Probabilistic modeling of eye movement data during conjunction search via feature-based attention

Where the eyes fixate during search is not random; rather, gaze reflects the combination of information about the target and the visual input. It is not clear, however, what information about a target is used to bias the underlying neuronal responses. We here engage subjects in a variety of simple conjunction search tasks while tracking their eye movements. We derive a generative model that reproduces these eye movements and calculate the conditional probabilities that observers fixate, given the target, on or near an item in the display sharing a specific feature with the target. We use these probabilities to infer which features were biased by top-down attention: Color seems to be the dominant stimulus dimension for guiding search, followed by object size, and lastly orientation. We use the number of fixations it took to find the target as a measure of task difficulty. We find that only a model that biases multiple feature dimensions in a hierarchical manner can account for the data. Contrary to common assumptions, memory plays almost no role in search performance. Our model can be fit to average data of multiple subjects or to individual subjects. Small variations of a few key parameters account well for the intersubject differences. The model is compatible with neurophysiological findings of V4 and frontal eye fields (FEF) neurons and predicts the gain modulation of these cells

Task-demands can immediately reverse the effects of sensory-driven saliency in complex visual stimuli

In natural vision both stimulus features and task-demands affect an observer's attention. However, the relationship between sensory-driven (“bottom-up”) and task-dependent (“top-down”) factors remains controversial: Can task-demands counteract strong sensory signals fully, quickly, and irrespective of bottom-up features? To measure attention under naturalistic conditions, we recorded eye-movements in human observers, while they viewed photographs of outdoor scenes. In the first experiment, smooth modulations of contrast biased the stimuli's sensory-driven saliency towards one side. In free-viewing, observers' eye-positions were immediately biased toward the high-contrast, i.e., high-saliency, side. However, this sensory-driven bias disappeared entirely when observers searched for a bull's-eye target embedded with equal probability to either side of the stimulus. When the target always occurred in the low-contrast side, observers' eye-positions were immediately biased towards this low-saliency side, i.e., the sensory-driven bias reversed. Hence, task-demands do not only override sensory-driven saliency but also actively countermand it. In a second experiment, a 5-Hz flicker replaced the contrast gradient. Whereas the bias was less persistent in free viewing, the overriding and reversal took longer to deploy. Hence, insufficient sensory-driven saliency cannot account for the bias reversal. In a third experiment, subjects searched for a spot of locally increased contrast (“oddity”) instead of the bull's-eye (“template”). In contrast to the other conditions, a slight sensory-driven free-viewing bias prevails in this condition. In a fourth experiment, we demonstrate that at known locations template targets are detected faster than oddity targets, suggesting that the former induce a stronger top-down drive when used as search targets. Taken together, task-demands can override sensory-driven saliency in complex visual stimuli almost immediately, and the extent of overriding depends on the search target and the overridden feature, but not on the latter's free-viewing saliency

Collective stability of networks of winner-take-all circuits

The neocortex has a remarkably uniform neuronal organization, suggesting that common principles of processing are employed throughout its extent. In particular, the patterns of connectivity observed in the superficial layers of the visual cortex are consistent with the recurrent excitation and inhibitory feedback required for cooperative-competitive circuits such as the soft winner-take-all (WTA). WTA circuits offer interesting computational properties such as selective amplification, signal restoration, and decision making. But, these properties depend on the signal gain derived from positive feedback, and so there is a critical trade-off between providing feedback strong enough to support the sophisticated computations, while maintaining overall circuit stability. We consider the question of how to reason about stability in very large distributed networks of such circuits. We approach this problem by approximating the regular cortical architecture as many interconnected cooperative-competitive modules. We demonstrate that by properly understanding the behavior of this small computational module, one can reason over the stability and convergence of very large networks composed of these modules. We obtain parameter ranges in which the WTA circuit operates in a high-gain regime, is stable, and can be aggregated arbitrarily to form large stable networks. We use nonlinear Contraction Theory to establish conditions for stability in the fully nonlinear case, and verify these solutions using numerical simulations. The derived bounds allow modes of operation in which the WTA network is multi-stable and exhibits state-dependent persistent activities. Our approach is sufficiently general to reason systematically about the stability of any network, biological or technological, composed of networks of small modules that express competition through shared inhibition.Comment: 7 Figure

Activity of human hippocampal and amygdala neurons during retrieval of declarative memories

Episodic memories allow us to remember not only that we have seen an item before but also where and when we have seen it (context). Sometimes, we can confidently report that we have seen something (familiarity) but cannot recollect where or when it was seen. Thus, the two components of episodic recall, familiarity and recollection, can be behaviorally dissociated. It is not clear, however, whether these two components of memory are represented separately by distinct brain structures or different populations of neurons in a single anatomical structure. Here, we report that the spiking activity of single neurons in the human hippocampus and amygdala [the medial temporal lobe (MTL)] contain information about both components of memory. We analyzed a class of neurons that changed its firing rate to the second presentation of a previously novel stimulus. We found that the neuronal activity evoked by the presentation of a familiar stimulus (during retrieval) distinguishes stimuli that will be successfully recollected from stimuli that will not be recollected. Importantly, the ability to predict whether a stimulus is familiar is not influenced by whether the stimulus will later be recollected. We thus conclude that human MTL neurons contain information about both components of memory. These data support a continuous strength of memory model of MTL function: the stronger the neuronal response, the better the memory

Competition through selective inhibitory synchrony

Models of cortical neuronal circuits commonly depend on inhibitory feedback to control gain, provide signal normalization, and to selectively amplify signals using winner-take-all (WTA) dynamics. Such models generally assume that excitatory and inhibitory neurons are able to interact easily, because their axons and dendrites are co-localized in the same small volume. However, quantitative neuroanatomical studies of the dimensions of axonal and dendritic trees of neurons in the neocortex show that this co-localization assumption is not valid. In this paper we describe a simple modification to the WTA circuit design that permits the effects of distributed inhibitory neurons to be coupled through synchronization, and so allows a single WTA to be distributed widely in cortical space, well beyond the arborization of any single inhibitory neuron, and even across different cortical areas. We prove by non-linear contraction analysis, and demonstrate by simulation that distributed WTA sub-systems combined by such inhibitory synchrony are inherently stable. We show analytically that synchronization is substantially faster than winner selection. This circuit mechanism allows networks of independent WTAs to fully or partially compete with each other.Comment: in press at Neural computation; 4 figure

Solving constraint-satisfaction problems with distributed neocortical-like neuronal networks

Finding actions that satisfy the constraints imposed by both external inputs and internal representations is central to decision making. We demonstrate that some important classes of constraint satisfaction problems (CSPs) can be solved by networks composed of homogeneous cooperative-competitive modules that have connectivity similar to motifs observed in the superficial layers of neocortex. The winner-take-all modules are sparsely coupled by programming neurons that embed the constraints onto the otherwise homogeneous modular computational substrate. We show rules that embed any instance of the CSPs planar four-color graph coloring, maximum independent set, and Sudoku on this substrate, and provide mathematical proofs that guarantee these graph coloring problems will convergence to a solution. The network is composed of non-saturating linear threshold neurons. Their lack of right saturation allows the overall network to explore the problem space driven through the unstable dynamics generated by recurrent excitation. The direction of exploration is steered by the constraint neurons. While many problems can be solved using only linear inhibitory constraints, network performance on hard problems benefits significantly when these negative constraints are implemented by non-linear multiplicative inhibition. Overall, our results demonstrate the importance of instability rather than stability in network computation, and also offer insight into the computational role of dual inhibitory mechanisms in neural circuits.Comment: Accepted manuscript, in press, Neural Computation (2018

Time course of target recognition in visual search

Visual search is a ubiquitous task of great importance: it allows us to quickly find the objects that we are looking for. During active search for an object (target), eye movements are made to different parts of the scene. Fixation locations are chosen based on a combination of information about the target and the visual input. At the end of a successful search, the eyes typically fixate on the target. But does this imply that target identification occurs while looking at it? The duration of a typical fixation (~170ms) and neuronal latencies of both the oculomotor system and the visual stream indicate that there might not be enough time to do so. Previous studies have suggested the following solution to this dilemma: the target is identified extrafoveally and this event will trigger a saccade towards the target location. However this has not been experimentally verified. Here we test the hypothesis that subjects recognize the target before they look at it using a search display of oriented colored bars. Using a gaze-contingent real-time technique, we prematurely stopped search shortly after subjects fixated the target. Afterwards, we asked subjects to identify the target location. We find that subjects can identify the target location even when fixating on the target for less than 10ms. Longer fixations on the target do not increase detection performance but increase confidence. In contrast, subjects cannot perform this task if they are not allowed to move their eyes. Thus, information about the target during conjunction search for colored oriented bars can, in some circumstances, be acquired at least one fixation ahead of reaching the target. The final fixation serves to increase confidence rather then performance, illustrating a distinct role of the final fixation for the subjective judgment of confidence rather than accuracy

Human episodic memory retrieval is accompanied by a neural contiguity effect

Cognitive psychologists have long hypothesized that experiences are encoded in a temporal context that changes gradually over time. When an episodic memory is retrieved, the state of context is recovered—a jump back in time. We recorded from single units in the MTL of epilepsy patients performing an item recognition task. The population vector changed gradually over minutes during presentation of the list. When a probe from the list was remembered with high confidence, the population vector reinstated the temporal context of the original presentation of that probe during study—a neural contiguity effect that provides a possible mechanism for behavioral contiguity effects. This pattern was only observed for well-remembered probes; old probes that were not well-remembered showed an anti-contiguity effect. These results constitute the first direct evidence that recovery of an episodic memory in humans is associated with retrieval of a gradually-changing state of temporal context—a neural “jump-back-in-time” that parallels the act of remembering

Synthesizing cognition in neuromorphic electronic systems

The quest to implement intelligent processing in electronic neuromorphic systems lacks methods for achieving reliable behavioral dynamics on substrates of inherently imprecise and noisy neurons. Here we report a solution to this problem that involves first mapping an unreliable hardware layer of spiking silicon neurons into an abstract computational layer composed of generic reliable subnetworks of model neurons and then composing the target behavioral dynamics as a “soft state machine” running on these reliable subnets. In the first step, the neural networks of the abstract layer are realized on the hardware substrate by mapping the neuron circuit bias voltages to the model parameters. This mapping is obtained by an automatic method in which the electronic circuit biases are calibrated against the model parameters by a series of population activity measurements. The abstract computational layer is formed by configuring neural networks as generic soft winner-take-all subnetworks that provide reliable processing by virtue of their active gain, signal restoration, and multistability. The necessary states and transitions of the desired high-level behavior are then easily embedded in the computational layer by introducing only sparse connections between some neurons of the various subnets. We demonstrate this synthesis method for a neuromorphic sensory agent that performs real-time context-dependent classification of motion patterns observed by a silicon retina

The relation of phase noise and luminance contrast to overt attention in complex visual stimuli

Models of attention are typically based on difference maps in low-level features but neglect higher order stimulus structure. To what extent does higher order statistics affect human attention in natural stimuli? We recorded eye movements while observers viewed unmodified and modified images of natural scenes. Modifications included contrast modulations (resulting in changes to first- and second-order statistics), as well as the addition of noise to the Fourier phase (resulting in changes to higher order statistics). We have the following findings: (1) Subjects' interpretation of a stimulus as a “natural” depiction of an outdoor scene depends on higher order statistics in a highly nonlinear, categorical fashion. (2) Confirming previous findings, contrast is elevated at fixated locations for a variety of stimulus categories. In addition, we find that the size of this elevation depends on higher order statistics and reduces with increasing phase noise. (3) Global modulations of contrast bias eye position toward high contrasts, consistent with a linear effect of contrast on fixation probability. This bias is independent of phase noise. (4) Small patches of locally decreased contrast repel eye position less than large patches of the same aggregate area, irrespective of phase noise. Our findings provide evidence that deviations from surrounding statistics, rather than contrast per se, underlie the well-established relation of contrast to fixation