CONEUR-459; NO OF PAGES 7 The role of neuronal synchronization in selective attention Thilo Womelsdorf and Pascal Fries Attention selectively enhances the influence of neuronal distant areas, ultimately enhancing effective interactions responses conveying information about relevant sensory among those neuronal groups that convey the behaviou- attributes. Accumulating evidence suggests that this selective rally relevant information [3]. neuronal modulation relies on rhythmic synchronization at local and long-range spatial scales: attention selectively Growing evidence suggests that both of these neuronal synchronizes the rhythmic responses of those neurons that are characteristics of selective attention depend on selective tuned to the spatial and featural attributes of the attended neuronal synchronization. Attention selectively modulates sensory input. The strength of synchronization is thereby which neurons synchronize their responses with the rhyth- functionally related to perceptual accuracy and behavioural mic fluctuation of a local functional group of neurons that efficiency. Complementing this synchronization at a local level, represents the attended stimulus feature or position. Like- attention has recently been demonstrated to regulate which wise, the influence of selective attention to shape neuronal locally synchronized neuronal groups phase-synchronize their interactions among distant neuronal populations is likely to rhythmic activity across long-range connections. These results recruit selective synchronization. Such long-range synchro- point to a general computational role for selective nization of locally enhanced neuronal representations has synchronization in dynamically controlling which neurons long been implicated in attention, but only recent studies communicate information about sensory inputs effectively. demonstrate that neuronal representations that pertain to attended, relevant information are mutually phase-syn- Addresses FC Donders Centre for Cognitive Neuroimaging, Radboud University chronized across long distances. Nijmegen, Kapittelweg 29, 6525 EN Nijmegen, The Netherlands In this article we review evidence, gathered over the past Corresponding author: Womelsdorf, Thilo two years from animal and human studies, that suggests a ([email protected]) functional role for local and long-range selective synchro- nization of rhythmic neuronal activity. The view emer- Current Opinion in Neurobiology 2007, 17:1–7 ging from these studies is that synchronization might reflect a basic computational principle that underlies This review comes from a themed issue on the dynamic control of effective interactions along selec- Cognitive neuroscience Edited by Keiji Tanaka and Takeo Watanabe tive subsets of the anatomically possible neuronal con- nections [4]. 0959-4388/$ – see front matter Selective synchronization and spatial # 2006 Elsevier Ltd. All rights reserved. attention Investigating the influence of selective attention on DOI 10.1016/j.conb.2007.02.002 neuronal synchronization depends on tasks in which there is identical sensory stimulation across conditions but covert attention is directed to different aspects of this Introduction sensory input. Based on such tasks, visual cortical neurons Voluntary ‘top-down’ attention is a key mechanism to that have receptive fields overlapping with an attended select relevant subsets of sensory information for detailed stimulus synchronize their spiking responses more and effective processing and to actively suppress distract- strongly with the local field potential (LFP) than do ing irrelevant sensory information. The behavioural con- neurons that are activated by a non-attended stimu- sequences of attentional selection are manifold and lus [5]. This early finding from monkey visual area V4 include faster processing and reaction times, higher has recently been extended by showing a rather continu- accuracy levels, enhanced sensitivity for fine changes ous relationship between the strength of selective syn- and increased apparent contrast. These behavioural con- chronization and behavioural performance [6]. In this sequences of attention are accomplished by highly selec- study, attention was spatially cued to select one of two tive modulation of neuronal responses at two spatial stimuli to detect a colour change of the attended stimulus. scales of processing: within and across cortical regions. The speed of detecting the behaviourally relevant colour First, attention enhances the neuronal representation of change in an attended stimulus varied across trials and attended sensory input within the local neuronal popu- could be partially predicted by the degree of synchroni- lations that are tuned to the attended spatial [1] or featural zation in response to that stimulus. Notably, synchroniza- [2] dimensions. Second, selective attention regulates tion in the gamma-frequency band (40–100 Hz) predicted the communication among neuronal groups in spatially the speed of change detection shortly before the colour www.sciencedirect.com Current Opinion in Neurobiology 2007, 17:1–7 Please cite this article in press as: Womelsdorf T, Fries P, The role of neuronal synchronization in selective attention, Curr Opin Neurobiol (2007), doi:10.1016/j.conb.2007.02.002 CONEUR-459; NO OF PAGES 7 2 Cognitive neuroscience change had occurred. This finding suggests that the Recent EEG and MEG recordings in humans also processing or the signalling of a sensory change is more complement the results from monkey cortex about the efficient when it is handled by an area that is engaged in functional relevance of gamma-band oscillations, by enhanced gamma-band synchronization [6]. demonstrating a relationship to response times [22] and accuracy [16]. Although macroscopic EEG and MEG Importantly, the influence of local synchronization of recordings in humans are limited in how precisely they behavioural responses was spatially selective: neurons can locate the cortical sources of the observed attentional activated by an unattended stimulus showed the lowest effects, they have the advantage of enabling the functional synchronization when the monkeys were particularly fast coupling to be analyzed across distant cortical areas. With in detecting changes of the attended stimulus that were regard to attentional processing, this is demonstrated in a outside their neuronal receptive fields [6]. Thus, the recent human EEG study [23], which cued attention to strength of synchronization is modulated at a fine spatial either global or local letter stimuli and reports phase syn- scale in the visual cortex, being upregulated and down- chronization selectively among bilateral parietal sites regulated for neuronal groups that process relevant and during global attention suggestive of selective interhemi- distracting information, respectively. This finding rules spheric integration. out a possible influence of globally increased synchroni- zation during states of enhanced alertness and arousal Feature-based attention and selective (compare with [7–9]). synchronization Attention does more than synchronize the responses of In addition to using reaction time as a measure of beha- neurons based on the spatial proximity of their receptive vioural performance, a recent study [10] successfully fields to the focus of attention. Recent evidence demon- used an error analysis based on gamma-band synchroni- strates that attention to a particular feature selectively zation to predict the spatial focus of attention in macaque synchronizes the responses of those sensory neurons that visual cortex. Taylor et al. cued attention to one of two are tuned to the attended feature. Bichot et al. [24] visual shapes, both of which changed continuously recorded neuronal spiking responses and LFPs in macaque throughout the trial. Monkeys had to track the cued visual area V4 while monkeys searched in multi-stimulus shape to detect the reoccurrence of its first outline. displays for a target stimulus defined by colour, shape or Epidurally-recorded field potentials revealed a strong both. When monkeys searched, for example for a red attentional effect, with enhanced gamma-band synchro- stimulus, by shifting their gaze across stimuli on the dis- nization in response to the attended shape within visual play, the receptive fields of the recorded neurons could area V4. This effect was stronger for correct trials than for encompass either non-target stimuli (e.g. of blue colour) or miss trials, and the degree of synchronization also pre- the target stimulus (red) before the time when the monkey dicted whether the monkey was paying attention to the detected the target. The authors found that neurons syn- distractor, ultimately demonstrating that the strength of chronized to the LFP more strongly in response to their synchronization indexes which stimulus the monkey preferred stimulus feature when it was the attended target attended. feature of the search rather than a distractor feature. Attention and gamma-frequency Thus, attention enhanced synchronization of the responses synchronization in humans of neurons that shared a preference for the attended target The aforementioned studies from macaque cortex feature — and did so irrespective of the spatial location of demonstrate that the degree of synchronization indexes attention [24]. This feature-based modulation was also whether a spatially confined, local neuronal group is evident during a conjunction search task involving targets processing an attended stimulus effectively. This con- that were defined by