Brief wide-field photostimuli evoke and modulate oscillatory reverberating activity in cortical networks.
Cell assemblies manipulation by optogenetics is pivotal to advance neuroscience and neuroengineering. In in vivo applications, photostimulation often broadly addresses a population of cells simultaneously, leading to feed-forward and to reverberating responses in recurrent microcircuits. The former arise from direct activation of targets downstream, and are straightforward to interpret. The latter are consequence of feedback connectivity and may reflect a variety of time-scales and complex dynamical properties. We investigated wide-field photostimulation in cortical networks in vitro, employing substrate-integrated microelectrode arrays and long-term cultured neuronal networks. We characterized the effect of brief light pulses, while restricting the expression of channelrhodopsin to principal neurons. We evoked robust reverberating responses, oscillating in the physiological gamma frequency range, and found that such a frequency could be reliably manipulated varying the light pulse duration, not its intensity. By pharmacology, mathematical modelling, and intracellular recordings, we conclude that gamma oscillations likely emerge as in vivo from the excitatory-inhibitory interplay and that, unexpectedly, the light stimuli transiently facilitate excitatory synaptic transmission. Of relevance for in vitro models of (dys)functional cortical microcircuitry and in vivo manipulations of cell assemblies, we give for the first time evidence of network-level consequences of the alteration of synaptic physiology by optogenetics.
Theoretical Neurobiology &Neuroengineering, University of Antwerp, Antwerp, Belgium.
Rocco
R
Pulizzi
Theoretical Neurobiology &Neuroengineering, University of Antwerp, Antwerp, Belgium.
Gabriele
G
Musumeci
Laboratory of Neurobiology and Gene Therapy, Katholieke Universiteit Leuven, Leuven, Belgium.|Leuven Viral Vector Core, Katholieke Universiteit Leuven, Leuven, Belgium.
Chris
C
Van den Haute
Theoretical Neurobiology &Neuroengineering, University of Antwerp, Antwerp, Belgium.
Sebastiaan
S
Van De Vijver
Laboratory of Neurobiology and Gene Therapy, Katholieke Universiteit Leuven, Leuven, Belgium.
Veerle
V
Baekelandt
Theoretical Neurobiology &Neuroengineering, University of Antwerp, Antwerp, Belgium.|Department of Computer Science, University of Sheffield, S1 4DP Sheffield, UK.|Laboratory of Neural Microcircuitry, Brain Mind Institute, EPFL, CH-1015 Lausanne, Switzerland.
Michele
M
Giugliano
D000818:Animals; D002478:Cells, Cultured; D002540:Cerebral Cortex / Q000502:physiology*; D005071:Evoked Potentials; D065818:Gamma Rhythm; D015870:Gene Expression; D066298:In Vitro Techniques; D008027:Light; D008959:Models, Neurological; D009434:Neural Pathways; D009474:Neurons / Q000502:physiology*; D055355:Opsins / Q000235:genetics / Q000378:metabolism; D010775:Photic Stimulation; D051381:Rats; D011963:Receptors, GABA-A / Q000378:metabolism; D009435:Synaptic Transmission
D055355:Opsins; D011963:Receptors, GABA-A