Long-range neural coupling through synchronization with attention

Abstract

In a crowded visual scene, we typically employ attention to select stimuli that are behaviorally relevant. Two likely cortical sources of top-down attentional feedback to cortical visual areas are the prefrontal (PFC) and posterior parietal (PPC) cortices. Recent neurophysiological studies show that areas in PFC and PPC process signals about the locus of attention earlier than in extrastriate visual areas and are therefore likely to mediate attentional selection. Moreover, attentional selection appears to be mediated in part by neural synchrony between neurons in PFC/PPC and early visual areas, with phase relationships that seem optimal for increasing the impact of the top-down inputs to the visual cortex.

Introduction

When exploring the world around us, our visual system is confronted with more objects than it can process at any given moment. As a result, we are only aware of a limited number of objects, typically those that are a subject of our attention. Research on the neural mechanisms of visual attention in the last two decades has provided new insights into how neural systems allow us to monitor selectively particular objects or locations while blocking out all distracting information. Attention limits visual processing to objects or locations that are relevant to behavior by selectively enhancing their representation. In electrophysiological studies this is typically seen in enhanced visual responses or increased sensitivity of individual neurons to locations or objects of interest at the expense of distracting stimuli (Luck et al., 1997; McAdams and Maunsell, 2000; Moran and Desimone, 1985; Motter, 1994; Reynolds et al., 1999; Treue and Maunsell, 1996). We originally proposed that top-down attentional feedback biased the competition between multiple stimulus representations in the cortex (Desimone and Duncan, 1995). More recent neurophysiological and modeling studies have formalized and quantified this “biased competition” idea and suggest that the competition between stimulus representations is more generally a form of contrast normalization in the cortex (Lee and Maunsell, 2009; Reynolds et al., 1999; Reynolds and Heeger, 2009).

In addition to enhanced firing rates with attention, recent studies have found that attention can also change the relative timing of spikes in populations of neurons (Bichot et al., 2005; Fries et al., 2001; Saalmann et al., 2007; Steinmetz et al., 2000). Cells with receptive fields (RFs) at the attended location (Fries et al., 2001) as well as cells selective for the attended feature (Bichot et al., 2005) synchronize their activity in the gamma-frequency range (above 30 Hz). Given that cells have short integration times, even small increases in synchrony in a given population can result in pronounced firing rate changes in downstream neurons (Börgers and Kopell, 2008; Murthy and Fetz, 1994; Salinas and Sejnowski, 2000). Consequently, synchrony can act as another potential amplifier of behaviorally relevant signals. Indeed, recent modeling studies show how synchronized activity for attended stimuli could result in the filtering of responses to distracters (Borgers et al., 2008; Tiesinga et al., 2008; Zeitler et al., 2008).

Although both synchrony and firing rates have been shown to be modulated by attention in the visual cortex the exact mechanisms and sources of this modulation in the brain are less clear. Two likely sources of top-down feedback are the prefrontal cortex (PFC) and posterior parietal cortex (PPC) (Corbetta and Shulman, 2002; Desimone and Duncan, 1995; Gottlieb et al., 1998; Miller and Cohen, 2001; Thompson and Bichot, 2005; Thompson and Schall, 2000). Here, we review recent physiological evidence coming from simultaneous recordings in different cortical areas that support the role of PFC and PPC in enhancing and synchronizing visual cortex responses with attention. More generally, the results suggest that phase-coupled gamma-frequency oscillations play an important role in communication across brain regions.