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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 when food is given at hour 2 of recording and the data are referenced to the entry of the animal into the recording apparatus. (B) Illustrates the mean normalized RAT frequency when food is given at hour 2 of recording, but the data are referenced to the expected food time (6 pm). The frequency distribution produced by generating 1000 shuffled versions of the frequency dataset is illustrated in (C). The vertical dashed lines indicate two standard deviations from the mean of the distribution. The vertical black arrow represents the magnitude of the correlation of the data shown in (A) against the reference sine, while the vertical blue arrow represents the magnitude of the correlation of the data illustrated in (B) against the reference sine (shown in red).
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Figure 3: (A) The mean (±sem) normalized RAT frequency when food is given at hour 2 of recording and the data are referenced to the entry of the animal into the recording apparatus. (B) Illustrates the mean normalized RAT frequency when food is given at hour 2 of recording, but the data are referenced to the expected food time (6 pm). The frequency distribution produced by generating 1000 shuffled versions of the frequency dataset is illustrated in (C). The vertical dashed lines indicate two standard deviations from the mean of the distribution. The vertical black arrow represents the magnitude of the correlation of the data shown in (A) against the reference sine, while the vertical blue arrow represents the magnitude of the correlation of the data illustrated in (B) against the reference sine (shown in red).

Mentions: In this experiment, time-series data were either shifted to be aligned to entry into the environment (which also coincided with a food delivery event) or aligned to regular feeding time (6 pm). The mean RAT frequency was compared with the reference wave as described previously. As illustrated in Figure 3A, the frequency of RAT was significantly correlated (r = 0.331, p = 0.011) with the reference sine when the data were aligned to environment entry (and therefore also to food delivery). When the data were aligned to the previous regular feeding time, however, the relationship was eliminated (Frequency, r = 0.108, p = 0.415, n.s; Figure 3B). As in the previous experiments, 1000 randomly shuffled versions of the dataset were constructed and fitted to the reference sine. A Shapiro-Wilk normality test confirmed the normality of these fits (Frequency, W(1,1000) = 0.999, p = 0.624). The correlation coefficient of RAT frequency when the data was aligned with the start of recording (hour 1) were more than two standard deviations outside the mean of the shuffled distribution (Figure 3C).


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 when food is given at hour 2 of recording and the data are referenced to the entry of the animal into the recording apparatus. (B) Illustrates the mean normalized RAT frequency when food is given at hour 2 of recording, but the data are referenced to the expected food time (6 pm). The frequency distribution produced by generating 1000 shuffled versions of the frequency dataset is illustrated in (C). The vertical dashed lines indicate two standard deviations from the mean of the distribution. The vertical black arrow represents the magnitude of the correlation of the data shown in (A) against the reference sine, while the vertical blue arrow represents the magnitude of the correlation of the data illustrated in (B) against the reference sine (shown in red).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: (A) The mean (±sem) normalized RAT frequency when food is given at hour 2 of recording and the data are referenced to the entry of the animal into the recording apparatus. (B) Illustrates the mean normalized RAT frequency when food is given at hour 2 of recording, but the data are referenced to the expected food time (6 pm). The frequency distribution produced by generating 1000 shuffled versions of the frequency dataset is illustrated in (C). The vertical dashed lines indicate two standard deviations from the mean of the distribution. The vertical black arrow represents the magnitude of the correlation of the data shown in (A) against the reference sine, while the vertical blue arrow represents the magnitude of the correlation of the data illustrated in (B) against the reference sine (shown in red).
Mentions: In this experiment, time-series data were either shifted to be aligned to entry into the environment (which also coincided with a food delivery event) or aligned to regular feeding time (6 pm). The mean RAT frequency was compared with the reference wave as described previously. As illustrated in Figure 3A, the frequency of RAT was significantly correlated (r = 0.331, p = 0.011) with the reference sine when the data were aligned to environment entry (and therefore also to food delivery). When the data were aligned to the previous regular feeding time, however, the relationship was eliminated (Frequency, r = 0.108, p = 0.415, n.s; Figure 3B). As in the previous experiments, 1000 randomly shuffled versions of the dataset were constructed and fitted to the reference sine. A Shapiro-Wilk normality test confirmed the normality of these fits (Frequency, W(1,1000) = 0.999, p = 0.624). The correlation coefficient of RAT frequency when the data was aligned with the start of recording (hour 1) were more than two standard deviations outside the mean of the shuffled distribution (Figure 3C).

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