Oscillatory Dynamics in the Frontoparietal Attention Network during Sustained Attention in the Ferret

Abstract

Summary Sustained attention requires the coordination of neural activity across multiple cortical areas in the frontoparietal network, in particular prefrontal cortex (PFC) and posterior parietal cortex (PPC). Previous work has demonstrated that activity in these brain regions is coordinated by neuronal oscillations of the local field potential (LFP). However, the underlying coordination of activity in terms of organization of single unit (SU) spiking activity have remained poorly understood, particularly in a freely-moving task with unconstrained network dynamics. We found that long-range functional connectivity between anatomically connected PFC and PPC was mediated by oscillations in the theta frequency band. SU activity in PFC was phase-locked to theta oscillations in PPC; spiking activity in PFC and PPC was locked to local high-gamma activity. Together, our results support a model in which frequency-specific synchronization mediates functional connectivity between and within PFC and PPC of the frontoparietal attention network in the freely moving animal.

Functional dissociation of theta oscillations in the frontal and visual cortices and their long-range network during sustained attention

“…For instance, Spyropoulos et al (Spyropoulos et al, 2018) recently reported that theta oscillations in the visual cortex elicited by visual stimuli decreased in amplitude when visual attention was directed. In addition, another recent study found arousal-reduced theta power in the high-order visual area (i.e., posterior parietal cortex) of the ferret brain (Stitt et al, 2018) despite its enhanced long-range theta synchrony with the prefrontal cortex during sustained attention reported by an earlier study (Sellers et al, 2016). In fact, a pioneering neuro-feedback study in the 1970s reported similar results of an association between occipital theta suppression and improved performance in a visual detection task (Beatty et al, 1974).…”

“…It should be noted that the substantial work conducted in the frontal cortex has found gamma oscillations to play an important role in pro-cognitive functions (Cho et al, 2015; Kim et al, 2016). On the neuronal spike levels, the spiking activities of the frontal cortex in the high gamma band were locked to theta oscillations in the frontal and posterior parietal cortices during sustained attention (Sellers et al, 2016). In our study, we found effective modulation of low gamma, but not high gamma, by frontal theta using cross-frequency coupling analysis.…”

“…In particular, in No-Go trials, we expected the recruitment of both frontal and visual theta oscillations, depending on the attentive state of the animal. This is because elaborate sustained attention (i.e., remaining alert while inhibiting a Go response) has been known to elicit control-related theta in the frontal cortex (Clayton et al, 2015; Sellers et al, 2016), while visual perception without attention has been reported to elicit theta oscillations in the visual area (Spyropoulos et al, 2018). By tracking short-term behavioral performance within a single experimental session, we investigated state-dependent changes of frontal and visual theta oscillations and their coupling with higher frequency oscillations (e.g., gamma oscillations) to confirm their functional dissociation.…”

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

“…Recently, we reported that the 5-CSRTT engaged synchrony of oscillatory activity in the frontoparietal network of the ferret [16,17]. Phase synchronization both at the microscale of neuronal action potentials and the mesoscale of the population synaptic activity reflected in the local field potential was elevated in the theta-frequency range.…”

“…After successful training, the ferrets were surgically implanted with a chronic multichannel electrode array (2x8 tungsten electrode array, 250µm spacing, low-impedance reference electrode with the same length on the same array, MicroProbes Inc, Gaithersburg, MD) in LP/Pulvinar. Surgical procedure was similar to those previously described [16,22]. Briefly, ferrets were first injected with ketamine/xylazine (30 mg/kg of ketamine, 1-2 mg/kg of xylazine, IM) for anesthesia induction, and then were intubated and anesthetized with inhaled isoflurane (1.5-2%) in 100% medical oxygen (mechanically ventilated, 10-11 cc volume, 50 bpm).…”