model reproduces some rich and complex response patterns observed in V1, such as the contrast dependence, orientation tuning and spatial asymmetry of surround suppression, while also allowing for surround facilitation under conditions of weak stimulation. It also mimics the perceptual salience produced by simple displays, and leads to readily testable predictions. Our results provide a principled account of orientation-based contextual modulation in early vision and its sensitivity to the homogeneity and spatial arrangement of inputs, and lends statistical support to the theory that V1 computes visual salience

Doctor of Philosophy

dissertationPrimate primary visual cortex (V1) consists of six anatomical layers. There are both heterogeneous and homogeneous functional properties found across layers. Surround modulation (SM) occurs when neuronal responses to stimulation of a neuron's receptive field (RF) is modulated by simultaneous simulation outside of the RF. There are three potential candidates for SM: feedforward (FF) and intra-V1 horizontal (HZ) connections underpin the region nearby RF (near surround), while the modulatory signal arising from distant regions (far surround) are conveyed by feedback (FB) connections from higher visual areas. Also, V1 layers show distinct patterns of FF, HZ, and FB terminations. The goal of my dissertation research was to study 1) the properties of SM across V1 layers, 2) how simple visual stimuli in the RF and surround of a V1 column activate V1 layers, and (3) what specific afferent circuits to and within the V1 column of these stimuli recruit. Using single electrode recordings sampling from all the layers of V1, I found that near SM is more sharply orientation-tuned in the superficial layers (L3B, 4B and 4C?), where there are prominent horizontal connections. However, far SM is more orientation-tuned in L4B, possibly reflecting the orientation organization of feedback connections to this layer. Using laminar recordings, I investigated the temporal dynamics of inputs (local field potentials, LFPs) to each layer when stimulating surround elements. Near surround stimulation simultaneously localized the first inputs in superficial and deep layers with a significant delay in L4C, suggesting both HZ and FB contribute to near SM. Feedback recipient layers (L1/2A and L5/6) received the earliest inputs with far surround stimulation. Measuring the latency of spiking activity while co-stimulating RF and surround, the untuned near SM first emerged in L4C, but, tuned near SM and far SM, emerged outside thalamic recipient layers, suggesting a cortical origin. Finally, I found that brain oscillations in response to stimuli in the surround, mirror the structure of the underlying horizontal and feedback connections. Grating patches positioned on the collinear axis to a cell's preferred orientation, evoke a greater power in different frequency bands of LFP, including alpha, beta, and gamma, compared to orthogonal position in both near and far surround. We propose that horizontal and feedback connections, substrates of near and far surround, are aligned collinearly in the visual field and help generate brain oscillations

Towards a Unified View on Pathways and Functions of Neural Recurrent Processing

There are three neural feedback pathways to the primary visual cortex (V1): corticocortical, pulvinocortical, and cholinergic. What are the respective functions of these three projections? Possible functions range from contextual modulation of stimulus processing and feedback of high-level information to predictive processing (PP). How are these functions subserved by different pathways and can they be integrated into an overarching theoretical framework? We propose that corticocortical and pulvinocortical connections are involved in all three functions, whereas the role of cholinergic projections is limited by their slow response to stimuli. PP provides a broad explanatory framework under which stimulus-context modulation and high-level processing are subsumed, involving multiple feedback pathways that provide mechanisms for inferring and interpreting what sensory inputs are about

Change blindness: eradication of gestalt strategies

Arrays of eight, texture-defined rectangles were used as stimuli in a one-shot change blindness (CB) task where there was a 50% chance that one rectangle would change orientation between two successive presentations separated by an interval. CB was eliminated by cueing the target rectangle in the first stimulus, reduced by cueing in the interval and unaffected by cueing in the second presentation. This supports the idea that a representation was formed that persisted through the interval before being 'overwritten' by the second presentation (Landman et al, 2003 Vision Research 43149–164]. Another possibility is that participants used some kind of grouping or Gestalt strategy. To test this we changed the spatial position of the rectangles in the second presentation by shifting them along imaginary spokes (by ±1 degree) emanating from the central fixation point. There was no significant difference seen in performance between this and the standard task [F(1,4)=2.565, p=0.185]. This may suggest two things: (i) Gestalt grouping is not used as a strategy in these tasks, and (ii) it gives further weight to the argument that objects may be stored and retrieved from a pre-attentional store during this task

Laminar Cortical Dynamics of Visual Form and Motion Interactions During Coherent Object Motion Perception

How do visual form and motion processes cooperate to compute object motion when each process separately is insufficient? A 3D FORMOTION model specifies how 3D boundary representations, which separate figures from backgrounds within cortical area V2, capture motion signals at the appropriate depths in MT; how motion signals in MT disambiguate boundaries in V2 via MT-to-Vl-to-V2 feedback; how sparse feature tracking signals are amplified; and how a spatially anisotropic motion grouping process propagates across perceptual space via MT-MST feedback to integrate feature-tracking and ambiguous motion signals to determine a global object motion percept. Simulated data include: the degree of motion coherence of rotating shapes observed through apertures, the coherent vs. element motion percepts separated in depth during the chopsticks illusion, and the rigid vs. non-rigid appearance of rotating ellipses.Air Force Office of Scientific Research (F49620-01-1-0397); National Geospatial-Intelligence Agency (NMA201-01-1-2016); National Science Foundation (BCS-02-35398, SBE-0354378); Office of Naval Research (N00014-95-1-0409, N00014-01-1-0624