University of Alberta

Year: 2010

Ups and downs in the hippocampus: the influence of oscillatory sleep states on “neuroplasticity” at different time scales

PMID: 20394778

Dickson CT

Behav. Brain Res. 2010 Dec;214(1):35-41


Spontaneous state-dependent oscillatory dynamics in the brain are relevant to both ongoing and prospective neural and behavioural function. In the hippocampus, the presence of different patterns of coordinated network activity during offline (sleep) states has the potential to modify neural connections and thus influence memory storage. In addition to theta (3-12Hz) and ripple (100-300Hz) activity, the hippocampus also demonstrates a slow oscillation (SO: < or =1Hz) during sleep which prominently organizes hippocampal cellular activity and dynamically coordinates ensembles across the entire forebrain into temporal frames of activity (UP) and inactivity (DOWN). The SO also significantly modulates hippocampal excitatory synaptic transmission on both a short (within cycle) and medium (across state) time scale and through its dynamic coordination with neocortical areas has the potential to function as a platform for long-term bidirectional synaptic plasticity. Recent evidence suggests that it is of direct benefit for the consolidation of hippocampal-dependent memories and thus, further investigation of its mechanisms in modulating short-to-long-term neural plasticity is certainly warranted.

Short-duration epileptic discharges show a distinct phase preference during ongoing hippocampal slow oscillations

PMID: 20719925

de Guzman PH, Nazer F, Dickson CT

J. Neurophysiol. 2010 Oct;104(4):2194-202


Non-REM (slow-wave) sleep has been shown to facilitate temporal lobe epileptiform events, whereas REM sleep seems more restrictive. This state-dependent modulation may be the result of the enhancement of excitatory synaptic transmission and/or the degree of network synchronization expressed within the hippocampus of the temporal lobe. The slow oscillation (SO), a ∼1 Hz oscillatory pattern expressed during non-REM sleep and urethane anesthesia, has been recently shown to facilitate the generation, maintenance, and propagation of stimulus-evoked epileptiform activity in the hippocampus. To further address the state-dependent modulation of epileptic activity during the SO, we studied the properties of short-duration interictal-like activity generated by focal application of penicillin in the hippocampus of urethane-anesthetized rats. Epileptiform spikes were larger but only slightly more prevalent during the SO as opposed to the theta (REM-like) state. More notably, however, epileptic spikes had a significant tendency to occur just following the peak negativity of ongoing SO cycles. Because of the known phase-dependent changes in 1) synaptic excitability (just following the positive peak of the SO) and 2) network synchronization (during the negative peak of the SO), these results suggest that it is the synchrony and not the changes in synaptic excitability that lead to the facilitation of epileptiform activity during sleep-like slow wave states.

Changes in hippocampal excitatory synaptic transmission during cholinergically induced theta and slow oscillation states

PMID: 19437417

Schall KP, Dickson CT

Hippocampus 2010 Feb;20(2):279-92


Neural processing in the hippocampus (HPC) during sleep is important for declarative memory storage. Previously, we have shown that alternations of sleep-like REM and non-REM brain states that involve changing patterns of synchronized oscillatory network activity in the HPC [i.e., theta and the slow oscillation (SO), respectively] robustly and differentially influence excitatory synaptic transmission in a variety of hippocampal pathways. Given that state in the HPC is dependent on variations in cholinergic tone in both sleep and under urethane anesthesia, in the present study we induced theta and SO states via systemic cholinergic manipulations in urethane-anesthetized rats to confirm similar changes in synaptic responsiveness. This was conducted using linear multiprobe recordings and current source density analysis of electrically evoked potentials in commissural and temporal ammonic inputs to CA1 and medial and lateral perforant path inputs to dentate gyrus (DG). Cholinergic agonism and antagonism induced theta and the SO, respectively, and similarly to the case with spontaneous states, also diminished and promoted, respectively, excitatory synaptic currents in all pathways (except for the medial perforant path input to DG which showed the opposite modulation). These results suggest that both state and cholinergic tone bias the hippocampal network during natural sleep across REM and non-REM episodes and that this modulation may play an important role in the consolidation of declarative memories.

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