Origin of Active States in Local Neocortical Networks during Slow Sleep Oscillation

Abstract

Slow-wave sleep is characterized by spontaneous alternations of activity and silence in corticothalamic networks, but the causes of transition from silence to activity remain unknown. We investigated local mechanisms underlying initiation of activity, using simultaneous multisite field potential, multiunit recordings, and intracellular recordings from 2 to 4 nearby neurons in naturally sleeping or anesthetized cats. We demonstrate that activity may start in any neuron or recording location, with tens of milliseconds delay in other cells and sites. Typically, however, activity originated at deep locations, then involved some superficial cells, but appeared later in the middle of the cortex. Neuronal firing was also found to begin, after the onset of active states, at depths that correspond to cortical layer V. These results support the hypothesis that switch from silence to activity is mediated by spontaneous synaptic events, whereby any neuron may become active first. Due to probabilistic nature of activity onset, the large pyramidal cells from deep cortical layers, which are equipped with the most numerous synaptic inputs and large projection fields, are best suited for switching the whole network into active state.

In vivo validation of the electronic depth control probes

“…Previous investigations showed large cortical oscillatory power in a wide frequency band (10 -200 Hz) during up-states, while the spectral power was much smaller during down-states. Our findings are in a perfect match with these reports [2,3,16]. Consistent with prior studies in animals, we have shown that the up-state was associated with increased firing and elevated spindle and gamma power during the surface-positive LFP half-wave, while the down-state was characterized by the widespread surface-negative LFP half-wave with decreased firing, and oscillatory activity.…”

“…More specifically, we found that the LFP is rhythmic at about 1 Hz; its depth profile well corresponds to previous findings, where the LFP inversion was taking place in layer III corresponding to a depth about 300 -500 μ m below the cortical surface [2,3,16]. We have also shown that the bimodality of the oscillation using MUA measures can be reliably characterized, which is also in correspondence with the basic properties of SWA and previous findings.…”

“…The up-state LFP is positive on the brain surface and negative in deeper layers; it contains nested higher-frequency oscillations (e.g., 5 -100 Hz) accompanied by cell firing. The down-state LFP is negative on the brain surface and inverts to positivity in the deeper layers, and contains no spectral or cellular firing activity [2,3,16].…”

“…By using the time stamps of the down-to up-state transition as a reference point, the average spatial, temporal, and spectral patterns of the SWA were calculated to relate our measurements to the findings of other results using different probes [2,3,16].…”

Supervised semi-automatic detection of slow waves in non-anaesthetized mice with the use of neural network approach

“…Simultaneous recordings of cortical intracellular activity and LFP showed that the SWs reflect synchronized activity of large groups of cortical neurons that nearly simultaneously alternate between depolarized and hyperpolarized states [2][3][4][5][6][7].…”