Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm

Abstract

SUMMARY Although it has been tacitly assumed that the hippocampus exerts an influence on neocortical networks, the mechanisms of this process are not well understood. We examined whether and how hippocampal theta oscillations affect neocortical assembly patterns by recording populations of single cells and transient gamma oscillations in multiple cortical regions, including the somatosensory area and prefrontal cortex in behaving rats and mice. Laminar analysis of neocortical gamma bursts revealed multiple gamma oscillators of varying frequency and location, which were spatially confined and synchronized local groups of neurons. A significant fraction of putative pyramidal cells and interneurons as well as localized gamma oscillations in all recorded neocortical areas were phase-biased by the hippocampal theta rhythm. We hypothesize that temporal coordination of neocortical gamma oscillators by hippocampal theta is a mechanism by which information contained in spatially widespread neocortical assemblies can be synchronously transferred to the associative networks of the hippocampus.

Chronic deep brain stimulation of the rat ventral medial prefrontal cortex disrupts hippocampal–prefrontal coherence

“…VH-IL coherence in both treatment groups was strongest within the 6 to 10 Hz theta frequency band. These data are consistent with previous examinations of communication between the medial prefrontal cortex and hippocampus of rodents (Siapas et al, 2005;Wilson, 2005a, 2005b;Hyman et al, 2005Hyman et al, , 2010Sirota et al, 2008;Hartwich et al, 2009;Young and McNaughton, 2009;Adhikari et al, 2010;Benchenane et al, 2010; also reviewed by Colgin, 2011). Most research in this area has looked at neural activity correlations between the dorsal hippocampus and the prelimbic cortex, located just dorsal to the IL, and patterns have been linked to cognitive variables such as working memory (Jones and Wilson, 2005b;Hyman et al, 2005) and expectation-based decision-making (Benchenane et al, 2010).…”

Gamma band directional interactions between basal forebrain and visual cortex during wake and sleep states

“…Our results are based on LFP recordings, whose biophysical origin continues to be debated (Sirota et al, 2008;Berens et al, 2008;Katzner et al, 2009;Xing et al, 2009;Kajikawa and Schroeder, 2011;Rainer, 2014). In our view, the LFP is an aggregate signal that is influenced by both super and subthreshold synaptic activations due to local recurrent processing, inputs from distant axonal sources (Nielsen et al, 2006;Rainer, 2008), as well as ephaptic coupling (Anastassiou et al, 2011) and non-synaptic sources due to volume-transmitted neuromodulators or gap junctions.…”

“…Convergent evidence suggests that higher frequency oscillations in the beta and gamma range tend to reflect local synchronized firing and are not passively propagated over large distances (Steriade and Amzica, 1996;Buzsáki and Wang, 2012;Welle and Contreras, 2016). Low frequency LFP modulations in delta, theta and alpha bands however need to be interpreted with particular caution, given the robust, large amplitude, and highly synchronized theta oscillations that are present in the hippocampus that have been shown to affect cortical LFP recordings particularly in the rat where these structures are in close proximity (Buzsáki, 2002;Sirota et al, 2008). For this reason, we focus our analyses and interpretation largely on beta and gamma band activity here.…”

“…In both BF and VC, we observed delta activity during SWS as well as theta activity during REM and wakefulness. LFP activity at these low frequencies is subject to potential contamination by volume conduction, such as for example from the hippocampus (Buzsáki, 2002;Sirota et al, 2008). We therefore do not proceed to perform a detailed analysis of these effects here, but show the spectra for illustrative purposes only.…”

Resolving the neural circuits of anxiety

“…This rhythm is thought to be driven by brainstem nuclei via projections through the medial septum 130 , and is universally reduced by anxiolytic drugs 131 . This HPC theta rhythm has been shown to entrain both single unit activity in pyramidal cells and interneurons of the PFC, as well as PFC gamma band activity 132 . Synchronization of PFC activity to the HPC theta rhythm has been observed within anxiety assays; in the threatening zones of the EPM and OFT (open arms and center, respectively), theta activity has been observed in the mPFC which is entrained to vHPC theta 129 .…”