A NOVEL SLOW (LESS-THAN-1 HZ) OSCILLATION OF NEOCORTICAL NEURONS IN-VIVO - DEPOLARIZING AND HYPERPOLARIZING COMPONENTS

We describe a novel slow oscillation in intracellular recordings from cortical association areas 5 and 7, motor areas 4 and 6, and visual ar eas 17 and 18 of cats under various anesthetics. The recorded neurons (n = 254) were antidromically and orthodromically identified as cortic othalamic or callosal elements receiving projections from appropriate thalamic nuclei as well as from homotopic foci in the contralateral co rtex. Two major types of cells were recorded: regular-spiking (mainly slow-adapting, but also fast-adapting) neurons and intrinsically burst ing cells. A group of slowly oscillating neurons (n = 21) were intrace llularly stained and found to be pyramidal-shaped cells in layers III- VI, with luxuriant basal dendritic arbors. The slow rhythm appeared in 88% of recorded neurons. It consisted of slow depolarizing envelopes (lasting for 0.81. 5 sec) with superimposed full action potentials or presumed dendritic spikes, followed by long-lasting hyperpolarizations . Such sequences recurred rhythmically at less than 1 Hz, with a preva iling oscillation between 0.3 and 0.4 Hz in 67% of urethane-anesthetiz ed animals. While in most neurons (almost-equal-to 70%) the repetitive spikes superimposed on the slow depolarization were completely blocke d by slight DC hyperpolarization, 30% of cells were found to display r elatively small (3-12 mV), rapid, all-or-none potentials after obliter ation of full action potentials. These fast spikes were suppressed in an all-or-none fashion at V(m) more negative than -90 mV. The depolari zing envelope of the slow rhythm was reduced or suppressed at a V(m) o f -90 to -100 mV and its duration was greatly reduced by administratio n of the NMDA blocker ketamine. In keeping with this action, most (56% ) neurons recorded in animals under ketamine and nitrous oxide or keta mine and xylazine anesthesia displayed the slow oscillation at higher frequencies (0.6-1 Hz) than under urethane anesthesia (0.3-0.4 Hz). In 18% of the oscillating cells, the slow rhythm mainly consisted of rep etitive (15-30 Hz), relatively short-lasting (15-25 msec) IPSPs that c ould be revealed by bringing the V(m) at more positive values than -70 mV. The long-lasting (almost-equal-to 1 sec) hyperpolarizing phase of the slow oscillation was best observed at the resting V(m) and was re duced at about -100 mV. Simultaneous recording of another cell across the membrane demonstrated synchronous inhibitory periods in both neuro ns. Intracellular diffusion of Cl- or Cs+ reduced the amplitude and/or duration of cyclic long-lasting hyperpolarizations. Thus, the newly d escribed oscillation is present in all investigated (sensory, motor, a nd associational) cortical areas, is displayed by morphologically and physiologically identified pyramidal cells, but does also seemingly in volve local-circuit inhibitory cells as inferred from the rhythmic (0. 3 Hz) sequences of repetitive IPSPs in pyramidal-type neurons. We then deal with a massive population event, as also indicated by the close correlation between the slow cellular and EEG oscillation. As shown in the following two companion articles (Steriade et al., 1993a,b), the slow cortical oscillation survives total lesions of thalamic perikarya projecting to the recorded cortical neurons and plays a pivotal role in grouping within the 0.3 Hz rhythm other sleep oscillations, such as spindle (7-14 Hz) and delta (1-4 Hz) waves. A new view of sleep oscil lations emerges, with various cerebral rhythms generated by intrinsic electrophysiological properties of thalamic and cortical neurons and b y synaptic interactions in complex corticothalamocortical networks.