State-dependent top-down and bottom-up processes in gamma-band (~40 Hz) oscillations of the cat EEG

Abstract

Cognitive processes rely on extensive thalamocortical and corticocortical recurrent interactions. The gamma frequency band ([~]40 Hz) of the electroencephalogram (EEG) emerges from these interactions. Importantly, cognitive processing depends on the interplay between bottom-up sensory inputs and top-down influences from higher-order cortical areas. However, the extent to which gamma-band oscillations are associated with directional patterns of functional interactions remains unclear. Therefore, the aim of this study was to investigate the directionality of gamma-band information flow during wakefulness (W) and sleep, under spontaneous conditions and in response to auditory stimulation. Cats were chronically implanted for polysomnographic recordings, with electrodes placed in multiple cortical and thalamic regions. Information-flow directionality was assessed using two complementary methods: (i) time-lag analysis of gamma-band amplitude envelopes between pairs of channels, and (ii) Granger Causality analysis of the same channel pairs. During quiet W gamma-band oscillations exhibited a predominantly top-down directional organization, from higher- to lower-order cortical areas, as well as from cortical regions to thalamic nuclei. Following auditory stimulation, a prominent gamma response emerged between 0.5 and 1.5 s after stimulus onset. Within this time window, distinct patterns of gamma-band information flow were observed depending on the nature of the stimulus. Specifically, a bottom-up directional predominance was observed for simple auditory stimuli (clicks), whereas top-down processing prevailed for complex variable stimuli. In contrast, no consistent directionality of information flow was observed during either NREM or REM sleep, regardless of whether auditory stimulation was present. These findings extend our understanding of gamma-band information-flow dynamics during wakefulness and sleep.