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The Journal of Neuroscience, December 17, 2008, 28(51):13828-13844; doi:10.1523/JNEUROSCI.2684-08.2008

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Behavioral/Systems/Cognitive
Spontaneous High-Frequency (10–80 Hz) Oscillations during Up States in the Cerebral Cortex In Vitro

Albert Compte,^1,2 Ramon Reig,^1,2 Vanessa F. Descalzo,^1,2 Michael A. Harvey,² Gabriel D. Puccini,² and Maria V. Sanchez-Vives^1,2,3

¹Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), 08036 Barcelona, Spain, ²Instituto de Neurociencias de Alicante, Universidad Miguel Hernández-Consejo Superior de Investigaciones Científicas, 03550 Sant Joan d'Alacant, Spain, and ³Institució Catalana de Recerca i Estudis Avançats (ICREA), 08010 Barcelona, Spain

Correspondence should be addressed to Albert Compte or Maria V. Sanchez-Vives, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Villarroel 170, 08036 Barcelona, Spain. Email: acompte{at}clinic.ub.es or Email: msanche3{at}clinic.ub.es

High-frequency oscillations in cortical networks have been linked to a variety of cognitive and perceptual processes. They have also been recorded in small cortical slices in vitro, indicating that neuronal synchronization at these frequencies is generated in the local cortical circuit. However, in vitro experiments have hitherto necessitated exogenous pharmacological or electrical stimulation to generate robust synchronized activity in the β/ range. Here, we demonstrate that the isolated cortical microcircuitry generates β and oscillations spontaneously in the absence of externally applied neuromodulators or synaptic agonists. We show this in a spontaneously active slice preparation that engages in slow oscillatory activity similar to activity during slow-wave sleep. β and synchronization appeared during the up states of the slow oscillation. Simultaneous intracellular and extracellular recordings revealed synchronization between the timing of incoming synaptic events and population activity. This rhythm was mechanistically similar to pharmacologically induced rhythms, as it also included sparse, irregular firing of neurons within the population oscillation, predominant involvement of inhibitory neurons, and a decrease of oscillation frequency after barbiturate application. Finally, we show in a computer model how a synaptic loop between excitatory and inhibitory neurons can explain the emergence of both the slow (<1 Hz) and the β-range oscillations in the neocortical network. We therefore conclude that oscillations in the β/ range that share mechanisms with activity reported in vivo or in pharmacologically activated in vitro preparations can be generated during slow oscillatory activity in the local cortical circuit, even without exogenous pharmacological or electrical stimulation.

Key words: ; β; microcircuit; synchronization; inhibition; slow oscillations

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Received May 29, 2008; revised Nov. 3, 2008; accepted Nov. 8, 2008.

Correspondence should be addressed to Albert Compte or Maria V. Sanchez-Vives, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Villarroel 170, 08036 Barcelona, Spain. Email: acompte{at}clinic.ub.es or Email: msanche3{at}clinic.ub.es

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