Developmental appearance and disappearance of cortical events and oscillations in infant rats

Abstract

Until recently, organized and state-dependent neocortical activity in infant rats was thought to commence with the emergence of delta waves at postnatal day (P)11. This view is changing with the discovery of several forms of cortical activity that are detectible soon after birth, including spindle bursts (SBs) and slow activity transients (SATs). Here we provide further evidence of surprisingly rich cortical activity patterns during early development and document, in P5-P13 rats, the appearance, disappearance, and transient expression of three cortical events and oscillations. EEG activity in frontal, parietal, and occipital cortices was recorded in unanesthetized, head-fixed subjects using 16-channel laminar silicon electrodes and Ag-AgCl electrodes. In addition to SATs, we identified two novel forms of activity: cortical sharp potentials (CSPs) and gamma bursts (GBs). SBs were not observed in these areas. CSPs, defined as discrete, biphasic events with a duration of 250 ms, exhibited an inverted-U developmental trajectory with peak prevalence at P9. In contrast, GBs, defined as brief bursts of 40-Hz activity, increased steadily in prevalence and duration from P5 through P13. The prevalence of SATs decreased steadily across the ages tested here. Furthermore, both CSPs and GBs were more likely to occur during sleep than during wakefulness. Because SATs, CSPs, and GBs exhibit different developmental trajectories and rates of occurrence, and can occur independently of each other, they appear to be distinct patterns of neuronal activity. We hypothesize that these diverse patterns of neurophysiological activity reflect the instantaneous local structure and connectivity of the developing neocortex.

Voltage-Sensitive Dye Imaging Reveals Dynamic Spatiotemporal Properties of Cortical Activity after Spontaneous Muscle Twitches in the Newborn Rat

“…Bursts of gammarange activity have also been described recently in the developing barrel cortex, under control of excitatory thalamic synapses (Minlebaev et al, 2011). Finally, two recent studies report slow (Ͼ0.1 Hz) oscillations in the developing sensory cortices (Colonnese and Khazipov, 2010;Seelke and Blumberg, 2010).…”

“…The study of correlated neural activity in developing mammalian cortex is currently characterized by a variety of patterns, described in a range of preparations, including cortical slices (Garaschuk et al, 2000;Corlew et al, 2004;Sun and Luhmann, 2007;Allene and Cossart, 2010) and the in vivo intact brain (Khazipov et al, 2004;Adelsberger et al, 2005;Marcano-Reik and Blumberg, 2008;Golshani et al, 2009;Seelke and Blumberg, 2010;Minlebaev et al, 2011). Most relevant to our results are patterns of activity described in vivo.…”

“…Most prominent of these is the spin-dle burst, an event lasting 200 -600 ms and consisting of a burst of 10 -25 Hz oscillations found in the somatosensory (Khazipov et al, 2004;Minlebaev et al, 2007) and visual cortices. Oscillations in the gamma range of frequencies (30 -40 Hz) also exist every 10 -30 s (Yang et al, 2009;Seelke and Blumberg, 2010), whereas long (40 s) bursts of 20 -30 Hz activity repeat every 20 -30 min (Yang et al, 2009). Bursts of gammarange activity have also been described recently in the developing barrel cortex, under control of excitatory thalamic synapses (Minlebaev et al, 2011).…”

“…3, 4) as well as regions outside of the sensory cortices (Fig. 8), in which our knowledge of activity patterns is limited (Seelke and Blumberg, 2010). Notable weaknesses of VSD imaging include a limited contribution to the signal from deep layers of cortex (Berger, 2007;Chemla and Chavane, 2010;Mohajerani et al, 2010), particularly relevant because synaptic inputs to superficial layers 2/3 are weak during early life (Stern, 2001;Bureau, 2004).…”

“…Distinct patterns of neural activity are found in different neural systems (Yvert et al, 2004;Crépel et al, 2007;Tritsch et al, 2007;Watt et al, 2009), and, in some cases, the function of these patterns has been determined (Torborg and Feller, 2005;Huberman, 2007;Wu et al, 2010). Distinct patterns of neural activity are present within the developing mammalian cortex as well (Garaschuk et al, 2000;Adelsberger et al, 2005;Dupont et al, 2006;Yang et al, 2009;Colonnese and Khazipov, 2010;Seelke and Blumberg, 2010;Minlebaev et al, 2011). Understanding these patterns is crucial because they may provide a template for future task-related activity by controlling axon growth and synaptogenesis (Allene and Cossart, 2010).…”