Beta rhythms (15-20 Hz) generated by nonreciprocal communication in hippocampus.
Generation of gamma rhythms in reciprocally connected areas of cortex produces synchronous neuronal firing, although little is known about the consequences of gamma rhythms when generated in nonreciprocally connected regions. This nonreciprocity exists in hippocampus, where gamma rhythms are generated in area CA3 in vitro and in vivo and nonreciprocally projected to area CA1 by the Schaffer collateral pathway. Here we demonstrate how this CA3 gamma rhythm generates two different patterns of local CA1 oscillation dependent on the degree of output from area CA1. 1) In conditions where activity projected to area CA1 produces only very low principal cell recruitment the local population rhythm mimics the gamma rhythm projected from CA3. This activity is generated predominantly by recruitment of CA1 basket cells in a manner dependent on phasic, feedforward excitation of this interneuron subclass. Interneurons in stratum oriens, not receiving CA3 feedforward input, fired at theta frequencies. 2) In the presence of serotonin CA1 principal cell recruitment was appreciably enhanced, resulting in dual activation of CA1 basket cells through both feedforward and feedback excitations. Feedback excitation to CA1 stratum oriens interneurons was also enhanced. The resulting change in interneuron network dynamics generated a beta-frequency CA1 rhythm (as a near-subharmonic of the gamma rhythm projected from CA3). These findings demonstrate that in nonreciprocally connected networks, the frequency of population rhythms in target areas serves to code for degree of principal cell recruitment by afferent input.
Bibbig
Andrea
A
Department of Physiology and Pharmacology, State University of New York Health Sciences Center, Brooklyn, New York, USA.
Middleton
Steven
S
Racca
Claudia
C
Gillies
Martin J
MJ
Garner
Helen
H
Lebeau
Fiona E N
FE
Davies
Ceri H
CH
Whittington
Miles A
MA
D000818:Animals; D001611:Beta Rhythm; D003627:Data Interpretation, Statistical; D004569:Electroencephalography; D004594:Electrophysiology; D019706:Excitatory Postsynaptic Potentials / Q000187:drug effects / Q000502:physiology; D017629:Gap Junctions / Q000502:physiology; D006624:Hippocampus / Q000502:physiology*; D007395:Interneurons / Q000502:physiology; D008564:Membrane Potentials / Q000187:drug effects; D008734:Methoxyhydroxyphenylglycol / Q000031:analogs & derivatives / Q000494:pharmacology; D009415:Nerve Net / Q000187:drug effects / Q000502:physiology; D046709:Pattern Recognition, Physiological / Q000502:physiology; D017966:Pyramidal Cells / Q000187:drug effects; D051381:Rats; D017207:Rats, Sprague-Dawley; D012701:Serotonin / Q000494:pharmacology; D013569:Synapses / Q000502:physiology
D012701:Serotonin; D008734:Methoxyhydroxyphenylglycol; C010117:3,4-dihydroxyphenylglycol