Relationships between Hippocampal Sharp Waves, Ripples, and Fast Gamma Oscillation: Influence of Dentate and Entorhinal Cortical Activity

Abstract

Summary Hippocampal sharp waves (SPW) and associated fast (‘ripple’) oscillations in the CA1 region are among the most synchronous physiological patterns in the mammalian brain. Using two-dimensional arrays of electrodes for recording local field potentials and unit discharges in freely moving rats, we studied the emergence of ripple oscillations (140–220 Hz) and compared their origin and cellular-synaptic mechanisms with fast gamma oscillations (90–140 Hz). We show that (a) hippocampal SPW-Rs and fast gamma oscillations are quantitatively distinct patterns but involve the same networks and share similar mechanisms, (b) both the frequency and magnitude of fast oscillations is positively correlated with the magnitude of SPWs, (c) during both ripples and fast gamma oscillations the frequency of network oscillation is higher in CA1 than in CA3, (d) SPWs and associated firing of neurons are synchronous in the dorsal hippocampus and dorso-medial entorhinal cortex but ripples are confined to the CA1 pyramidal layer and its downstream targets and (e) the emergence of CA3 population bursts, a prerequisite for SPW-ripples, is biased by activity patterns in the dentate gyrus and entorhinal cortex, with highest probability of ripples associated with an ‘optimum’ level of dentate gamma power. We hypothesize that each hippocampal subnetwork possesses distinct resonant properties, tuned by the magnitude of the excitatory drive.

Mechanisms of physiological and epileptic HFO generation

“…The frequency of these oscillations proved to be modulated by experimental manipulations of the size and duration of the IPSPs as predicted by computer simulations (Whittington et al, 1995). Inhibitory neurons also play a key role in pacing faster physiological activity, in the ripple band 80-250 Hz, as shown by unit recordings in vivo (Ylinen et al, 1995): as mentioned above the distinction between γ and ripples is less clear that it once seemed (Belluscio et al, 2012;Crone et al, 2006;Edwards et al, 2005;Sullivan et al, 2011). However, prolonged highfrequency oscillations based exclusively on synaptic mechanisms are unlikely because neurotransmitter depletion will lead to a strong synaptic depression and thus to termination of these oscillations (Zucker and Regehr, 2002).…”

“…However, we will review some aspects of γ oscillations, partly because they shed some light on HFO mechanisms, and partly because there can be overlap between γ and "ripples", a transient hippocampal HFO in the 100 Hz to 200-250 Hz band. Functionally γ and ripples can coexist under physiological conditions and share mechanisms (Sullivan et al, 2011), or can be linked under the term fast γ (90-150 Hz, with slow γ at 30-50 Hz and mid γ 50-90 Hz) (Belluscio et al, 2012), while other authors call oscillations from ~60 to 200-250 Hz "high γ" (Crone et al, 2006;Edwards et al, 2005).…”

New methods for understanding systems consolidation

“…Hippocampal and neocortical circuits are reactivated after learning during periods of sleep and inactivity (Wilson and McNaughton 1994;Qin et al 1997;Siapas and Wilson 1998;Nadasdy et al 1999;Louie and Wilson 2001;Hoffman and McNaughton 2002). Reactivation during these periods is initiated by sharp wave-ripple complexes (SPW-R) in the CA3 region of the hippocampus (Buzsaki 1989;Chrobak and Buzsaki 1996;Sullivan et al 2011). Blocking SPW-R events or disrupting the fibers by which they are transmitted to the neocortex impairs the consolidation of recently acquired memories (Daumas et al 2005;Girardeau et al 2009;Jadhav et al 2012).…”

State-of-the-art MEMS and microsystem tools for brain research

“…Although histological evidence supports the use of smaller, lattice-like structures, no group has yet provided strong evidence that reliable single-cell resolution can be achieved across many channels for more than even one year. Currently, the gold standard among neuroscientists seeking longterm single-cell recording is the use of a microdrive to periodically 'tune' the position of silicon neural probes (particularly those with thicknesses ranging from 12 to 15 μm and shanks measuring approximately 60 μm wide for rodent studies) 106 . Therefore, interest in and funding for advanced microelectrodes have been increasing given both the current success and the potential for further improvements of large-scale long-term electrophysiology.…”

“…Silicon devices can penetrate many brain types and depths. Unlike polymer arrays, silicon and other stiff materials have the ability to be moved on a microdrive during long-term recording and thereby maximizing the number of cells recorded in a session 106 .…”