Limbic gamma rhythms. II. Synaptic and intrinsic mechanisms underlying spike doublets in oscillating subicular neurons.
Gamma oscillations were evoked in the subiculum in rat transverse hippocampal slices by tetanic stimulation (200 ms/100 Hz) of either CA1 or subiculum. Gamma oscillations in the subiculum differed from those in CA1 in containing population spike doublets as well as singlets. The present study addresses the origin of this more complex form of gamma oscillation in the subiculum. Intracellular recordings from subicular neurons revealed that 63% of them fired double action potentials on cycles of the gamma oscillation that generated population spike doublets after tetanic stimulation of either CA1 or subiculum. The remaining cells produced excitatory postsynaptic potentials (EPSPs), and occasional single spikes, on each cycle. Neurons that fired occasional single action potentials during gamma rhythms were "regular spiking" cells. They did not produce burst discharges during depolarizing steps, had minimal membrane potential sags on hyperpolarizing steps, and responded to single afferent volleys with a single action potential on an EPSP followed by a large inhibitory postsynaptic potential complex. Fast spiking cells were observed too infrequently to be studied in detail. Neurons that fired doublets during gamma rhythms were "intrinsic burst" (IB) cells. They generated bursts of action potentials on step membrane depolarizations, had significant membrane potential sags on step hyperpolarizations with an anodal break potential on return to rest, and fired multiple action potentials in response to high-intensity single afferent volleys. IB neurons did not fire action potential doublets during 1-s membrane depolarizations. Double action potentials, however, were evoked in these cells by depolarizing pulses at 40 Hz from hyperpolarized membrane potentials (-100 mV). Computer simulations suggest that the hyperpolarization between the depolarizations was essential for action potential doublets. The results in this and the previous paper suggest the following: either CA1 or subiculum alone can generate gamma oscillations gated by local networks of interneurons, oscillations in CA1 project through pyramidal cell axons to subiculum with a time lag expected from axon conduction delays, and oscillating sequences of EPSPs and intrinsic and/or synaptic hyperpolarizing potentials in IB subicular neurons generate gamma frequency spike doublets, which depend on both the intrinsic properties of these neurons and their temporally patterned synaptic input. This phenomenon could amplify gamma output from CA1 and modify its coupling to gamma oscillations in the wider limbic system.
Stanford
I M
IM
Neuroscience Unit, Department of Physiology, The Medical School, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom.
Traub
R D
RD
Jefferys
J G
JG
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D001640:Bicuculline / Q000494:pharmacology; D003712:Dendrites / Q000187:drug effects / Q000502:physiology; D004558:Electric Stimulation; D005071:Evoked Potentials / Q000502:physiology*; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology*; D019706:Excitatory Postsynaptic Potentials / Q000187:drug effects / Q000502:physiology; D006624:Hippocampus / Q000502:physiology*; D066298:In Vitro Techniques; D008032:Limbic System / Q000502:physiology*; D008959:Models, Neurological; D019579:Neocortex / Q000502:physiology; D009415:Nerve Net / Q000502:physiology; D009431:Neural Conduction / Q000187:drug effects / Q000502:physiology; D009991:Oscillometry; D010721:Phosphinic Acids / Q000494:pharmacology; D011412:Propanolamines / Q000494:pharmacology; D017966:Pyramidal Cells / Q000187:drug effects / Q000502:physiology*; D011810:Quinoxalines / Q000494:pharmacology; D051381:Rats; D017207:Rats, Sprague-Dawley; D013569:Synapses / Q000187:drug effects / Q000502:physiology*; D009435:Synaptic Transmission / Q000187:drug effects / Q000502:physiology
D018691:Excitatory Amino Acid Antagonists; D010721:Phosphinic Acids; D011412:Propanolamines; D011810:Quinoxalines; C062865:2,3-dioxo-6-nitro-7-sulfamoylbenzo(f)quinoxaline; C085075:CGP 55845A; D001640:Bicuculline