GABAB receptor-mediated, layer-specific synaptic plasticity reorganizes gamma-frequency neocortical response to stimulation.
Repeated presentations of sensory stimuli generate transient gamma-frequency (30-80 Hz) responses in neocortex that show plasticity in a task-dependent manner. Complex relationships between individual neuronal outputs and the mean, local field potential (population activity) accompany these changes, but little is known about the underlying mechanisms responsible. Here we show that transient stimulation of input layer 4 sufficient to generate gamma oscillations induced two different, lamina-specific plastic processes that correlated with lamina-specific changes in responses to further, repeated stimulation: Unit rates and recruitment showed overall enhancement in supragranular layers and suppression in infragranular layers associated with excitatory or inhibitory synaptic potentiation onto principal cells, respectively. Both synaptic processes were critically dependent on activation of GABAB receptors and, together, appeared to temporally segregate the cortical representation. These data suggest that adaptation to repetitive sensory input dramatically alters the spatiotemporal properties of the neocortical response in a manner that may both refine and minimize cortical output simultaneously.
Hull York Medical School, University of York, Heslington, YO10 5DD, United Kingdom; Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, NE2 4HH, United Kingdom;
Matthew
M
Ainsworth
Department of Neuroscience, Brown University, Providence, RI 02912;
Shane
S
Lee
Interdisciplinary Computing and Complex Biosystems Research Group, School of Computing Science, Newcastle University, Newcastle upon Tyne, NE1 7RU, United Kingdom;
Marcus
M
Kaiser
Faculty of Medicine, National Heart and Lung Institute, Imperial College London, London, SW7 2AZ, United Kingdom;
Jennifer
J
Simonotto
Department of Mathematics and Statistics, Boston University, Boston, MA 02215 miles.whittington@hyms.ac.uk nk@bu.edu.
Nancy J
NJ
Kopell
Hull York Medical School, University of York, Heslington, YO10 5DD, United Kingdom; miles.whittington@hyms.ac.uk nk@bu.edu.
Miles A
0000-0002-0247-1362
MA
Whittington
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D002478:Cells, Cultured; D004558:Electric Stimulation / Q000379:methods; D059330:GABAergic Neurons / Q000502:physiology; D065818:Gamma Rhythm / Q000502:physiology*; D019579:Neocortex / Q000502:physiology*; D009415:Nerve Net / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology*; D051381:Rats; D017208:Rats, Wistar; D018080:Receptors, GABA-B / Q000378:metabolism*; D009435:Synaptic Transmission / Q000502:physiology*
D018080:Receptors, GABA-B
GABAB receptor; gamma rhythms; habituation; sensory processing; synaptic plasticity