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Involvement of the dorsal and ventral attention networks in oddball stimulus processing: a meta-analysis.

ABSTRACT: The aim of this study was to provide the first, comprehensive meta-analysis of the neuroimaging literature regarding greater neural responses to a deviant stimulus in a stream of repeated, standard stimuli, termed here oddball effects. The meta-analysis of 75 independent studies included a comparison of auditory and visual oddball effects and task-relevant and task-irrelevant oddball effects. The results were interpreted with reference to the model in which a large-scale dorsal frontoparietal network embodies a mechanism for orienting attention to the environment, whereas a large-scale ventral frontoparietal network supports the detection of salient, environmental changes. The meta-analysis yielded three main sets of findings. First, ventral network regions were strongly associated with oddball effects and largely common to auditory and visual modalities, indicating a supramodal "alerting" system. Most ventral network components were more strongly associated with task-relevant than task-irrelevant oddball effects, indicating a dynamic interplay of stimulus saliency and internal goals in stimulus-driven engagement of the network. Second, the bilateral inferior frontal junction, an anterior core of the dorsal network, was strongly associated with oddball effects, suggesting a central role in top-down attentional control. However, other dorsal network regions showed no or only modest association with oddball effects, likely reflecting active engagement during both oddball and standard stimulus processing. Finally, prominent oddball effects outside the two networks included the sensory cortex regions, likely reflecting attentive and preattentive modulation of early sensory activity, and subcortical regions involving the putamen, thalamus, and other areas, likely reflecting subcortical involvement in alerting responses.

SUBMITTER: Kim H

PROVIDER: S-EPMC6868981 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The need for fast and dynamic processing of relevant information imposes high demands onto the flexibility and efficiency of the nervous system. A good example for such flexibility is the attention-dependent selection of relevant sensory information. Studies investigating attentional modulations of neuronal responses to simultaneously arriving input showed that neurons respond, as if only the attended stimulus would be present within their receptive fields (RF). However, attention also improves neuronal representation and behavioral performance, when only one stimulus is present. Thus, attention serves for selecting relevant input and changes the neuronal processing of signals representing selected stimuli, ultimately leading to a more efficient behavioral performance. Here, we tested the hypothesis that attention configures the strength of functional coupling between a local neuronal network's neurons specifically for effective processing of signals representing attended stimuli. This coupling is measured as the strength of ?-synchronization between these neurons. The hypothesis predicts that the pattern of synchronization in local networks should depend on which stimulus is attended. Furthermore, we expect this pattern to be similar for the attended stimulus presented alone or together with irrelevant stimuli in the RF. To test these predictions, we recorded spiking-activity and local field potentials (LFP) with closely spaced electrodes in area V4 of monkeys performing a demanding attention task. Our results show that the ?-band phase coherence (?-PhC) between spiking-activity and the LFP, as well as the spiking-activity of two groups of neurons, strongly depended on which of the two stimuli in the RF was attended. The ?-PhC was almost identical for the attended stimulus presented either alone or together with a distractor. The functional relevance of dynamic ?-band synchronization is further supported by the observation of strongly degraded ?-PhC before behavioral errors, while firing rates were barely affected. These qualitatively different results point toward a failure of attention-dependent top-down mechanisms to correctly synchronize the local neuronal network in V4, even though this network receives the correctly selected input. These findings support the idea of a flexible, demand-dependent dynamic configuration of local neuronal networks, for performing different functions, even on the same sensory input.

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Involvement of the dorsal and ventral attention networks in oddball stimulus processing: a meta-analysis.

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