Subregional differences in the generation of fast network oscillations in the rat medial prefrontal cortex (mPFC) in vitro

Abstract

Key points Fast network oscillations in the beta (20–30 Hz) frequency range can be evoked with combined activation of muscarinic and kainate receptors in different subregions of the medial prefrontal cortex (mPFC). Subregional differences were observed as the oscillations in the dorsal prelimbic cortex (PrL) were smaller in magnitude than those in the ventral dorsopeduncular (DP) region, and these differences persisted in trimmed slices containing only PrL and DP regions.Oscillations in both regions were dependent upon GABAA and AMPA receptor activation but NMDA receptor blockade decreased oscillations only in the DP region.Subregional differences in neuronal properties of the presumed pyramidal cells were found between PrL and DP, with many more cells in DP firing rhythmically compared to the PrL region.Presumed inhibitory synaptic potentials (IPSPs) recorded from principal cells were more rhythmic and coherent, and significantly larger in amplitude, in the DP region; the data suggest that variation in the patterns of activity between subregions may reflect distinct functional roles. AbstractFast network oscillations in the beta (20–30 Hz) and low gamma (30–80 Hz) range underlie higher cognitive functions associated with the medial prefrontal cortex (mPFC) including attention and working memory. Using a combination of kainate (KA, 200 nm) and the cholinergic agonist carbachol (Cb, 10 μm) fast network oscillations, in the beta frequency range, were evoked in the rat mPFC in vitro. Oscillations were elicited in the prelimbic (PrL), infralimbic (IL) and the dorsopeduncular (DP) cortex, with the largest oscillations observed in DP cortex. Oscillations in both the PrL and DP were dependent, with slightly different sensitivities, on γ‐aminobutyric acid (GABA)A, α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazolepropionic acid (AMPA) and kainate receptors, but only oscillations in the DP were significantly reduced by N‐methyl‐d‐aspartate (NMDA) receptor blockade. Intracellular recordings showed that 9/20 regular spiking (RS) cells in the PrL exhibited a notable cAMP‐dependent hyperpolarisation activated current (I h) in contrast to 16/17 in the DP cortex. Extracellular single unit recordings showed that the majority of cells in the PrL, and DP regions had interspike firing frequencies (IFFs) at beta (20–30 Hz) frequencies and fired at the peak negativity of the field oscillation. Recordings in DP revealed presumed inhibitory postsynaptic potentials (IPSPs) that were larger in amplitude and more rhythmic than those in the PrL region. Our data suggest that each PFC subregion may be capable of generating distinct patterns of network activity with different cell types involved. Variation in the properties of oscillations evoked in the PrL and DP probably reflects the distinct functional roles of these different PFC regions.

Social defeat stress causes selective attenuation of neuronal activity in the ventromedial prefrontal cortex

“…Furthermore, some striking differences between the PL and IL regions may explain why the vmPFC but not the dmPFC generates apparent 20–40 Hz events: (1) the lamination in layer 2 and layer 3 is less clear in the IL region 44,45 ; (2) the neuronal density of the IL region is lower than that of the PL region 44,45 ; (3) the proportions of interneuron subtypes, including CCK-GABA and PV-GABA cells, differ in these two subregions 46 ; and (4) the IL region receives stronger inputs from subcortical areas and the hippocampus 8 . In addition, previous studies using in vitro slice preparations have demonstrated that kainite-induced fast network oscillations with a frequency of 15–30 Hz in the IL and DP regions occurred with higher power than those observed in the PL region 47,48 , consistent with our results showing that the vmPFC possesses the ability to generate oscillations at this frequency range. Future investigations should extend this work to assess the functional roles of vmPFC 20–40 Hz events.…”

Hetereogeneity in Neuronal Intrinsic Properties: A Possible Mechanism for Hub-Like Properties of the Rat Anterior Cingulate Cortex during Network Activity

“…We recorded from 61 cells in the ACC in the presence of excitatory transmitter blockers (see Methods) and found a wide variety of IPs, as has been previously reported in the prelimbic and infralimbic regions of the PFC ( Yang et al, 1996 ; Dembrow et al, 2010 ; Gee et al, 2012 ; van Aerde and Feldmeyer, 2015 ; Glykos et al, 2015 ).…”

“…Neurons recorded in this study could be subjectively divided into five broad groups similar to those described in other PFC regions ( Yang et al, 1996 ; Dembrow et al, 2010 ; Gee et al, 2012 ; Lee et al, 2014 ; Glykos et al, 2015 ; van Aerde and Feldmeyer, 2015 ). However, using a range of established clustering algorithms that have been used successfully in other cortical areas to identify distinct neuronal clusters based on electrophysiological properties ( Sosulina et al, 2006 ; Keshavarzi et al, 2014 ; Ferrante et al, 2016 ), we did not identify distinct clusters.…”

Cell-Type Specific Development of the Hyperpolarization-Activated Current, Ih, in Prefrontal Cortical Neurons

“…Ih plays essential roles in regulating neuronal properties, synaptic integration and plasticity, and synchronous activity among neurons in the brain (Huang et al, 2011 ; He et al, 2014 ; Engel and Seutin, 2015 ; Gasselin et al, 2015 ; Masi et al, 2015 ). Ih also contributes to regulating the neuronal excitability and synaptic activities of both pyramidal neurons and GABAergic interneurons by maintaining the resting membrane potential (RMP) and after-hyperpolarization potential (AHP; Aponte et al, 2006 ; Bonin et al, 2013 ; Glykos et al, 2015 ). Ih has distinct regionally specific developmental patterns.…”