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

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.

ABSTRACT

Fast 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 (Ih ) 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.