Long-term plasticity in identified hippocampal GABAergic interneurons in the CA1 area in vivo

Petrina Yau-Pok Lau,Kathryn Newton,Karri P Lamsa,Peter Saghy,Peter Somogyi,Linda Katona

doi:10.1007/s00429-016-1309-7

Petrina Yau-Pok Lau, Kathryn Newton + Show 4 more

Open Access

https://doi.org/10.1007/s00429-016-1309-7

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Abstract

Long-term plasticity is well documented in synapses between glutamatergic principal cells in the cortex both in vitro and in vivo. Long-term potentiation (LTP) and -depression (LTD) have also been reported in glutamatergic connections to hippocampal GABAergic interneurons expressing parvalbumin (PV+) or nitric oxide synthase (NOS+) in brain slices, but plasticity in these cells has not been tested in vivo. We investigated synaptically-evoked suprathreshold excitation of identified hippocampal neurons in the CA1 area of urethane-anaesthetized rats. Neurons were recorded extracellularly with glass microelectrodes, and labelled with neurobiotin for anatomical analyses. Single-shock electrical stimulation of afferents from the contralateral CA1 elicited postsynaptic action potentials with monosynaptic features showing short delay (9.95 ± 0.41 ms) and small jitter in 13 neurons through the commissural pathway. Theta-burst stimulation (TBS) generated LTP of the synaptically-evoked spike probability in pyramidal cells, and in a bistratified cell and two unidentified fast-spiking interneurons. On the contrary, PV+ basket cells and NOS+ ivy cells exhibited either LTD or LTP. An identified axo-axonic cell failed to show long-term change in its response to stimulation. Discharge of the cells did not explain whether LTP or LTD was generated. For the fast-spiking interneurons, as a group, no correlation was found between plasticity and local field potential oscillations (1–3 or 3–6 Hz components) recorded immediately prior to TBS. The results demonstrate activity-induced long-term plasticity in synaptic excitation of hippocampal PV+ and NOS+ interneurons in vivo. Physiological and pathological activity patterns in vivo may generate similar plasticity in these interneurons.

Highlights

Activity-induced long-term plasticity characterizes neuronal communication widely in the brain providing cellular level mechanisms for learning and memory (Morris 2013)
In 13 out of 72 spontaneously active cells recorded in the CA1 area, phaselocked action potential to single-shock stimulation was elicited with a short delay (9.95 ± 0.41 ms, n = 13, see methods for criteria) that corresponds to monosynaptic excitatory pathway (Buzsaki and Eidelberg 1982a, b)
Our experiments demonstrate that extracellullar recording with juxtacellular labeling for neuron identification allows a stable and non-invasive approach for measurements of changes in synaptic excitation in hippocampal neurons in vivo

Summary

Introduction

Activity-induced long-term plasticity characterizes neuronal communication widely in the brain providing cellular level mechanisms for learning and memory (Morris 2013). Various long-term plasticity forms have been characterized in interactions between glutamatergic neurons in the cortex in ex vivo slice preparation and in the intact brain in vivo. These include activity-induced synaptic long-term potentiation (LTP) and -depression (LTD), and changes in postsynaptic neuron excitability (Collingridge et al 2010; Luscher et al 2000; Lisman and Spruston 2005; Daoudal and Debanne 2003). We have investigated activity-induced long-term plasticity in synaptically evoked firing of identified CA1 interneurons in vivo in rats under urethane anesthesia in order to improve recording stability, and compared plasticity results after TBS stimulation during different oscillatory network states recorded as local field potential

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