Theta Oscillations Organize Spiking Activity in Higher-Order Visual Thalamus during Sustained Attention

Yu, Chunxiu; Stitt, Iain M.; Li, Yuhui; Zhou, Zhe Charles; Sellers, Kristin K.; Frohlich, Flavio · 2017 · Crossref

DOI: 10.1101/219626

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Summary

This study investigates the neural mechanisms underlying sustained attention, specifically focusing on the role of the higher-order visual thalamus, known as the lateral posterior-pulvinar complex (LP/pulvinar). While the fronto-parietal network is well-established in attention models, the contribution of subcortical structures remains poorly understood. The authors aimed to determine how neuronal dynamics in the LP/pulvinar are modulated during tasks requiring sustained attention, hypothesizing that this region plays an active role in orchestrating thalamic signaling. To address this, the researchers performed multichannel electrophysiological recordings in three ferrets trained to perform the five-choice serial reaction time task (5-CSRTT), a standard assay for spatial sustained attention. The task required animals to maintain attention during a 5-second delay period before responding to a visual stimulus. Chronic electrode arrays were implanted in the LP/pulvinar to record single-unit activity and local field potentials (LFPs) simultaneously with behavioral data. The analysis focused on the delay period, examining firing rates, spike-field coherence, and cross-frequency phase-amplitude coupling to assess how oscillatory activity organized spiking patterns. The results revealed that approximately half of the recorded neurons (130 of 259 units) exhibited progressively increasing firing rates during the delay period, termed "attention-modulated" units, while the remaining units responded only to the stimulus. Crucially, spike-field coherence in the theta frequency band (~5 Hz) was significantly higher for attention-modulated neurons compared to non-modulated ones throughout the trial epochs, particularly before stimulus onset and screen touch. Additionally, theta power and theta-gamma phase-amplitude coupling (PAC) were elevated during the sustained attention period. Although gamma power decreased during this time, the amplitude of gamma oscillations became more tightly locked to the phase of theta oscillations, indicating a behaviorally dependent synchronization mechanism. These findings suggest that theta oscillations in the higher-order visual thalamus play a central role in organizing spiking activity during sustained attention. The selective synchronization of attention-modulated neurons to theta rhythms implies that the LP/pulvinar actively participates in maintaining vigilance and preparing for sensory input. This mechanistic insight into subcortical contributions to attention may inform strategies for treating attention deficits associated with disorders such as ADHD, schizophrenia, and bipolar disorder, where sustained attention impairment persists even after symptom remission.

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