Heterogeneity of chandelier neurons in monkey neocortex: Corticotropin‐releasing factor‐and parvalbumin‐immunoreactive populations

Abstract

Chandelier neurons are a unique subclass of cortical nonpyramidal neurons. The axons of these neurons terminate in distinctive vertically arrayed cartridges that synapse on the axon initial segment of pyramidal neurons. In this study, the rapid Golgi method and immunohistochemical techniques were used to characterize the morphology, regional distribution, laminar location, and biochemical content of chandelier neurons in the prefrontal and occipital cortices of three monkey species. As in our previous studies of visual areas V1 and V2 (Lund: Journal of Comparative Neurology 257:60-92, 1987; Lund et al.: Journal of Comparative Neurology 202:19-45, 1981, 276:1-29, 1988), Golgi impregnations of areas 46 and 9 of macaque prefrontal cortex show chandelier neurons to be present in layers 2 through superficial 5. The vertical arrays of terminal boutons (axon cartridges) typical of this neuron class are also present in layers 2-6 of the prefrontal cortex, but are not found in layer 1 or the subcortical white matter. In immunohistochemical studies, a calcium-binding protein, parvalbumin, and a neuropeptide, corticotropin-releasing factor (CRF), identify rod-like structures that are morphologically similar to the axon cartridges of chandelier neurons seen in the Golgi material. In addition, both parvalbumin- and CRF-immunoreactive cartridges are located below the somata of unlabeled pyramidal neurons and appear to outline the axon initial segment of these neurons. However, we find that parvalbumin and CRF are present in only subpopulations of chandelier axon cartridges. For example, in adult primary visual cortex, parvalbumin-labeled cartridges are present in very low numbers only in layers 2-3, whereas in prefrontal and occipital association cortices these cartridges are a very prominent component of layers 2-superficial 3 and are present in much lower density in the deeper cortical layers. In contrast to these findings in adult macaque monkeys, prefrontal and occipital association cortices of infant macaque monkeys contain a very high density of parvalbumin-labeled cartridges in layer 4 and relatively few in the superficial cortical layers. Furthermore, in adult squirrel monkey prefrontal cortex, CRF-labeled cartridges are predominately present in layer 4, but these CRF-immunoreactive structures have not been observed in the homologous regions of infant or adult macaque monkeys. These findings indicate that even for neurons of such distinctive morphology and presumably constant functional role as chandelier neurons, factors such as regional and laminar location, age, and primate species are associated with differences in the biochemical content of subpopulations of these neurons.

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).…”

A subclass of prefrontal γ-aminobutyric acid axon terminals are selectively altered in schizophrenia

“…Such a change would certainly contribute to the substantial alterations in activity within the PFC and in interconnected cortical and subcortical regions (36,37) that are thought to account for the cognitive abnormalities characteristic of schizophrenia (38,39). In addition, parvalbumin-containing cortical neurons, which include chandelier cells (21,27), have been shown to be synaptic targets of dopamine axons (40) and to express dopamine D4 receptors (41). These neurons also receive input from serotonin-containing axons (42).…”

Parvalbumin deficiency affects network properties resulting in increased susceptibility to epileptic seizures

“…control of pyramidal cell excitability (Blümcke et al, 1990;Cauli et al, 1997;DeFelipe et al, 1989DeFelipe et al, , 1993Hendrickson et al, 1991;Hendry et al, 1989;Lewis and Lund, 1990). Thus, it is expected that any alteration in the functional properties of the PVir interneurones will modify local inhibition, which eventually may affect the collective activity of the whole neuronal network.…”