Cholinergic Enhancement of Visual Attention and Neural Oscillations in the Human Brain

Abstract

SummaryCognitive processes such as visual perception and selective attention induce specific patterns of brain oscillations [1–6]. The neurochemical bases of these spectral changes in neural activity are largely unknown, but neuromodulators are thought to regulate processing [7–9]. The cholinergic system is linked to attentional function in vivo [10–13], whereas separate in vitro studies show that cholinergic agonists induce high-frequency oscillations in slice preparations [14–16]. This has led to theoretical proposals [17–19] that cholinergic enhancement of visual attention might operate via gamma oscillations in visual cortex, although low-frequency alpha/beta modulation may also play a key role. Here we used MEG to record cortical oscillations in the context of administration of a cholinergic agonist (physostigmine) during a spatial visual attention task in humans. This cholinergic agonist enhanced spatial attention effects on low-frequency alpha/beta oscillations in visual cortex, an effect correlating with a drug-induced speeding of performance. By contrast, the cholinergic agonist did not alter high-frequency gamma oscillations in visual cortex. Thus, our findings show that cholinergic neuromodulation enhances attentional selection via an impact on oscillatory synchrony in visual cortex, for low rather than high frequencies. We discuss this dissociation between high- and low-frequency oscillations in relation to proposals that lower-frequency oscillations are generated by feedback pathways within visual cortex [20, 21].

Cholinergic Stimulation Enhances Bayesian Belief Updating in the Deployment of Spatial Attention

“…Psychopharmacological neuroimaging studies in humans have indeed reported activation decreases in areas such as the parietal cortex in response to nicotine (e.g., Thiel et al, 2005;Vossel et al, 2008), but this effect is predominantly seen during invalidly cued trials and interpreted as facilitated attentional shifting or enhanced processing efficiency. In contrast, studies using cholinesterase inhibitors have reported an enhancement of voluntary attentional modulation at the behavioral and neural level (Rokem et al, 2010;Bauer et al, 2012). Similarly, muscarinic blockade with scopolamine reduces spatial attentional top-down modulation of responses to visual stimuli in visual cortex (Herrero et al, 2008), and theoretical modeling has shown that inhibitory drive by muscarinic receptors may effectively render the system more sensitive to feedback influences (i.e., attentional modulation) (Deco and Thiele, 2011).…”

Cortical cholinergic signaling controls the detection of cues

“…Precisely timed cholinergic transients could be essential for synchronizing cortical neuronal output driven by salient cues, thereby coordinating local network activity recruited by a cue (33,34). Moreover, the selection of cues for guiding the behavior per se may be mediated by fronto-visual oscillations that are generated by trial-based, phasic cholinergic signaling (35). Such neuronal coordination through coherence therefore could be necessary for the engagement of a particular motor plan for executing selected cue-guided responses.…”

Imaging human brain networks to improve the clinical efficacy of non-invasive brain stimulation

“…The task-related boosting (or suppression) of neural oscillations at specific frequencies between cortical regions can enhance performance in processes involved in task selection, attention and memory (Marshall et al, 2004;Lakatos et al, 2008;Bauer et al, 2012;Helfrich et al, 2014). Both rTMS and tDCS can modify ongoing oscillatory activity, and in so doing, may mimic or augment the amplitude of normal endogenous neural oscillations to promote task performance and cortical connectivity.…”