Rhythmic properties of the hamster suprachiasmatic nucleus in vivo

Abstract

We recorded multiple unit neural activity [multiunit activity (MUA)] from inside and outside of the suprachiasmatic nucleus (SCN) in freely moving male golden hamsters housed in running-wheel cages under both light/dark cycles and constant darkness. The circadian period of MUA in the SCN matched the period of locomotor activity; it was approximately 24 hr in wild-type and 20 hr in homozygous tau mutant hamsters. The peak of MUA in the SCN always occurred in the middle of the day or, in constant darkness, the subjective day. There were circadian rhythms of MUA outside of the SCN in the ventrolateral thalamic nucleus, the caudate putamen, the accumbens nucleus, the medial septum, the lateral septum, the ventromedial hypothalamic nucleus, the medial preoptic region, and the stria medullaris. These rhythms were out-of-phase with the electrical rhythm in the SCN but in-phase with the rhythm of locomotor activity, peaking during the night or subjective night. In addition to circadian rhythms, there were significant ultradian rhythms present; one, with a period of approximately 80 min, was in antiphase between the SCN and other brain areas, and another, with a period of approximately 14 min, was in-phase between the SCN and other brain areas. The periods of these ultradian rhythms were not significantly different in wild-type and tau mutant hamsters. Of particular interest was the unique phase relationship between the MUA of the bed nucleus of the stria terminalis (BNST) and the SCN; in these two areas both circadian and ultradian components were always in-phase. This suggests that the BNST is strongly coupled to the SCN and may be one of its major output pathways. In addition to circadian and ultradian rhythms of MUA, neural activity both within and outside the SCN was acutely affected by locomotor activity. Whenever a hamster ran on its wheel, MUA in the SCN and the BNST was suppressed, and MUA in other areas was enhanced.

Fig. 1.

Examples of MUA recorded for 10 d from the SCN of three wild-type hamsters. Animals were kept in light/dark cycles (14:10 hr LD) for 4 d and then released into constant darkness (lighting condition indicated at thebottom of the figure). Neuronal spikes are plotted in 6 min bins. Wheel-running activity is plotted at thebottom of A–C as the number of revolutions per 6 min; the y-axis for this portion of the figure shows 0–200 revolutions per 6 min. A, Recorded from the ventrolateral portion of the central region of the left SCN. B, Recorded from the ventromedial portion of the right SCN at the center of the rostrocaudal axis. C, Recorded from the ventromedial portion of the right SCN near the caudal end of the nucleus.

Fig. 2.

Daily and circadian rhythms of neural activity in several regions of the brain. MUA and locomotor activity are plotted in 6 min bins as in Figure 1. Recordings were made from the following:A, right side of the ventrolateral thalamic nucleus (VLT); B, right side of the medial septum (MS); C, right side of the stria medullaris (sm); D, right side of the LS;E, the optic chiasm (oc). Each plot represents a different wild-type hamster except forA (same animal as in E) andC (same animal as in Fig. 1C). Note (most clearly in B) that the peak of neural activity coincides with wheel-running activity.

Fig. 3.

Wheel-running behavior and neural activity records from the SCN and LS of a wild-type hamster (WT) in constant darkness. Electrodes were located in the left ventromedial region of the central SCN and in the right LS. The time scale shows hours after the hamster was released into constant darkness. A, MUA in the SCN in 6 min bins.B, MUA in the LS in 6 min bins.C, Wheel revolutions per 6 min. The data marked by thedouble-headed arrows are presented below (see Fig. 8).

Fig. 4.

Mathematical analysis of the phase angle difference of the circadian rhythms recorded in the SCN and LS in a wild-type hamster. Original data are shown in Figure3A,B. Data reconstructed by SSA for the SCN (A) and for the LS (B).C, Instantaneous phase angle difference between the circadian rhythms shown in A and B. The time series A and B were individually converted to their Hilbert transforms (the time series with a 90° phase shift). The resultant time series are series of complex numbers representing the original data (real part) and the Hilbert transform (imaginary part). The magnitude of each of these complex numbers is an estimate at that time of the circadian rhythm amplitude (data not shown). The angle of each of these complex numbers is an estimate at that time of the phase of the circadian rhythm relative to the beginning. The difference between the angles of A andB at each point is the instantaneous phase difference between the two circadian rhythms.

Fig. 5.

Wheel-running behavior and neural activity records from the SCN and CP of a tau mutant hamster in constant darkness. Electrodes were located in the right ventromedial part of the central region of the SCN and in the right CP. A, MUA in the SCN in 6 min bins. B, MUA in the CP in 6 min bins.C, Wheel revolutions per 6 min. The data marked by thedouble-headed arrows are presented below (see Fig. 10).SS, Homozygous taumutant.

Fig. 6.

Mathematical analysis of the phase angle difference of the circadian rhythms recorded in the SCN and CP in atau mutant hamster. Original data are shown in Figure 5.A, B, Data reconstructed by SSA for the SCN (A) and for the CP (B).C, Instantaneous phase angle difference between the circadian rhythms shown in A andB.

Fig. 7.

Circadian and ultradian rhythms of MUA in the SCN of a tau mutant hamster in constant darkness. In this case, the bipolar electrode became separated in the brain, with one electrode positioned on the left side and the other positioned on the right side of the ventromedial region of the caudal SCN. Top bars of A and B show wheel-running activity, plotted as a black bar when the wheel revolved more than once in 6 min. The time scale shows hours after the animal was released into constant darkness. A, Plot of MUA in 6 min bins. B, Expanded plot of 20 hr (one circadian cycle for the tau mutant hamster) of data from A with neuronal activity in 1 min bins showing ultradian rhythms of both periods as well as the negative correlation between wheel-running activity and neural activity.

Fig. 8.

Ultradian rhythms in neural activity records from the SCN and LS of a wild-type hamster. A, Expanded plot of the 24 hr neural activity record in 1 min bins from the SCN (from Fig. 3A, double-headed arrow). Thetop bar shows wheel-running activity, plotted as ablack bar whenever the wheel revolved more than once in 6 min. B, Expanded plot of the concurrent record from the LS (from Fig. 3B, double-headed arrow). Note the negative correlation of neural activity with wheel-running activity in the SCN and the positive correlation in the LS.

Fig. 9.

Mathematical analysis of ultradian rhythms recorded from the SCN and LS (from Fig.3A,B). A, Data reconstructed by SSA of the 80 min ultradian rhythms in the SCN (solid line) and the LS (dotted line) for the first 72 hr of the record. B, Phase angle difference of the 80 min ultradian rhythms between the SCN and the LS plotted for 144 hr (see text and Fig. 4 for details).

Fig. 10.

Ultradian rhythms in neural activity records from the SCN and CP in a tau mutant hamster.A, Expanded plot of 24 hr neural activity in 1 min bins from the SCN (from Fig. 5A, double-headed arrow). The top bar shows wheel-running activity, plotted as a black bar whenever the wheel revolved more than once in 6 min. B, Expanded plot of the concurrent record from the CP (from Fig. 5B,double-headed arrow). Note the positive (CP) and negative (SCN) correlations with wheel-running behavior.

Fig. 11.

Mathematical analysis of the ultradian rhythms recorded from the SCN and CP in a tau mutant hamster.A, Data reconstructed by SSA of the 80 min ultradian rhythms in the SCN (solid line) and the CP (dotted line) for the first 72 hr of the record.B, Phase angle difference of the 80 min ultradian rhythms between the SCN and the CP plotted for 144 hr (see text and Fig. 4 for details).

Fig. 12.

Neural activity records obtained simultaneously from the SCN and the BNST in a wild-type hamster in constant darkness. Electrodes were located in the right ventromedial portion of the central SCN and in the right anteromedial portion of the BNST.A, MUA in the SCN in 6 min bins. B, MUA in the BNST in 6 min bins. C, Wheel revolutions per 6 min. The data marked by the double-headed arrows are presented below (see Fig. 14). Note the almost perfect phase lock between these two regions and that both are in antiphase with wheel running.

Fig. 13.

Mathematical analysis of the phase angle difference of the circadian rhythms recorded in the SCN and the BNST in a wild-type hamster (original data in Fig. 12). A,B, Data reconstructed by SSA for the SCN (A) and for the BNST (B).C, Instantaneous phase angle difference between the circadian rhythms shown in A and B (see text and Fig. 4 for details).

Fig. 14.

Ultradian rhythms of neural activity recorded from the SCN and the BNST in a wild-type hamster. A, Expanded plot of 24 hr neural activity record in 1 min bins from the SCN (from Fig. 12A, double-headed arrow). The top bar shows wheel-running activity, plotted as a black bar whenever the wheel revolved more than once in 6 min. B, Expanded plot of 24 hr neural activity record in 1 min bins from the BNST (from Fig.12B, double-headed arrow). Note that both the 80 and 14 min ultradian rhythms are usually in-phase.

Fig. 15.

Mathematical analysis of the ultradian rhythms recorded from the SCN and the BNST in a wild-type hamster.A, Data reconstructed by SSA of the 80 min ultradian rhythms in the SCN (solid line) and the BNST (dotted line) for the first 72 hr of the record.B, Phase angle difference of the 80 min ultradian rhythms between the SCN and the BNST plotted for 144 hr (see text and Fig. 4 for details).