Different types of theta rhythmicity are induced by social and fearful stimuli in a network associated with social memory
- University of Haifa, Israel
Figures
Figure 1
A simplistic scheme of sensory information flow in the network of brain regions thought to underlie social recognition memory.
Social olfactory cues are detected by sensory neurons in the main olfactory epithelium (MOE) and vomeronasal organ (VNO). These neurons project to the main (MOB) and accessory (AOB) olfactory bulbs, …
Figure 2
Theta rhythmicity in the rat brain is enhanced during social encounters, in correlation with the novelty of the social stimulus.
(A) A scheme of the habituation–dishabituation SRM paradigm. (B) Examples of LFP traces recorded in the MOB, LS, and MeA during a social encounter. (C) Power spectral density (PSD) analyses of a …
Figure 3
Theta rhythmicity is modulated by the novelty of social, but not other tested stimuli.
(A) TP for all brain areas (upper) as well as IT (lower) during the SRM test of one animal, using awake and anesthetized social stimuli as well as object and smell stimuli, all except smell tested …
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Figure 3—source data 1
Theta power (TP) modulation between encounters.
One-way ANOVA (repeated measures) test was used to determine whether there is a significant difference between the mean ΔTP of all five encounters during either social (1a) or object (1b) recognition. The assumption of normality was assessed by Lilliefors and Shapiro–Wilk tests. Sphericity was assessed by Mauchly's test.
- https://doi.org/10.7554/eLife.03614.007
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Figure 3—source data 2
Statistical assessment of habituation and dishabituation.
Paired t-tests were used for the social (2a) and object (2b) recognition paradigms, to examine if the differences between Enc.1 and Enc. 4 (habituation), as well as between Enc. 4 and Enc. 5 (dishabituation) are statistically significant. Tests were one-sided and corrected for multiple comparisons using Bonferroni's correction.
- https://doi.org/10.7554/eLife.03614.008
Figure 4 with 7 supplements
Modulation of the theta rhythmicity by social stimulus novelty reflects an internal state in the brain.
(A) Color-coded spectrograms of the LFP recorded in the MOB (upper), LS (middle), and MeA (lower) for 5 min before (Base), during (Enc. 1), and after (Post 1) the first encounter of the SRM test. …
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Figure 4—source data 1
Comparison of ΔTP between Enc. and Post periods.
Paired t-tests were used to compare between the mean ΔTP across Enc. vs the mean ΔTP across Post periods. The assumption of normality was assessed by Lilliefors and Shapiro–Wilk tests.
- https://doi.org/10.7554/eLife.03614.010
Figure 4—figure supplement 1
Mean LFP spectrograms across the SRM paradigm for the AOB.
Color-coded spectrograms (0–20 Hz) of the LFP recorded in the AOB during the SRM test. Gray bar marks the 15 s needed for stimulus delivery to the arena. Mean of five animals.
Figure 4—figure supplement 2
Mean LFP spectrograms across the SRM paradigm for the MOB.
Color-coded spectrograms (0–20 Hz) of the LFP recorded in the MOB during the SRM test. Gray bar marks the 15 s needed for stimulus delivery to the arena. Mean of five animals.
Figure 4—figure supplement 3
Mean LFP spectrograms across the SRM paradigm for the MEA.
Color-coded spectrograms (0–20 Hz) of the LFP recorded in the MEA during the SRM test. Gray bar marks the 15 s needed for stimulus delivery to the arena. Mean of five animals.
Figure 4—figure supplement 4
Mean LFP spectrograms across the SRM paradigm for the LS.
Color-coded spectrograms (0–20 Hz) of the LFP recorded in the LS during the SRM test. Gray bar marks the 15 s needed for stimulus delivery to the arena. Mean of four animals.
Figure 4—figure supplement 5
Mean LFP spectrograms across the SRM paradigm for the Pir.
Color-coded spectrograms (0–20 Hz) of the LFP recorded in the Pir during the SRM test. Gray bar marks the 15 s needed for stimulus delivery to the arena. Mean of five animals.
Figure 4—figure supplement 6
Comparison of mean instantaneous TP between social and object stimuli, for the AOB and MOB.
Upper panels—instantaneous ΔTP (change from mean Base) in each brain area averaged over all animals (mean ± SEM) during the Enc. and Post periods of all trials (1–5), for social (left, n = 5 rats) …
Figure 4—figure supplement 7
Comparison of mean instantaneous TP between social and object stimuli, for the MeA and Pir.
Upper panels—instantaneous ΔTP (change from mean Base) in each brain area averaged over all animals (mean±SEM) during the Enc. and Post periods of all trials (1–5), for social (left, n = 5 rats) and …
Figure 5
Differential and dynamic correlation of theta rhythmicity between specific brain regions.
(A) Upper—superimposed LFP traces (filtered 5–11 Hz) from the MeA (black) and LS (colored) of one animal during Base (left, red) and Enc. 1 (right, blue). Lower—cross-correlations between both …
Figure 6 with 3 supplements
Theta coherence between specific brain regions increases during social encounter.
(A) Mean (n = 10 animals) coherence (0–100 Hz) of the LFP signals recorded in the MeA and LS during Base, Enc. 1, and Post 1 periods. (B) Same animals, coherence analysis between the MeA and MOB. (C)…
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Figure 6—source data 1
Assessment of change in theta Coherence from Base to either Enc. 1 or Post 1.
The change from Base to Enc. 1 (upper) and from Base to Post 1 (lower), in theta coherence during social recognition between the MeA and all other areas (1a) and between the MOB and all areas (1b), as well as during object recognition between the MeA and all other areas (1c), and between the MOB and all areas (1d), was statistically validated using paired t-tests, corrected for multiple comparisons (Bonferroni correction). The assumption of normality was assessed by Lilliefors and Shapiro–Wilk tests.
- https://doi.org/10.7554/eLife.03614.020
Figure 6—figure supplement 1
Mean spectrograms of coherence between the MeA and all other areas during trial 1 of the SRM paradigm.
Color-coded spectrograms (0–20 Hz) of the mean LFP coherence (MOB, AOB—n = 11; LS, Pir—n = 10, cMeA—contralateral MeA—n = 3) between the MOB and all other brain areas, during the first trial of SRM …
Figure 6—figure supplement 2
Mean spectrograms of coherence between the MOB and all other areas during trial 1 of the SRM paradigm.
Color-coded spectrograms (0–20 Hz) of the mean LFP coherence (MeA, AOB—n = 11; LS, Pir—n = 10, cMeA—contralateral MeA—n = 3) between the MOB and all other brain areas, during the first trial of SRM …
Figure 6—figure supplement 3
Mean theta coherence during trial 1 of the SRM paradigm.
(A) Mean coherence at 8 Hz between the MeA and all other areas (MOB, AOB n = 11; LS, Pir n = 10, cMeA—contralateral MeA—n = 3) during the Base, Enc. 1, and Post 1 periods of the SRM paradigm. (B) …
Figure 7 with 1 supplement
Distinct types of theta rhythmicity are induced by social and fearful stimuli.
(A) PSD analyses (0–20 Hz) of LFP signal recorded in the LS of one animal, 5 min prior to stimulus introduction (Base, red) and 15 s following it (Stimulus, blue) during fear memory recall (left, …
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Figure 7—source data 1
Comparison of change in theta power in low and high theta bands between social and fearful stimuli.
Comparison of the change in theta power between social recognition (SR) and fear conditioning (FC) at high and low theta ranges, statistically validated using two-way repeated measures ANOVA (p—experiment X theta range interaction). The assumption of normality was assessed by Lilliefors and Shapiro–Wilk tests.
- https://doi.org/10.7554/eLife.03614.025
Figure 7—figure supplement 1
Arousal-driven locomotion during recall of fear memory.
(A) A schematic drawing of the fear conditioning session, comprising five events of 40-sec tone (gray bar) followed by brief electrical foot shock (red bar). (B) Locomotion activity of one animal …
Figure 8
Distinct changes in theta coherence between various brain regions are induced by social and fearful stimuli.
(A) Coherence analyses (0–20 Hz) of LFP signal recorded in the LS and MeA of one animal, 5 min prior to stimulus introduction (Base, red) and 15 s following it (Stimulus, blue) during fear memory …
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Figure 8—source data 1
Comparison of change in coherence in low and high theta bands between social and fearful stimuli.
Comparison of the change in coherence between social recognition (SR) and fear conditioning (FC) at high and low theta ranges (right), statistically validated using two-way repeated measures ANOVA (p—experiment X theta range interaction). The assumption of normality was assessed by Lilliefors and Shapiro–Wilk tests.
- https://doi.org/10.7554/eLife.03614.028
Figure 9
Different patterns of coherence change characterize the distinct arousal states.
Graphical color-coded presentation of the mean changes in coherence for the FC and SR experiments.
Videos
Video 1
Social encounter between two adult male rats in the experimental arena.
The recorded subject carries a black transmitter equipped with a flashing led light on its head. Frame number is shown in the right low corner. The graph below the video shows the LFP recorded in …
