Changes in hippocampal cell discharge patterns and theta rhythm spectral properties as a function of walking velocity in the guinea pig

Abstract

Dorsal hippocampal theta rhythm (theta) and extracellular unit activity from CA1 pyramidal layer were recorded in awake guinea pigs, both during standing and during walking on a conveyor belt at increasing speeds. Amplitude, frequency and rhythmicity of theta increased linearly with the movement speed. In this preparation we found the same three types of unit discharge patterns that have been described in anesthetized rats in the presence of spontaneous or induced hippocampal theta: type 1, rhythmic at theta frequency and phase-locked with theta; type 2, discharging non-rhythmically but phase-locked with theta; and type 3, discharging at random. Furthermore, all units modified their firing pattern when the animals walked, either by increasing their rhythmicity and/or phase-locking with theta or by increasing their firing frequency. During walking, some type 3 units changed into type 2 or type 1, type 2 units changed to type 1, and type I increased their rhythmicity. Consequently, the unit discharge rhythmicity and phase-locking with theta increased with the speed of movement. The mean rate of neuronal discharges increased linearly as a function of walking speed. In this paper we show that the progressive spectral theta changes determined by the intensity of movement are concomitant with the increase in rhythmicity of hippocampal cells. Moreover, the firing rate of these cells, and the amplitude, frequency and rhythmicity of theta, increased linearly as a function of walking speed, suggesting that neuronal excitation may be basically responsible for these changes in theta properties.

Cosine Directional Tuning of Theta Cell Burst Frequencies: Evidence for Spatial Coding by Oscillatory Interference

“…Burgess et al (2005Burgess et al ( , 2007 introduced an "oscillatory interference" theory, hypothesizing that theta oscillations are generated by velocity-controlled oscillators (VCOs), which perform path integration by modulating their frequencies in proportion with the speed and direction of a rat's translational movements. Supporting this idea, theta frequency is indeed modulated by a rat's movement speed (Rivas et al, 1996;Geisler et al, 2007), and oscillatory properties of spatial neurons are correlated with their spatial tuning parameters in accordance with predictions of oscillatory interference models (Burgess et al, 2007;Giocomo et al, 2007;Jeewajee et al, 2008a;Zilli et al, 2009). However, oscillatory interference models explicitly require that VCO frequencies vary as the cosine of an animal's movement direction, and such directional modulation of theta oscillations has never been observed.…”

“…Averaged across all directions, these opposing influences should cancel each other out, yielding a prediction that the mean VCO frequency would be identical for all running speeds. Contradicting this prediction, prior studies have shown that the theta frequency increases with running speed when movement direction is disregarded (Rivas et al, 1996;Geisler et al, 2007;Jeewajee et al, 2008a). One simple way to account for these results is to assume that the VCO base frequency [Eq.…”

Arc length coding by interference of theta frequency oscillations may underlie context-dependent hippocampal unit data and episodic memory function

“…The model is supported by data showing that running speed influences the frequency of theta rhythm (Whishaw and Vanderwolf 1973;Rivas et al 1996;Slawinska and Kasicki 1998;Maurer et al 2005). The modulation of entorhinal frequency (or distal dendritic frequency) by running speed s should alter the frequency of current sinks in stratum lacunosum-moleculare of region CA1 (Brankack et al 1993).…”

An unexpected role for TASK-3 potassium channels in network oscillations with implications for sleep mechanisms and anesthetic action

“…3A). However, because it has been reported (27)(28)(29)(30) that the frequency of the exploratory theta oscillations increases with the speed of the animal, we investigated whether or not this occurred in our mice. Because of the limitations of conventional power spectra in terms of time/ frequency resolution, we calculated the Wavelet power spectrum (31) as a function of time ( Fig.…”