Limits...
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 frequency of spontaneously generated hippocampal theta rhythm during each hour of recording (black line). The reference sine wave used for comparison is shown in red. (B) The frequency distribution produced by correlating 1000 shuffled versions of the data shown in (A) against the reference sine. The vertical dashed black lines demark two standard deviations from the mean of the distribution. The vertical black arrow indicates the magnitude of the correlation of the unshuffled data shown in (A) against the reference sine.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4356069&req=5

Figure 1: (A) The mean (±sem) normalized frequency of spontaneously generated hippocampal theta rhythm during each hour of recording (black line). The reference sine wave used for comparison is shown in red. (B) The frequency distribution produced by correlating 1000 shuffled versions of the data shown in (A) against the reference sine. The vertical dashed black lines demark two standard deviations from the mean of the distribution. The vertical black arrow indicates the magnitude of the correlation of the unshuffled data shown in (A) against the reference sine.

Mentions: It has previously been established that the firing rate of CA1 place cells is associated with features of hippocampal theta (Buzsàki and Eidelberg, 1983; Fox et al., 1986; O’Keefe and Recce, 1993; Skaggs et al., 1996; Hasselmo, 2005; Foster and Wilson, 2007). To test whether this relationship between theta and cell activity existed in the present dataset the mean theta frequency in each hour of recording was compared with the mean normalized firing rate of place cells recorded from the same animals and previously reported in Munn and Bilkey (2012); there was a very strong correlation between these two datasets (r = 0.907, p < 0.001). In our previous study (Munn and Bilkey, 2012) we had demonstrated that the mean firing rate of hippocampal place cells, was modulated at circadian periods and that this data was best fitted to a sinusoidal wave with a period of 25 h and a positive peak 2 h after recording onset. Given the relationship between firing rate and theta frequency observed in our data and the results of the initial analysis that indicated an acrophase in the theta data at or near to the recording start we set up the a priori hypothesis that guided all subsequent data analyses; that the theta frequency dataset would be well-fitted by a sinusoid with a 25 h period and peak 2 h into the recording, when the individual data were referenced to the proper entraining stimulus. This procedure markedly reduced the degrees of freedom in our analysis. When a comparison was made between this reference sine and normalized theta frequency as determined at the point of maximum power within the theta band a significant correlation was apparent (r = 0.414, p = 0.02; Figure 1A). This association decreased slightly but remained significant when the contribution of movement speed (determined from the average speed in each recording hour) was partialled out (r = 0.404, p = 0.026). Mean running speed itself was not significantly correlated with mean theta frequency (r = 0.088, p = 0.637, n.s) or with the sine reference (r = 0.223, p = 0.228, n.s).


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 frequency of spontaneously generated hippocampal theta rhythm during each hour of recording (black line). The reference sine wave used for comparison is shown in red. (B) The frequency distribution produced by correlating 1000 shuffled versions of the data shown in (A) against the reference sine. The vertical dashed black lines demark two standard deviations from the mean of the distribution. The vertical black arrow indicates the magnitude of the correlation of the unshuffled data shown in (A) against the reference sine.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: (A) The mean (±sem) normalized frequency of spontaneously generated hippocampal theta rhythm during each hour of recording (black line). The reference sine wave used for comparison is shown in red. (B) The frequency distribution produced by correlating 1000 shuffled versions of the data shown in (A) against the reference sine. The vertical dashed black lines demark two standard deviations from the mean of the distribution. The vertical black arrow indicates the magnitude of the correlation of the unshuffled data shown in (A) against the reference sine.
Mentions: It has previously been established that the firing rate of CA1 place cells is associated with features of hippocampal theta (Buzsàki and Eidelberg, 1983; Fox et al., 1986; O’Keefe and Recce, 1993; Skaggs et al., 1996; Hasselmo, 2005; Foster and Wilson, 2007). To test whether this relationship between theta and cell activity existed in the present dataset the mean theta frequency in each hour of recording was compared with the mean normalized firing rate of place cells recorded from the same animals and previously reported in Munn and Bilkey (2012); there was a very strong correlation between these two datasets (r = 0.907, p < 0.001). In our previous study (Munn and Bilkey, 2012) we had demonstrated that the mean firing rate of hippocampal place cells, was modulated at circadian periods and that this data was best fitted to a sinusoidal wave with a period of 25 h and a positive peak 2 h after recording onset. Given the relationship between firing rate and theta frequency observed in our data and the results of the initial analysis that indicated an acrophase in the theta data at or near to the recording start we set up the a priori hypothesis that guided all subsequent data analyses; that the theta frequency dataset would be well-fitted by a sinusoid with a 25 h period and peak 2 h into the recording, when the individual data were referenced to the proper entraining stimulus. This procedure markedly reduced the degrees of freedom in our analysis. When a comparison was made between this reference sine and normalized theta frequency as determined at the point of maximum power within the theta band a significant correlation was apparent (r = 0.414, p = 0.02; Figure 1A). This association decreased slightly but remained significant when the contribution of movement speed (determined from the average speed in each recording hour) was partialled out (r = 0.404, p = 0.026). Mean running speed itself was not significantly correlated with mean theta frequency (r = 0.088, p = 0.637, n.s) or with the sine reference (r = 0.223, p = 0.228, n.s).

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