Abstract
The long-range coupling within prefrontal-hippocampal networks that account for cognitive performance emerges early in life. The discontinuous hippocampal theta bursts have been proposed to drive the generation of neonatal prefrontal oscillations, yet the cellular substrate of these early interactions is still unresolved. Here, we selectively target optogenetic manipulation of glutamatergic projection neurons in the CA1 area of either dorsal or intermediate/ventral hippocampus at neonatal age to elucidate their contribution to the emergence of prefrontal oscillatory entrainment. We show that despite stronger theta and ripples power in dorsal hippocampus, the prefrontal cortex is mainly coupled with intermediate/ventral hippocampus by phase-locking of neuronal firing via dense direct axonal projections. Theta band-confined activation by light of pyramidal neurons in intermediate/ventral but not dorsal CA1 that were transfected by in utero electroporation with high-efficiency channelrhodopsin boosts prefrontal oscillations. Our data causally elucidate the cellular origin of the long-range coupling in the developing brain.
Highlights
In the adult rodent brain, coordinated patterns of oscillatory activity code in a frequency-specific manner for sensory and cognitive performance
While different organization and function of dHP vs. i/vHP of adults have been extensively characterized (Thompson et al, 2008; Dong et al, 2009; Patel et al, 2013), their patterns of structural and functional maturation are still poorly understood. To fill this knowledge gap, we firstly examined the network oscillatory and firing activity of CA1 area of either dHP or i/vHP by performing extracellular recordings of the local field potential (LFP) and multiple unit activity (MUA) in neonatal [postnatal day (P) 8–10] non-anesthetized and urethane-anesthetized mice (n = 153)
While urethane anesthesia led to an overall decrease of amplitude and power of oscillatory activity when compared to the nonanesthetized state of the same group of pups, the firing rate and timing as well as the synchrony and interactions within prefrontal-hippocampal networks were similar during both states (Figure 1— figure supplement 1)
Summary
In the adult rodent brain, coordinated patterns of oscillatory activity code in a frequency-specific manner for sensory and cognitive performance. Learning and memory critically depend on oscillations within theta frequency band (4–12 Hz) that functionally couple the medial prefrontal cortex (PFC) and hippocampus (HP) (Siapas and Wilson, 1998; Benchenane et al, 2010; Brincat and Miller, 2015; Backus et al, 2016; Eichenbaum, 2017; Wirt and Hyman, 2017). These frequency-tuned brain states are present already during early development, long before the memory and attentional abilities have fully matured. It is accompanied by slow delta waves as well as by faster discharges (beta and gamma oscillations) that account for local activation of circuits (Brockmann et al, 2011; Yang et al, 2016)
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
