Diurnal influences on electrophysiological oscillations and coupling in the dorsal striatum and cerebellar cortex of the anesthetized rat

Abstract

Circadian rhythms modulate behavioral processes over a 24 h period through clock gene expression. What is largely unknown is how these molecular influences shape neural activity in different brain areas. The clock gene Per2 is rhythmically expressed in the striatum and the cerebellum and its expression is linked with daily fluctuations in extracellular dopamine levels and D2 receptor activity. Electrophysiologically, dopamine depletion enhances striatal local field potential (LFP) oscillations. We investigated if LFP oscillations and synchrony were influenced by time of day, potentially via dopamine mechanisms. To assess the presence of a diurnal effect, oscillatory power and coherence were examined in the striatum and cerebellum of rats under urethane anesthesia at four different times of day zeitgeber time (ZT1, 7, 13 and 19—indicating number of hours after lights turned on in a 12:12 h light-dark cycle). We also investigated the diurnal response to systemic raclopride, a D2 receptor antagonist. Time of day affected the proportion of LFP oscillations within the 0–3 Hz band and the 3–8 Hz band. In both the striatum and the cerebellum, slow oscillations were strongest at ZT1 and weakest at ZT13. A 3–8 Hz oscillation was present when the slow oscillation was lowest, with peak 3–8 Hz activity occurring at ZT13. Raclopride enhanced the slow oscillations, and had the greatest effect at ZT13. Within the striatum and with the cerebellum, 0–3 Hz coherence was greatest at ZT1, when the slow oscillations were strongest. Coherence was also affected the most by raclopride at ZT13. Our results suggest that neural oscillations in the cerebellum and striatum, and the synchrony between these areas, are modulated by time of day, and that these changes are influenced by dopamine manipulation. This may provide insight into how circadian gene transcription patterns influence network electrophysiology. Future experiments will address how these network alterations are linked with behavior.

Circadian regulation of membrane physiology in neural oscillators throughout the brain

“…Limitations of this study include possible effects of cerebellar organization (e.g., zebrin II expression banding), use of pups from postnatal days 0 to 3 prior to cerebellar network development, and potential light contamination during dark phase experiments. The second study (Frederick, Bourget‐Murray, Chapman, Amir, & Courtemanche, ) examined day–night differences in local field potential (LFP) oscillations in the rat cerebellum and striatum through dopaminergic mechanisms based on evidence that rhythms of dopamine levels (Ferris et al., ; Hood et al., ; Owasoyo, Walker, & Whitworth, ) and expression of D2 receptors are linked with expression of Per2 (Gravotta, Gavrila, Hood, & Amir, ; Hood et al., ). The coherence of oscillations of these regions was explored because of their cooperative role in sensory motor control and locomotor regulation.…”

Rhythms and blues: modulation of oscillatory synchrony and the mechanism of action of antidepressant treatments

“…Disruption of hippocampal θ rhythms (4–8 Hz) through blockade of neuronal gap junctions in the dorsal hippocampus impairs context‐dependent memory formation as well as c‐fos expression, suggesting a functional link between θ frequency oscillations and a neuroplastic process mediated by electrical synapses . In the circuits that mediate circadian rhythms, changes in oscillatory synchrony correlate with changes in dopaminergic tone and, through voltage‐ and ligand‐gated ion channels, with cyclical changes in gene expression . In the context of antidepressant treatment, ultradian oscillatory synchrony has been observed to be related to fluctuation in serotonergic tone and has been hypothesized to play a prominent role in antidepressant medication efficacy, as well as to affect expression of genes related to serotonin synthesis .…”

Gap Junction Modulation of Low-Frequency Oscillations in the Cerebellar Granule Cell Layer

“…Surgical procedures followed the same protocol as previously described by Frederick et al [40]. Briefly, Sprague-Dawley male rats (250-500 g, Charles River, St.…”

“…1), as we showed recently [40]. The recording of LFP oscillations in urethane-anesthetized animals has been used extensively to investigate slow rhythms in other brain areas, including theta oscillations in the hippocampus [42,[48][49][50] and lowfrequency delta oscillations [51].…”

“…In the present study, we examined physiologically the influence of electrical coupling on oscillations within the GCL by recording 5-15 Hz LFP oscillations in the rat cerebellar cortex in vivo during urethane anesthesia [40] and by testing the effect of local application of gap junction blockers. We examined the effect of the non-specific gap junction blocker, carbenoxolone (CBX), and the Cx36 and Cx50 subtypespecific blocker mefloquine [41,42].…”