Theta Phase Classification of Interneurons in the Hippocampal Formation of Freely Moving Rats

Abstract

Earlier work on freely moving rats classified neurons in Ammon's horn as pyramidal cells (including place cells) or interneurons (previously called "theta cells") based on temporal discharge correlates and waveform configurations, but the anatomical and biochemical diversity of interneurons suggests they may have other distinguishing characteristics. To explore this possibility, we made extracellular recordings as rats foraged for food in an open space, used accepted criteria to identify interneurons, and found two additional categorization methods. First, interneurons were separated into theta-modulated and theta-independent groups using spike autocorrelograms. Second, theta-modulated interneurons were further separated into four groups by the phase of the ϳ8 Hz theta rhythm at which firing was most rapid. These phase groups resemble the four phase peak groups of five anatomically identified interneuron types (two with the same preferred phase) recorded during the slow (ϳ4 Hz) theta rhythm in urethane-anesthetized rats. We suggest that the similar number of peak phase groups in walking rats and urethane-anesthetized rats and the partial agreement between peak phase values reflect a similar organization of theta rhythm in both states, so that the discharge properties of anatomically identified interneurons can be described in freely moving rats. Interestingly, the average spatial firing precision of the interneuron classes does not differ significantly, suggesting that the strong location-specific firing of place cells may be due to segregated high-and low-precision interneuron ensembles rather than to one or more dedicated high-precision classes.

Theta Rhythmic Clock-Like Activity of Single Units in the Mouse Hippocampus

“…The recording microdrive was designed to implant two independently movable electrode bundles of 12 tetrodes and 24 stereotrodes into both sides of dorsal hippocampi, as described in our previous work (Lin et al, 2006). The tetrodes were constructed from four and two, respectively, twisted 13 m nichrome wires (California Fine Wire) bound together by melting their insulation (Czurkó et al, 2011), with gold-plated tips to reduce the electrode impedance to 500 -800 K⍀ at 1 kHz.…”

“…Individual neurons were identified and sorted by clustering methods in Offline Sorter version 2.8 software (http://www.plexon.com), and performed manually in a threedimensional parameter space. The following two major criteria were used to identify interneurons: Ͼ5 Hz firing rates and 100 -300 s spike durations (Czurkó et al, 2011). Then interspike intervals (ISIs) were used to further isolate theta clock-spiking cells from the other cells.…”

“…The gamma power (root mean square) of the filtered signal was calculated by sliding a 25 ms window every 1 ms, and the threshold of detecting gamma episodes was set to 2 SDs above the background mean power (Csicsvari et al, 2003).…”

“…They are pyramidal cells that become active when animals enter particular places in the environment (O'Keefe and Dostrovsky, 1971). The discharges of place cells are also characterized by temporal coding phenomena, such as theta phase locking and theta phase precession (Huxter et al, 2003). In addition, it was reported that certain neurons in the hippocampal CA1 encode concept (Quiroga et al, 2005;Lin et al, 2007), time (MacDonald et al, 2011), and other information via their unique firing patterns.…”

“…In addition, it was reported that certain neurons in the hippocampal CA1 encode concept (Quiroga et al, 2005;Lin et al, 2007), time (MacDonald et al, 2011), and other information via their unique firing patterns. As for interneurons in the hippocampus, their firing activities often show relevance to hippocampal local field potential (LFP) rhythm, for example, the theta-locked neurons (Klausberger et al, 2003;Zhang et al, 2012), the gamma-locked neurons (Csicsvari et al, 2003), and the ripple-related neurons (Klausberger et al, 2003). These various firing patterns observed in rodent hippocampus in vivo are critical for describing the principles of hippocampal function and to reveal the mechanisms of information coding of hippocampal neurons.…”