Abstract
Medial septal GABAergic neurons of the basal forebrain innervate the hippocampus and related cortical areas, contributing to the coordination of network activity, such as theta oscillations and sharp wave-ripple events, via a preferential innervation of GABAergic interneurons. Individual medial septal neurons display diverse activity patterns, which may be related to their termination in different cortical areas and/or to the different types of innervated interneurons. To test these hypotheses, we extracellularly recorded and juxtacellularly labeled single medial septal neurons in anesthetized rats in vivo during hippocampal theta and ripple oscillations, traced their axons to distant cortical target areas, and analyzed their postsynaptic interneurons. Medial septal GABAergic neurons exhibiting different hippocampal theta phase preferences and/or sharp wave-ripple related activity terminated in restricted hippocampal regions, and selectively targeted a limited number of interneuron types, as established on the basis of molecular markers. We demonstrate the preferential innervation of bistratified cells in CA1 and of basket cells in CA3 by individual axons. One group of septal neurons was suppressed during sharp wave-ripples, maintained their firing rate across theta and non-theta network states and mainly fired along the descending phase of CA1 theta oscillations. In contrast, neurons that were active during sharp wave-ripples increased their firing significantly during “theta” compared to “non-theta” states, with most firing during the ascending phase of theta oscillations. These results demonstrate that specialized septal GABAergic neurons contribute to the coordination of network activity through parallel, target area- and cell type-selective projections to the hippocampus.
Highlights
Projections from the medial septum (MS) of the basal forebrain to the hippocampal formation provide a key contribution to hippocampal network activity and resulting1 3 Vol.:(0123456789)Brain Structure and Function (2018) 223:2409–2432(Petsche et al 1962), they have been proposed to be a key component of hippocampal theta genesis via disinhibition of principal cells (Freund and Antal 1988)
The temporal redistribution of inhibition depends on hippocampal network states, as different types of hippocampal interneuron show differential activity in relation to theta oscillations and sharp wave-ripple (SWR) events (Klausberger and Somogyi 2008)
Many MS neurons show preferential firing at specific phases of the hippocampal theta cycle (King et al 1998; Dragoi et al 1999), and they may be active, remain silent, or may be inhibited during SWRs (Borhegyi et al 2004; Viney et al 2013). It is not known whether individual septal neurons that fire differentially during network oscillations uniformly innervate all types of hippocampal interneuron or are selective for particular types of interneurons
Summary
Projections from the medial septum (MS) of the basal forebrain to the hippocampal formation provide a key contribution to hippocampal network activity and resulting1 3 Vol.:(0123456789)Brain Structure and Function (2018) 223:2409–2432(Petsche et al 1962), they have been proposed to be a key component of hippocampal theta genesis via disinhibition of principal cells (Freund and Antal 1988). The temporal redistribution of inhibition depends on hippocampal network states, as different types of hippocampal interneuron show differential activity in relation to theta oscillations and sharp wave-ripple (SWR) events (Klausberger and Somogyi 2008). Many MS neurons show preferential firing at specific phases of the hippocampal theta cycle (King et al 1998; Dragoi et al 1999), and they may be active, remain silent, or may be inhibited during SWRs (Borhegyi et al 2004; Viney et al 2013). In a recent testing of this hypothesis, Joshi et al (2017) found that in the mouse hippocampus, a type of septo-hippocampal GABAergic neuron, the Teevra cell, was phase-coupled to the trough of CA1 theta cycles and selectively innervated theta peak firing axo-axonic neurons, but surprisingly preferentially in the CA3 area
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