Synchronous λ frequency oscillations (20-80 Hz) represent a temporally coherent activity and are thought to be important in cortical information processing. Hippocampal interneurons have a pivotal role in driving inhibition-based rhythms, including gamma frequency network oscillations. It is, however, unknown whether different types of interneurons show a different degree of involvement during λ activity. Therefore, using brief pressure ejection of kainate, an approach that allowed us to generate network oscillatory activity in submerged slices, we investigated how the anatomical heterogeneity of hippocampal interneurons is reflected in their behaviour during λ frequency oscillations.
Hippocampal slices (450 mm thickness) were prepared from C57 mice (P 18-25). All animals were humanely killed. Whilst measuring extracellular field potentials whole-cell patch-clamp recordings in current and voltage clamp mode were obtained from stratum oriens/alveus interneurons in area CA3. Patch pipettes contained the marker biocytin and all labelled neurons were processed for post-hoc anatomical identification. Student’s t test was used for statistical comparisons. Average values are expressed as means ± S.E.M.
Our data demonstrate a differential degree of involvement of two types of stratum oriens interneurons in network activity, distal dendrite targeting O-LM and proximal dendrite targeting trilaminar cells. The kinetics of the EPSP/Cs and the amplitude of synaptic events of these cells during oscillations were significantly different. The mean amplitude of excitatory synaptic currents in O-LM interneurons was 54.3 ± 1.6 pA, being significantly smaller than those in trilaminar cells (150.1 ± 8.8 pA; P < 0.05). Likewise, the 10-90 % rise time of averaged EPSCs in O-LM interneurons was slower (0.84 ± 0.09 ms) than those in trilaminar cells (0.53 ± 0.05 ms). The mean decay time constant of EPSCs was 2.52 ± 0.20 ms in O-LM cells and 1.40 ± 0.23 ms in trilaminar cells (P < 0.05). Moreover, although both classes of cells received a similar sustained barrage of high-frequency (~300 Hz) rhythmic input, modulated at gamma frequency, their discharge patterns were significantly different. O-LM interneurons consistently fired at lower frequencies in the theta frequency range (mean 9.0 ± 2.7 Hz, n = 7), whereas trilaminar interneurons generated at least one action potential per gamma cycle, frequently firing spike doublets (n = 4).
These observations demonstrate that distally targeting O-LM interneurons generate theta frequency-modulated output during field λ, whereas trilaminar interneurons phase postsynaptic cells with λ frequency IPSPs and presumably play a critical role in the generation and maintenance of rhythmic oscillatory activity in this frequency band.
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