Local-circuit neurones in the medial prefrontal cortex (areas 25, 32 and 24b) in the rat: Morphology and quantitative distribution

Abstract

This paper is a light microscopical study describing the detailed morphology and quantitative distribution of local circuit neurones in areas 25, 32, and 24b of the medial prefrontal cortex (mPFC) in the rat. Cortical interneurones were identified immunocytochemically by their expression of calretinin (CR), parvalbumin (PV), and calbindin D-28k (CB) immunoreactivity. Neurones immunoreactive for gamma-aminobutyric acid (GABA) were also investigated, as were interneurones containing reduced nicotinamide adenine dinucleotide phosphate (NADPH) diaphorase activity. Several distinct classes of CR+, PV+, and CB+ neurones were identified; the most frequent were: bipolar/bitufted CR+ cells in upper layer 3; multipolar PV+ neurones in layers 3 and 5; and bitufted/multipolar CB+ neurones in lower layer 3. CB+ neurones resembling Martinotti and neurogliaform cells were also present in layers 5/6. The morphologies and depth distributions of each cell type were consistent across the three areas of mPFC studied. Seven classes of diaphorase-reactive mPFC neurone are described; these cells were composed about 0.8% of the total neurone population and had a peak distribution located in mid- to lower layer 5 in each area. In areas 32 and 25, three defined bands of diffuse NADPH diaphorase staining were located in layer 2 and in upper and deep layer 5. Diaphorase reactivity was very infrequently colocalised with either CR, PV, or CB immunoreactivities. The numerical densities of neurones (N(V), number of cells per mm3) in each layer were calculated stereologically. The mean total neuronal N(V) estimate for areas 25, 32, and 24b was 51,603 +/- 3,324 (mean +/- S.D.; n = 8). Significant interareal differences were detected. From cortical thickness data and neuronal N(V) estimates, the absolute number of neurones under 1 mm2 of cortical surface (N(C)) have been derived. The mean N(C) value for areas 25, 32, and 24b was 57,328 +/- 7,505 neurones. In immunolabelled Nissl-stained sections, CR+ neurones constituted an overall 4.0%, PV+ cells 5.6%, and CB+ 3.4% of the total neurone populations in mPFC. GABA+ cells represented a mean of 16.2% (14.8-17.2%) of neurones in areas 25, 32 and 24b. The absolute numbers of CR+, PV+, CB+, and GABA+ neurones within individual layers in a column of cortex under 1 mm2 of cortical surface (N(L)) have also been derived, with significant interareal differences in N(L) values being detected. The data provide the structural basis for a qualitative and quantitative definition of local cortical circuits in the rat mPFC.

Systemic administration of the benzodiazepine receptor partial inverse agonist FG‐7142 disrupts corticolimbic network interactions

“…A paucity of recordings from interneurons in mPFC has been observed in other studies (Homayoun et al, 2005;Jackson et al, 2004;Laviolette et al, 2005) and is likely due to both anatomical and technical considerations. Anatomical studies indicate that the majority of neurons in mPFC are pyramidal cells (Gabbott et al, 1997). Furthermore, the large diameter (50 mm) metal electrodes used in the present study preferentially detect activity in larger pyramidal cells when compared with smaller interneurons (Snodderly, 1973).…”

“…However, it remains unclear why only the lowest dose of FG-7142 increased neuronal activity. However, it is possible that the distinct subtypes of GABA interneurons present in mPFC (Gabbott et al, 1997;Kawaguchi and Kondo, 2002;Kawaguchi and Kubota, 1997) and BLA (McDonald and Mascagni, 2001, 2002Muller et al, 2003; are involved in mediating this dose-related increase in unit firing. FG-7142 also elevates monoamine metabolism in mPFC and BLA (Bradberry et al, 1991;Dazzi et al, 2002;Ida et al, 1991) and evidence indicates that monoamines can attenuate unit firing rate in these regions (Mantz et al, 1988;Nakano et al, 1987;Rosenkranz and Grace, 1999;Sesack and Bunney, 1989).…”

GABAergic Neurons Immunoreactive for Calcium Binding Proteins are Reduced in the Prefrontal Cortex in Major Depression

“…These cells differ by morphology, type of contacts with pyramidal neurons, pattern of firing, and monoaminergic innervation. PV-IR interneurons correspond to basket or chandelier cells, make contacts on somata and axonal initial segments of pyramidal neurons and regulate cortical output activity (Baimbridge et al, 1992;Cauli et al, 1997;Conde et al, 1994;Cruz et al, 2003;DeFelipe, 1989DeFelipe, , 1997Gabbott et al, 1997;Lewis and Lund, 1990;Lund and Lewis, 1993;Somogyi et al, 1998). PV-IR neurons have physiological properties characteristic of fast-spiking interneurons Kubota, 1993, 1997;Zaitsev et al, 2005).…”

The Neurotensin Agonist PD149163 Increases Fos Expression in the Prefrontal Cortex of the Rat

“…GABAergic interneurons in the cortex can be divided into three largely non-overlapping classes based on expression of one of three calcium-binding proteins: parvalbumin (PV), calbindin (CB), or calretinin (CR) (DeFelipe, 1997;Gabbott et al, 1997;Rogers, 1992). In the present study, we assessed the effects of acute administration of the truncated peptide NT agonist, PD149163 (Feifel et al, , 1999Wustrow et al, 1995), on regional forebrain expression of Fos, a marker of neurons that are metabolically activated, with a particular focus on determining if the NT agonist activates prefrontal cortical GABAergic interneurons.…”