Non-theta States Research Articles

Hippocampal interneuron activity in unanesthetized rats: Relationship to the sleep-wake cycle

Evoked population spikes and interneuronal discharges were recorded throughout the sleep-wake cycle in hippocampal regions CA1 and dentate gyrus (DG) of ten chronically implanted rats. During quiet wakefulness (QW) and slow-wave-sleep (SWS) (non-theta rhythm states), the primary shock of paired stimuli evoked in CA1 both high amplitude population spikes and multiple interneuron discharges when compared to active wakefulness (AW) and rapid-eye-movement (REM) sleep (theta rhythm states). A second shock was delivered to CA1 afferents 60 ms after the first shock. This second shock evoked a small population spikes during non-theta states, whereas it evoked higher amplitude population spikes in theta states. The second shock also evoked unit interneuron discharges in non-theta states but not in theta states. In the dentate gyrus, identical primary afferent stimulation evoked similar interneuron activity and uniform amplitude population spikes throughout the sleep-wake cycle. In contrast, the secondary shocks evoked a striking potentiation of the field population spike during sleep, SWS and REM sleep compared to AW and QW. Evoked DG interneuron spikes following the second population spike were greater in number during SWS compared to the other stages. Our findings suggest that hippocampal field potentials and interneuron activity recorded in vivo are regionally regulated, have unique state-dependent expression and are strongly influenced by inhibitory feed-forward mechanisms.

Coherence of compound field potentials reveals discontinuities in the CA1-subiculum of the hippocampus in freely-moving rats

The ongoing micro-electroencephalogram was recorded with a chronically implanted comb-like array of 16 tungsten semi-microelectrodes 0.2 or 0.25 mm apart, spanning CA1 strata oriens, pyramidale and radiatum and into subiculum, in four behavioral states: walking, standing still, paradoxical and slow wave sleep and under scopolamine. Power, phase and coherence spectra were computed, the latter two for each of the 120 pairs, in frequency bands from 1 to 64 Hz. (1) Coherence is high for all frequencies within the same subfield, e.g. stratum radiatum, but falls with distance. Theta frequency (8 Hz), when prominent and widespread (during “theta states” walking and paradoxical sleep), shows the most widespread synchrony: coherence falls slowly, from 1.0 at 0.2mm to 0.7 at c. 2 mm longitudinally within stratum radiatum; all other frequencies fall two or three times faster. (2) An abrupt drop in coherence occurs across field borders (CA1-subiculum) and between stratum oriens and radiatum, across a line just under stratum pyramidale, between high coherence regions on each side of the coherence discontinuity. A less extreme drop occurs in stratum radiatum 0.4 mm from the subiculum border, without obvious histological correlate. The discontinuities in coherence are stable through all four behavioral states as well as under scopolamine. (3) Phase profiles diagonally across CA1 and into subiculum show abrupt, local shifts of phase (up to 125°) at these same levels. No gradual shift reaching 180° (phase reversal) occurs in the span of loci examined. (4) The theta power peak in theta states is not necessarily due to additional energy in that band; in some conditions it is mainly due to reduced power in other frequencies. Root mean square voltage is generally less in the high theta (“synchronized”) than in the non-theta states. Only the theta peak correlates with a peak in coherence. (5) Significant microstructure in the dynamics of neuronal cooperativity distinguishes behavioral states and regions of the hippocampal cortex.

Neural group properties in the rat hippocampus during the theta rhythm.

The ensemble properties of unit activity in the rat hippocampus were studied during different behavioral states defined by the presence or absence of the theta rhythm. A 24-channel microelectrode was used to monitor the parallel activity of several single neurons simultaneously. Individual units were characterized by waveform, firing repertoire and firing relation to theta phase. Group patterns were characterized by multiple cross-correlations at different temporal resolutions during the presence and absence of the theta rhythm. Coactivation of units was frequently observed at a fine temporal resolution under both theta and non-theta states. In addition rhythmic synchronization of units was observed at a broader temporal resolution and was selective to the theta state. The combined findings suggest that the theta rhythm signifies a powerful patterning of group activity imposed upon a fixed connectivity of neighboring neurons.