Inhibitory synchrony as a mechanism for attentional gain modulation

Recordings from area V4 of monkeys have revealed that when the focus of attention is on a visual stimulus within the receptive field of a cortical neuron, two distinct changes can occur: The firing rate of the neuron can change and there can be an increase in the coherence between spikes and the local field potential in the gamma-frequency range (30-50 Hz). The hypothesis explored here is that these observed effects of attention could be a consequence of changes in the synchrony of local interneuron networks. We performed computer simulations of a Hodgkin-Huxley type neuron driven by a constant depolarizing current, I, representing visual stimulation and a modulatory inhibitory input representing the effects of attention via local interneuron networks. We observed that the neuron's firing rate and the coherence of its output spike train with the synaptic inputs was modulated by the degree of synchrony of the inhibitory inputs. The model suggest that the observed changes in firing rate and coherence of neurons in the visual cortex could be controlled by top-down inputs that regulated the coherence in the activity of a local inhibitory network discharging at gamma frequencies.Comment: J.Physiology (Paris) in press, 11 figure

Predictive Coding as a Model of Biased Competition in Visual Attention

Attention acts, through cortical feedback pathways, to enhance the response of cells encoding expected or predicted information. Such observations are inconsistent with the predictive coding theory of cortical function which proposes that feedback acts to suppress information predicted by higher-level cortical regions. Despite this discrepancy, this article demonstrates that the predictive coding model can be used to simulate a number of the effects of attention. This is achieved via a simple mathematical rearrangement of the predictive coding model, which allows it to be interpreted as a form of biased competition model. Nonlinear extensions to the model are proposed that enable it to explain a wider range of data

A feedback model of visual attention

Feedback connections are a prominent feature of cortical anatomy and are likely to have significant functional role in neural information processing. We present a neural network model of cortical feedback that successfully simulates neurophysiological data associated with attention. In this domain our model can be considered a more detailed, and biologically plausible, implementation of the biased competition model of attention. However, our model is more general as it can also explain a variety of other top-down processes in vision, such as figure/ground segmentation and contextual cueing. This model thus suggests that a common mechanism, involving cortical feedback pathways, is responsible for a range of phenomena and provides a unified account of currently disparate areas of research

An integrated microcircuit model of attentional processing in the neocortex

[EN] Selective attention is a fundamental cognitive function that uses top-down signals to orient and prioritize information processing in the brain. Single-cell recordings from behaving monkeys have revealed a number of attention-induced effects on sensory neurons, and have given rise to contrasting viewpoints about the neural underpinning of attentive processing. Moreover, there is evidence that attentional signals originate from the prefrontoparietal working memory network, but precisely how a source area of attention interacts with a sensory system remains unclear. To address these questions, we investigated a biophysically based network model of spiking neurons composed of a reciprocally connected loop of two (sensory and working memory) networks. We found that a wide variety of physiological phenomena induced by selective attention arise naturally in such a system. In particular, our work demonstrates a neural circuit that instantiates the "feature-similarity gain modulation principle," according to which the attentional gain effect on sensory neuronal responses is a graded function of the difference between the attended feature and the preferred feature of the neuron, independent of the stimulus. Furthermore, our model identifies key circuit mechanisms that underlie feature-similarity gain modulation, multiplicative scaling of tuning curve, and biased competition, and provide specific testable predictions. These results offer a synthetic account of the diverse attentional effects, suggesting a canonical neural circuit for feature-based attentional processing in the cortex.This work was supported by the Volkswagen Foundation, the Spanish Ministry of Education and Science (S.A., A.C.), the European Regional Development Fund (A.C.), and the Swartz Foundation (X.-J.W.). A.C. was supported by a Ramón y Cajal Research Fellowship of the Spanish Ministry of Education and Science and by the Researcher Stabilization Program of the Health Department of the Generalitat de Catalunya. We thank S. Treue for helpful discussions on feature-based attention, and E. Marder, J. Mazer, and A. Renart for helpful comments on a previous version of this manuscript.Ardid-Ramírez, JS.; Wang, X.; Compte, A. (2007). An integrated microcircuit model of attentional processing in the neocortex. Journal of Neuroscience. 27(32):8486-8495. https://doi.org/10.1523/JNEUROSCI.1145-07.2007S84868495273

Cortical Dynamics of Contextually-Cued Attentive Visual Learning and Search: Spatial and Object Evidence Accumulation

How do humans use predictive contextual information to facilitate visual search? How are consistently paired scenic objects and positions learned and used to more efficiently guide search in familiar scenes? For example, a certain combination of objects can define a context for a kitchen and trigger a more efficient search for a typical object, such as a sink, in that context. A neural model, ARTSCENE Search, is developed to illustrate the neural mechanisms of such memory-based contextual learning and guidance, and to explain challenging behavioral data on positive/negative, spatial/object, and local/distant global cueing effects during visual search. The model proposes how global scene layout at a first glance rapidly forms a hypothesis about the target location. This hypothesis is then incrementally refined by enhancing target-like objects in space as a scene is scanned with saccadic eye movements. The model clarifies the functional roles of neuroanatomical, neurophysiological, and neuroimaging data in visual search for a desired goal object. In particular, the model simulates the interactive dynamics of spatial and object contextual cueing in the cortical What and Where streams starting from early visual areas through medial temporal lobe to prefrontal cortex. After learning, model dorsolateral prefrontal cortical cells (area 46) prime possible target locations in posterior parietal cortex based on goalmodulated percepts of spatial scene gist represented in parahippocampal cortex, whereas model ventral prefrontal cortical cells (area 47/12) prime possible target object representations in inferior temporal cortex based on the history of viewed objects represented in perirhinal cortex. The model hereby predicts how the cortical What and Where streams cooperate during scene perception, learning, and memory to accumulate evidence over time to drive efficient visual search of familiar scenes.CELEST, an NSF Science of Learning Center (SBE-0354378); SyNAPSE program of Defense Advanced Research Projects Agency (HR0011-09-3-0001, HR0011-09-C-0011

Sequential presentation protects working memory from catastrophic interference

Neural network models of memory are notorious for catastrophic interference: old items are forgotten as new items are memorized (e.g., French, 1999; McCloskey & Cohen, 1989). While Working Memory (WM) in human adults shows severe capacity limitations, these capacity limitations do not reflect neural-network style catastrophic interference. However, our ability to quickly apprehend the numerosity of small sets of objects (i.e., subitizing) does show catastrophic capacity limitations, and this subitizing capacity and WM might reflect a common capacity. Accordingly, computational investigations (Knops, Piazza, Sengupta, Eger, & Melcher, 2014; Sengupta, Surampudi, & Melcher, 2014) suggest that mutual inhibition among neurons can explain both kinds of capacity limitations as well as why our ability to estimate the numerosity of larger sets is limited according to a Weber ratio signature. Based on simulations with a saliency map-like network and mathematical proofs, we provide three results. First, mutual inhibition among neurons leads to catastrophic interference when items are presented simultaneously. The network can remember a limited number of items, but when more items are presented, the network forgets all of them. Second, if memory items are presented sequentially rather than simultaneously, the network remembers the most recent items rather than forgetting all of them. Hence, the tendency in WM tasks to sequentially attend even to simultaneously presented items might not only reflect attentional limitations, but an adaptive strategy to avoid catastrophic interference. Third, the mean activation level in the network can be used to estimate the number of items in small sets, but does not accurately reflect the number of items in larger sets. Rather, we suggest that the Weber ratio signature of large number discrimination emerges naturally from the interaction between the limited precision of a numeric estimation system and a multiplicative gain control mechanism

Spatiotemporal dynamics of feature-based attention spread: evidence from combined electroencephalographic and magnetoencephalographic recordings

Attentional selection on the basis of nonspatial stimulus features induces a sensory gain enhancement by increasing the firing-rate of individual neurons tuned to the attended feature, while responses of neurons tuned to opposite feature-values are suppressed. Here we recorded event-related potentials (ERPs) and magnetic fields (ERMFs) in human observers to investigate the underlying neural correlates of feature-based attention at the population level. During the task subjects attended to a moving transparent surface presented in the left visual field, while task-irrelevant probe stimuli executing brief movements into varying directions were presented in the opposite visual field. ERP and ERMF amplitudes elicited by the unattended task-irrelevant probes were modulated as a function of the similarity between their movement direction and the task-relevant movement direction in the attended visual field. These activity modulations reflecting globally enhanced processing of the attended feature were observed to start not before 200 ms poststimulus and were localized to the motion-sensitive area hMT. The current results indicate that feature-based attention operates in a global manner but needs time to spread and provide strong support for the feature-similarity gain model

A Bayesian inference theory of attention: neuroscience and algorithms

The past four decades of research in visual neuroscience has generated a large and disparate body of literature on the role of attention [Itti et al., 2005]. Although several models have been developed to describe specific properties of attention, a theoretical framework that explains the computational role of attention and is consistent with all known effects is still needed. Recently, several authors have suggested that visual perception can be interpreted as a Bayesian inference process [Rao et al., 2002, Knill and Richards, 1996, Lee and Mumford, 2003]. Within this framework, topdown priors via cortical feedback help disambiguate noisy bottom-up sensory input signals. Building on earlier work by Rao [2005], we show that this Bayesian inference proposal can be extended to explain the role and predict the main properties of attention: namely to facilitate the recognition of objects in clutter. Visual recognition proceeds by estimating the posterior probabilities for objects and their locations within an image via an exchange of messages between ventral and parietal areas of the visual cortex. Within this framework, spatial attention is used to reduce the uncertainty in feature information; feature-based attention is used to reduce the uncertainty in location information. In conjunction, they are used to recognize objects in clutter. Here, we find that several key attentional phenomena such such as pop-out, multiplicative modulation and change in contrast response emerge naturally as a property of the network. We explain the idea in three stages. We start with developing a simplified model of attention in the brain identifying the primary areas involved and their interconnections. Secondly, we propose a Bayesian network where each node has direct neural correlates within our simplified biological model. Finally, we elucidate the properties of the resulting model, showing that the predictions are consistent with physiological and behavioral evidence

Allocation of Computational Resources in the Nervous System.

The nervous system integrates past information together with predictions about the future in order to produce rewarding actions for the organism. This dissertation focuses on the resources underlying these computations, and the task-dependent allocation of these resources. We present evidence that principles from optimal coding and optimal estimation account for overt and covert orienting phenomena, as observed from both behavioral experiments and neuronal recordings. First, we review behavioral measurements related to selective attention and discuss models that account for these data. We show that reallocation of resources emerges as a natural property of systems that encode their inputs efficiently under non-uniform constraints. We continue by discussing the attentional modulation of neuronal activity, and showthat: (1) Modulation of coding strategies does not require special mechanisms: it is possible to obtain dramatic modulation even when signals informing the system about fidelity requirements enter the system in a fashion indistinguishable from sensory signals. (2) Optimal coding under non-uniform fidelity requirements is sufficient to account for the firing rate modulation observed during selective attention experiments. (3) The response of a single neuron cannot bewell characterized by measurements of attentional modulation of only a single sensory stimulus. (4) The magnitude of the activity modulation depends on the capacity of the neural circuit. A later chapter discusses the neural mechanisms for resource allocation, and the relation between attentional mechanisms and receptive field formation. The remainder of the dissertation focuses on overt orienting phenomena and active perception. We present a theoretical analysis of the allocation of resources during state estimation of multiple targets with different uncertainties, together with eye-tracking experiments that confirm our predictions. We finish by discussing the implications of these results to our current understanding of orienting phenomena and the neural code