Interneuron-specific plasticity at parvalbumin and somatostatin inhibitory synapses onto CA1 pyramidal neurons shapes hippocampal output

• Published in: Nature communications Vol. 11; no. 1; p. 4395
• Main Authors: Udakis, Matt, Pedrosa, Victor, Chamberlain, Sophie E. L., Clopath, Claudia, Mellor, Jack R.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 02.09.2020; Nature Publishing Group; Nature Portfolio
• Subjects: 13; 631/378/116/1925; 631/378/1595/1554; 631/378/2591/2595; 9/74; Action Potentials; Activity patterns; Animals; CA1 Region, Hippocampal - cytology; CA1 Region, Hippocampal - physiology; Calcium; Calcium channels (T-type); Calcium Channels, T-Type - metabolism; Channelrhodopsins - metabolism; Circuits; Cortex (entorhinal); Hippocampus; Hippocampus - cytology; Hippocampus - physiology; Humanities and Social Sciences; Interneurons; Interneurons - metabolism; Light; Long-term depression; Long-term potentiation; Mice; multidisciplinary; Neurons; Optogenetics - methods; Parvalbumin; Parvalbumins - metabolism; Patch-Clamp Techniques; Photovoltaic cells; Plastic properties; Plasticity; Pyramidal cells; Pyramidal Cells - physiology; Representations; Science; Science (multidisciplinary); Signal Transduction; Somatostatin; Somatostatin - metabolism; Spatial discrimination; Synapses; Synapses - metabolism; Synaptic depression; Synaptic strength
• DOI: 10.1038/s41467-020-18074-8
• ISSN: 2041-1723

The formation and maintenance of spatial representations within hippocampal cell assemblies is strongly dictated by patterns of inhibition from diverse interneuron populations. Although it is known that inhibitory synaptic strength is malleable, induction of long-term plasticity at distinct inhibitory synapses and its regulation of hippocampal network activity is not well understood. Here, we show that inhibitory synapses from parvalbumin and somatostatin expressing interneurons undergo long-term depression and potentiation respectively (PV-iLTD and SST-iLTP) during physiological activity patterns. Both forms of plasticity rely on T-type calcium channel activation to confer synapse specificity but otherwise employ distinct mechanisms. Since parvalbumin and somatostatin interneurons preferentially target perisomatic and distal dendritic regions respectively of CA1 pyramidal cells, PV-iLTD and SST-iLTP coordinate a reprioritisation of excitatory inputs from entorhinal cortex and CA3. Furthermore, circuit-level modelling reveals that PV-iLTD and SST-iLTP cooperate to stabilise place cells while facilitating representation of multiple unique environments within the hippocampal network. Inhibitory interneuron subtypes differentially control place cell representations in CA1. Here, the authors show that parvalbumin and somatostatin interneuron synapses onto CA1 pyramidal neurons exhibit distinct plasticity mechanisms and incorporating this insight into circuit-level modeling leads to stable place cell representations.