A model for attentional information routing through coherence predicts biased competition and multistable perception

Daniel Harnack, Udo Alexander Ernst, Klaus Richard Pawelzik
2015 Journal of Neurophysiology  
Harnack D, Ernst UA, Pawelzik KR. A model for attentional information routing through coherence predicts biased competition and multistable perception. Selective attention allows to focus on relevant information and to ignore distracting features of a visual scene. These principles of information processing are reflected in response properties of neurons in visual area V4: if a neuron is presented with two stimuli in its receptive field, and one is attended, it responds as if the nonattended
more » ... mulus was absent (biased competition). In addition, when the luminance of the two stimuli is temporally and independently varied, local field potentials are correlated with the modulation of the attended stimulus and not, or much less, correlated with the nonattended stimulus (information routing). To explain these results in one coherent framework, we present a two-layer spiking cortical network model with distancedependent lateral connectivity and converging feed-forward connections. With oscillations arising inherently from the network structure, our model reproduces both experimental observations. Hereby, lateral interactions and shifts of relative phases between sending and receiving layers (communication through coherence) are identified as the main mechanisms underlying both biased competition as well as selective routing. Exploring the parameter space, we show that the effects are robust and prevalent over a broad range of parameters. In addition, we identify the strength of lateral inhibition in the first model layer as crucial for determining the working regime of the system: increasing lateral inhibition allows a transition from a network configuration with mixed representations to one with bistable representations of the competing stimuli. The latter is discussed as a possible neural correlate of multistable perception phenomena such as binocular rivalry. biased competition; multistable perception; coherence; attention; routing IT IS A WIDESPREAD BELIEF that the brain has limited resources available for information processing (Marois and Ivanoff 2005) . Selective attention provides a means of efficient and flexible operation under this restriction by allowing preferential allocation of processing resources to a particular area or feature in the visual scenery while ignoring distractors. Hints towards the mechanisms selective attention employs are provided by two seminal studies. By showing a preferred and a nonpreferred stimulus at separate spatial locations to a V4 neuron, Moran and Desimone (1985) discovered that presenting both at the same time results in an averaged rate between the rates the stimuli would elicit if presented alone. Attending one stimulus biased the response towards the rate the attended stimulus would evoke if presented alone (biased competition). These results suggest that attention selectively modulates the information flow through the visual hierarchy. Grothe et al. (2015) tested this hypothesis directly for the first time: by independently varying the luminance of two stimuli eliciting equally strong responses in V4 neurons, it was found that the luminance modulation of the attended stimulus was represented in the neuronal activity, but the modulation of the nonattended stimulus, however, was represented to a much lesser degree. Fries (2005) proposed a possible mechanistic explanation for these effects by introducing the concept of "Communication through Coherence" (CTC): a neuron with oscillating membrane potential can be driven to fire by relatively weak input when it is close to the threshold, while if it is in a phase of low excitability, even stronger input might fail to elicit an action potential. Thus shifting relative phases of oscillating sending and receiving populations could be utilized to gate information. Experimental support is provided by the findings that attention increases synchrony of ␥-oscillations within V4 (Taylor et al. 2005; Fries et al. 2001 Fries et al. , 2008 , that communication between different populations oscillating in the ␥-band is most effective for a specific phase relation (Womelsdorf et al. 2007) , and that the ␥-coherence between neuronal ensembles in V1 and V4 is elevated under attention (Grothe et al. 2012; Bosman et al. 2012) . Also, Gregoriou et al. (2009) showed that CTC might be used for effective communication between the frontal eye field and V4. Several models were conceived that exploit oscillatory dynamics to explain information routing or biased competition Montijn et al. 2012; Mishra et al. 2006) . However, there is no model that has been shown to reproduce both key experimental findings in a unifying framework while implementing a phase-shifting mechanism in a biologically plausible manner. We hypothesize that feed-forward networks of recurrently coupled, mixed excitatory and inhibitory neurons with distance-dependent lateral interaction are capable of achieving just that. By constructing a two-layered, fan-in feed-forward system with lateral connectivity, mimicking the convergent architecture of the visual system, we show that intrinsically generated oscillations "self-organize" their relative phase relations to optimize information transmission for attended stimuli. This enables our model to reproduce both biased competition and information routing. We query the robustness of our finding and confirm that both effects are observed over a broad range of relevant model parameters. Furthermore, we identify different working regimes of the model, enabling both mixed and bistable representations of the competing stimuli, which estab-
doi:10.1152/jn.01038.2014 pmid:26108958 pmcid:PMC4563023 fatcat:ukjvsauqujarjbzshcm3j3y6dq