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The frequency of hippocampal theta rhythm is modulated on a circadian period and is entrained by food availability.

Munn RG, Tyree SM, McNaughton N, Bilkey DK - Front Behav Neurosci (2015)

Bottom Line: Because this effect can be observed without having to feed the animal to encourage movement we were able to identify what stimulus entrains the circadian oscillation.This pattern did not occur when data were referenced to the start of the recording session or to the actual time of day when this was not also related to feeding time.One interpretation of this finding is that the hippocampus is responsive to a food entrainable oscillator (FEO) that might modulate foraging behavior over circadian periods.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Otago Dunedin, New Zealand ; Department of Neurobiology, Stanford University Stanford, CA, USA.

ABSTRACT
The hippocampal formation plays a critical role in the generation of episodic memory. While the encoding of the spatial and contextual components of memory have been extensively studied, how the hippocampus encodes temporal information, especially at long time intervals, is less well understood. The activity of place cells in hippocampus has previously been shown to be modulated at a circadian time-scale, entrained by a behavioral stimulus, but not entrained by light. The experimental procedures used in the previous study of this phenomenon, however, necessarily conflated two alternative entraining stimuli, the exposure to the recording environment and the availability of food, making it impossible to distinguish between these possibilities. Here we demonstrate that the frequency of theta-band hippocampal EEG varies with a circadian period in freely moving animals and that this periodicity mirrors changes in the firing rate of hippocampal neurons. Theta activity serves, therefore, as a proxy of circadian-modulated hippocampal neuronal activity. We then demonstrate that the frequency of hippocampal theta driven by stimulation of the reticular formation also varies with a circadian period. Because this effect can be observed without having to feed the animal to encourage movement we were able to identify what stimulus entrains the circadian oscillation. We show that with reticular-activated recordings started at various times of the day the frequency of theta varies quasi-sinusoidally with a 25 h period and phase-aligned when referenced to the animal's regular feeding time, but not the recording start time. Furthermore, we show that theta frequency consistently varied with a circadian period when the data obtained from repeated recordings started at various times of the day were referenced to the start of food availability in the recording chamber. This pattern did not occur when data were referenced to the start of the recording session or to the actual time of day when this was not also related to feeding time. This double dissociation demonstrates that hippocampal theta is modulated with a circadian timescale, and that this modulation is strongly entrained by food. One interpretation of this finding is that the hippocampus is responsive to a food entrainable oscillator (FEO) that might modulate foraging behavior over circadian periods.

No MeSH data available.


Related in: MedlinePlus

(A) The mean (±sem) normalized RAT frequency data obtained when individual recordings are referenced to entry into the recording apparatus, but not the time of feeding, are not correlated with the reference sine shown in red. (B) When the individual RAT frequency data are shifted such that they are referenced to the time of feeding (6 pm solar time), the mean data are significantly correlated with the reference (p < 0.05). Data are smoothed using a 5-point moving average for these illustrations only. (C) illustrates the frequency distribution produced when 1000 shuffled versions of the dataset are generated and correlated against the reference sine. The vertical dashed lines demark two standard deviations from the mean of the distribution. The vertical blue arrow denotes the magnitude of the correlation of the dataset shown in (A) and the vertical black arrow denotes the magnitude of the correlation of the dataset shifted relative to a feeding reference in (B).
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Figure 2: (A) The mean (±sem) normalized RAT frequency data obtained when individual recordings are referenced to entry into the recording apparatus, but not the time of feeding, are not correlated with the reference sine shown in red. (B) When the individual RAT frequency data are shifted such that they are referenced to the time of feeding (6 pm solar time), the mean data are significantly correlated with the reference (p < 0.05). Data are smoothed using a 5-point moving average for these illustrations only. (C) illustrates the frequency distribution produced when 1000 shuffled versions of the dataset are generated and correlated against the reference sine. The vertical dashed lines demark two standard deviations from the mean of the distribution. The vertical blue arrow denotes the magnitude of the correlation of the dataset shown in (A) and the vertical black arrow denotes the magnitude of the correlation of the dataset shifted relative to a feeding reference in (B).

Mentions: The mean (unsmoothed) data from the two alignments were then compared to the reference sine wave. The normalized RAT frequency for these two analyses and the corresponding sine fit are illustrated in Figure 2. When data were aligned to entry to the environment, there was no significant correlation between normalized RAT frequency and the sine reference (r = 0.110, p = 0.450, n.s; Figure 2A). When the data were individually phase-shifted to align with regular food time, the mean time-series was significantly correlated with the reference sine frequency (r = 0.307, p = 0.025; Figure 2B).


The frequency of hippocampal theta rhythm is modulated on a circadian period and is entrained by food availability.

Munn RG, Tyree SM, McNaughton N, Bilkey DK - Front Behav Neurosci (2015)

(A) The mean (±sem) normalized RAT frequency data obtained when individual recordings are referenced to entry into the recording apparatus, but not the time of feeding, are not correlated with the reference sine shown in red. (B) When the individual RAT frequency data are shifted such that they are referenced to the time of feeding (6 pm solar time), the mean data are significantly correlated with the reference (p < 0.05). Data are smoothed using a 5-point moving average for these illustrations only. (C) illustrates the frequency distribution produced when 1000 shuffled versions of the dataset are generated and correlated against the reference sine. The vertical dashed lines demark two standard deviations from the mean of the distribution. The vertical blue arrow denotes the magnitude of the correlation of the dataset shown in (A) and the vertical black arrow denotes the magnitude of the correlation of the dataset shifted relative to a feeding reference in (B).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4356069&req=5

Figure 2: (A) The mean (±sem) normalized RAT frequency data obtained when individual recordings are referenced to entry into the recording apparatus, but not the time of feeding, are not correlated with the reference sine shown in red. (B) When the individual RAT frequency data are shifted such that they are referenced to the time of feeding (6 pm solar time), the mean data are significantly correlated with the reference (p < 0.05). Data are smoothed using a 5-point moving average for these illustrations only. (C) illustrates the frequency distribution produced when 1000 shuffled versions of the dataset are generated and correlated against the reference sine. The vertical dashed lines demark two standard deviations from the mean of the distribution. The vertical blue arrow denotes the magnitude of the correlation of the dataset shown in (A) and the vertical black arrow denotes the magnitude of the correlation of the dataset shifted relative to a feeding reference in (B).
Mentions: The mean (unsmoothed) data from the two alignments were then compared to the reference sine wave. The normalized RAT frequency for these two analyses and the corresponding sine fit are illustrated in Figure 2. When data were aligned to entry to the environment, there was no significant correlation between normalized RAT frequency and the sine reference (r = 0.110, p = 0.450, n.s; Figure 2A). When the data were individually phase-shifted to align with regular food time, the mean time-series was significantly correlated with the reference sine frequency (r = 0.307, p = 0.025; Figure 2B).

Bottom Line: Because this effect can be observed without having to feed the animal to encourage movement we were able to identify what stimulus entrains the circadian oscillation.This pattern did not occur when data were referenced to the start of the recording session or to the actual time of day when this was not also related to feeding time.One interpretation of this finding is that the hippocampus is responsive to a food entrainable oscillator (FEO) that might modulate foraging behavior over circadian periods.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Otago Dunedin, New Zealand ; Department of Neurobiology, Stanford University Stanford, CA, USA.

ABSTRACT
The hippocampal formation plays a critical role in the generation of episodic memory. While the encoding of the spatial and contextual components of memory have been extensively studied, how the hippocampus encodes temporal information, especially at long time intervals, is less well understood. The activity of place cells in hippocampus has previously been shown to be modulated at a circadian time-scale, entrained by a behavioral stimulus, but not entrained by light. The experimental procedures used in the previous study of this phenomenon, however, necessarily conflated two alternative entraining stimuli, the exposure to the recording environment and the availability of food, making it impossible to distinguish between these possibilities. Here we demonstrate that the frequency of theta-band hippocampal EEG varies with a circadian period in freely moving animals and that this periodicity mirrors changes in the firing rate of hippocampal neurons. Theta activity serves, therefore, as a proxy of circadian-modulated hippocampal neuronal activity. We then demonstrate that the frequency of hippocampal theta driven by stimulation of the reticular formation also varies with a circadian period. Because this effect can be observed without having to feed the animal to encourage movement we were able to identify what stimulus entrains the circadian oscillation. We show that with reticular-activated recordings started at various times of the day the frequency of theta varies quasi-sinusoidally with a 25 h period and phase-aligned when referenced to the animal's regular feeding time, but not the recording start time. Furthermore, we show that theta frequency consistently varied with a circadian period when the data obtained from repeated recordings started at various times of the day were referenced to the start of food availability in the recording chamber. This pattern did not occur when data were referenced to the start of the recording session or to the actual time of day when this was not also related to feeding time. This double dissociation demonstrates that hippocampal theta is modulated with a circadian timescale, and that this modulation is strongly entrained by food. One interpretation of this finding is that the hippocampus is responsive to a food entrainable oscillator (FEO) that might modulate foraging behavior over circadian periods.

No MeSH data available.


Related in: MedlinePlus