Contrasting Activity Profile of Two Distributed Cortical Networks as a Function of Attentional Demands

Recent human functional MRI (fMRI) studies have revealed that two widely distributed groups of cortical areas display inverse changes in activity when attentional demands increase, with one group showing higher (task-on) and the second lower (task-off) blood oxygen level-dependent (BOLD) signals. Moreover, task-on and task-off regions also exhibit slow (<0.2 Hz) inversely correlated fluctuations in BOLD signal at rest. However, the neuronal correlates of these reciprocal BOLD signal fluctuations are unknown. Here, we addressed this question using simultaneous recordings of unit activity and local field potentials (LFPs) in the cat homologues of task-on and task-off regions. In all states of vigilance, LFP power was lower in task-off than task-on regions with no difference in firing rates. Both sets of regions displayed slow (0.5-0.15 Hz) cyclical modulations in LFP power in all frequency bands but with large and variable phase differences such that task-on and task-off regions were often anticorrelated. Inversely correlated LFP power fluctuations were state-dependent in that they were much more frequent in waking and paradoxical sleep than in slow-wave sleep. Moreover, consistent with fMRI findings, when attentional demands increased, LFP power in task-on and task-off regions changed in opposite directions, further augmenting and decreasing, respectively. At odds with previous fMRI studies, however, the decreased LFP power in task-off regions was associated with increased firing rates, suggesting that the engagement of task-off regions might not be reduced but in fact enhanced during attention.