Abstract
Although oscillations during development have been characterized in a wide range of neural systems, little is known about the interaction between these network oscillations and neuronal spiking, and the interactions among different oscillation frequencies. Here we recorded the spontaneous and visual-elicited local field potential (LFP) and multi-unit activity (MUA) in the visual cortex of freely-moving juvenile ferrets before and after eye-opening. We found that both the spontaneous and visually-elicited LFP power was increased after eye-opening, especially in higher frequency bands (>30 Hz). Spike LFP phase coupling was decreased for lower frequency bands (theta and alpha) but slightly increased for higher frequencies (high-gamma band). A similar shift towards faster frequencies also occurred for phase-amplitude coupling; with maturation, the coupling of the theta/alpha/beta band amplitude to the delta phase was decreased and the high-gamma amplitude coupling to theta/alpha phase was increased. This shift towards higher frequencies was also reflected in the visual responses; the LFP oscillation became more entrained by visual stimulation with higher frequencies (>10 Hz). Taken together, these results suggest gamma oscillation as a signature of the maturation of cortical circuitry.
Highlights
Previous studies of brain development have revealed a critical period when external experience is crucial for the normal development of cortical functional organization[22,23,24]
Our results reveal profound changes in high frequency oscillations after eye-opening, including (1) increase in high frequency oscillation amplitude, (2) decreased spike coupling to low frequency phase but increase to high frequency phase (>50 Hz), (3) decreased theta (4–8 Hz)/alpha/ beta band amplitude coupling to delta (1–4 Hz) band phase but increased high-gamma band amplitude coupling to theta/alpha band phase, and (4) increased entrainment of the local field potential (LFP) by periodic exogenous visual stimuli
We found that in contrast to the more continuous activity patterns presented after eye-opening (Fig. 1F, example from a P50 animal, refer to Fig. 2 for more examples with higher temporal resolution), spontaneous activity before eye-opening was characterized by short periods of pronounced LFP amplitude and spiking rate, interleaved with periods of relative silence (Fig. 1E, example from a P29 animal)
Summary
Previous studies of brain development have revealed a critical period when external experience is crucial for the normal development of cortical functional organization[22,23,24]. To untangle the influence of sensory-independent and experience-elicited neural activity on the development of cortical networks, it is necessary to compare patterns of network activity across different periods throughout development. Our results reveal profound changes in high frequency oscillations after eye-opening, including (1) increase in high frequency (especially >30 Hz) oscillation amplitude, (2) decreased spike coupling to low frequency phase (theta/alpha) but increase to high frequency phase (>50 Hz), (3) decreased theta (4–8 Hz)/alpha/ beta band amplitude coupling to delta (1–4 Hz) band phase but increased high-gamma band amplitude coupling to theta/alpha band phase, and (4) increased entrainment of the LFP by periodic exogenous visual stimuli. Our results support the hypothesis that the development of higher frequency oscillations (especially >30 Hz) serves as a biomarker for the maturation of cortical circuits
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