Structural and functional changes in the hippocampal neuronal network of the brain allow organisms to adapt to the environment. Such plasticity leads to the encoding of newly acquired information and the replacement or updating of stored knowledge by new experience. Information is carried by the output of active pyramidal cell assemblies during transient network oscillations. In the CA1 area, the activity of pyramidal cells is regulated by at least 22 distinct types of GABAergic interneuron, some expressing the neuropeptide somatostatin (SOM) and innervating the dendrites of their postsynaptic targets. The in vivo spike-timing of identified types of GABAergic cell in freely moving rodents has been largely unknown until recently. Although thousands of interneurons have been reported from large scale extracellular recordings their identity has remained indefinite. How do different types of GABAergic cell regulate pyramidal cell output during behaviour? We have explored the roles of identified hippocampal interneuron types during network rhythms. Specifically, we have tested the hypothesis that distinct types of GABAergic cell have different effects on pyramidal cell firing during exploration and sleep. First, we have extracellularly recorded single interneurons in freely moving rats (male, 300-570 g, n=14) followed by neurobiotin-labelling of these neurons using the juxtacellular technique for cell type identification (Lapray et al., 2012). Results: 1. The reported neurons are SOM- and/or NPY-expressing, dendrite-targeting cells, including O-LM (n=4), bistratified (n=5) and putative projection cells (n=5). 2. Behaviour and network states differentiate the activities of SOM-expressing GABAergic cell types in freely moving rats, as shown by comparing firing rates (mean±s.e.m.) per cell type per behavioural- or network states using repeated-measures ANOVA. 3. During sleep, O-LM cells decrease firing to 11.9±5.2 Hz from 20.9±5.2 Hz during awake states, and are mostly inhibited during sharp wave-ripples (SWRs). 4. Bistratified cells fire at higher rates during sleep (28.7±5.0 Hz) than O-LM cells (11.9±5.2 Hz) and projection cells (14.4±2.8 Hz), and unlike O-LM cells, strongly increase spiking during SWRs. Projection cells have variable SWR responses. 5. During movement, O-LM (19.0±8.1 Hz) and bistratified cells (35.8±7.2 Hz) fire cooperatively at the troughs of theta oscillations but with different frequencies. Individual projection cells couple their spiking to different phases of theta cycles. We suggest that GABA and SOM are differentially released to distinct dendritic zones of CA1 pyramidal cells during sleep and wakefulness to coordinate segregated glutamatergic inputs from the CA3 area and the entorhinal cortex. Furthermore, long-range projections may synchronise the activity of regionally distributed pyramidal cells.
Physiology 2014 (London, UK) (2014) Proc Physiol Soc 31, C18
Oral Communications: Sleep and movement segregate distinct types of somatostatin-expressing GABAergic interneuron in hippocampal network operations
L. Katona1, T. Viney1, D. Lapray1,2, B. Micklem1, Z. Borhegyi3, T. Klausberger1,3, P. Somogyi1,3
1. MRC Anatomical Neuropharmacology Unit, University of Oxford, Oxford, United Kingdom. 2. Brain Mind Institute, EPFL, Lausanne, Switzerland. 3. Center for Brain Research, Medical University of Vienna, Vienna, Austria.
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