Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin

Kawaguchi, Yasuo; Katsumaru, Hironobu; Kosaka, Toshio; Heizmann, Claus W.; Hama, Kiyoshi

doi:10.1016/0006-8993(87)90921-8

Cited by 465 publications

(222 citation statements)

References 19 publications

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“…The precise mechanism of the increased excitability of FS cells by CBD is unknown; it could be hypothesized that CBD interacts with the membrane leak channels altering the membrane permeability to sodium ions, or perhaps CBD directly modulates the calcium buffering capacity of PV within FS cells changing the rate of firing. The FS cells typically innervate the soma and dendrites of pyramidal cells (Kawaguchi et al, 1987; Freund and Buzsaki, 1996) and therefore are able to directly inhibit excessive excitatory discharge of pyramidal cells, enabling them to efficiently entrain and synchronize neuronal networks. The effect of CBD resulting in an enhanced neuronal discharge of FS cells will be a favoured outcome in epilespy as a direct increase of inhibitory effects which may contribute towards the supression of the disease progression.…”

Section: Discussionmentioning

confidence: 99%

Cannabidiol exerts antiepileptic effects by restoring hippocampal interneuron functions in a temporal lobe epilepsy model

Khan

Shekh‐Ahmad²,

Khalil³

et al. 2018

British J Pharmacology

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Background and PurposeA non‐psychoactive phytocannabinoid, cannabidiol (CBD), shows promising results as an effective potential antiepileptic drug in some forms of refractory epilepsy. To elucidate the mechanisms by which CBD exerts its anti‐seizure effects, we investigated its effects at synaptic connections and on the intrinsic membrane properties of hippocampal CA1 pyramidal cells and two major inhibitory interneurons: fast spiking, parvalbumin (PV)‐expressing and adapting, cholecystokinin (CCK)‐expressing interneurons. We also investigated whether in vivo treatment with CBD altered the fate of CCK and PV interneurons using immunohistochemistry.Experimental ApproachElectrophysiological intracellular whole‐cell recordings combined with neuroanatomy were performed in acute brain slices of rat temporal lobe epilepsy in in vivo (induced by kainic acid) and in vitro (induced by Mg2+‐free solution) epileptic seizure models. For immunohistochemistry experiments, CBD was administered in vivo (100 mg·kg−1) at zero time and 90 min post status epilepticus, induced with kainic acid.Key ResultsBath application of CBD (10 μM) dampened excitability at unitary synapses between pyramidal cells but enhanced inhibitory synaptic potentials elicited by fast spiking and adapting interneurons at postsynaptic pyramidal cells. Furthermore, CBD restored impaired membrane excitability of PV, CCK and pyramidal cells in a cell type‐specific manner. These neuroprotective effects of CBD were corroborated by immunohistochemistry experiments that revealed a significant reduction in atrophy and death of PV‐ and CCK‐expressing interneurons after CBD treatment.Conclusions and ImplicationsOur data suggest that CBD restores excitability and morphological impairments in epileptic models to pre‐epilepsy control levels through multiple mechanisms to reinstate normal network function.

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Section: Discussionmentioning

confidence: 99%

Cannabidiol exerts antiepileptic effects by restoring hippocampal interneuron functions in a temporal lobe epilepsy model

Khan

Shekh‐Ahmad²,

Khalil³

et al. 2018

British J Pharmacology

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“…CBPs accordingly can also shape discharge patterns and in their absence or paucity permit phasic discharge by neurons (Li et al, 1995). Throughout the forebrain, Parv ϩ neurons are commonly fast spiking cells, as evident from in vitro and in vivo recording studies of identified neurons (Celio, 1986;Kawaguchi et al, 1987;Kawaguchi, 1993;Kawaguchi and Kubota, 1993;Sik et al, 1995). In the medial septumdiagonal band, Parv ϩ cells have been found to be fast spiking by in vitro recordings (Morris et al, 1999) and in the BF (in one cell) by in vivo recordings (Duque et al, 2000).…”

Section: Functional Significance Of Cbp Content In Bf Cell Groupsmentioning

confidence: 98%

“…In the hippocampus and neocortex, neurons containing the CBPs, which are commonly GABAergic interneurons, have been distinguished in their electrophysiologic properties from those lacking CBPs, i.e., the pyramidal neurons, by their frequently continuous and fast spiking discharge (Celio, 1986;Kawaguchi et al, 1987;Kawaguchi and Hama, 1988;Kawaguchi and Kubota, 1993;Freund and Buzsaki, 1996). Indeed, the CBPs serve to buffer Ca 2ϩ and accordingly prevent Ca 2ϩ -activated K ϩ currents from hyperpolarizing the membrane and inhibiting spike generation (Baimbridge et al, 1992).…”

Section: Functional Significance Of Cbp Content In Bf Cell Groupsmentioning

confidence: 99%

Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat

Gritti

Manns

Mainville

et al. 2003

J of Comparative Neurology

178

197

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The basal forebrain (BF) plays an important role in modulating cortical activity and facilitating processes of attention, learning, and memory. This role is subserved by cholinergic neurons but also requires the participation of other noncholinergic neurons. Noncholinergic neurons include ␥-amino butyric acidergic (GABAergic) neurons, some of which project in parallel with the cholinergic cells to the cerebral cortex, others of which project caudally or locally. With the original aim of distinguishing different subgroups of GABAergic neurons, we examined immunostaining for the calcium binding proteins (CBPs) parvalbumin (Parv), calbindin (Calb), and calretinin (Calret) in the rat. Although the CBP ϩ cell groups were distributed in a coextensive manner with the GABAergic cells, they were collectively more numerous. Of cells retrogradely labeled with cholera toxin (CT) from the prefrontal or parietal cortex, Parv ϩ and Calb ϩ cells, but not Calret ϩ cells, represented substantial proportions (ϳ35-45% each) that collectively were greater than that of GABAergic projection neurons. From dual immunostaining for the CBPs and glutamic acid decarboxylase (GAD), it appeared that the vast majority (Ͼ90%) of the Parv ϩ group was GAD ϩ , whereas only a small minority (Ͻ10%) of the Calb ϩ or Calret ϩ group was GAD ϩ . Significant proportions of Calb ϩ (Ͼ40%) and Calret ϩ (Ͼ80%) neurons were immunopositive for phosphate-activated glutaminase, the synthetic enzyme for transmitter glutamate. The results suggested that, whereas Calret ϩ cells predominantly comprise caudally or locally projecting, possibly glutamatergic BF neurons, Parv ϩ cells likely comprise the cortically projecting GABAergic BF neurons and Calb ϩ cells the cortically projecting, possibly glutamatergic BF neurons that would collectively participate with the cholinergic cells in the modulation of cortical activity.

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“…Apart from being excellent markers of subpopulations of non-pyramidal neurons, their presence has been correlated with a variety of functions, all connected with intracellular calciun buffering and mobilization (Blaustein, 1988;Bairnbridge et al, 1992). A strong correlation has been demonstrated between the occurrence of Parv and the fast firing properties of hippocampal interneurons (Kawaguchi et al, 1987). Recently, the distribution of Calb DZsK has been found to overlap with that of P-type calcium channels (Hillman et al,199 1).…”

Section: Models Of Cell Lineage Compatible With These Observationsmentioning

confidence: 99%

Lineage analysis reveals neurotransmitter (GABA or glutamate) but not calcium-binding protein homogeneity in clonally related cortical neurons

et al. 1994

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Studies of cell lineage in the rat cerebral cortex have provided new insights into the mechanisms of neuronal and glial determination. They have shown that clonally related cells, marked with retrovirus injection at embryonic day 16 (E16), express the same glial or neuronal phenotype, suggesting that separate progenitors for each of these cell phenotypes exist in the ventricular zone at that stage of corticogenesis. However, it is not known if such committed progenitors are present in the ventricular zone before E16. Another important question concerns which neurochemical features are shared by clonally related cells of the adult cerebral cortex. In this study we have addressed the first question by injecting a retroviral vector expressing beta-galactosidase into the telencephalic ventricles of rat embryos at different stages (E14-E19). In order to classify clonally related neurons in the cerebral cortex of these rats, we have used postembedding immunohistochemistry for the amino acid neurotransmitters glutamate, aspartate, and GABA. Glutamate and GABA immunoreactivity marked nonoverlapping populations of cells that corresponded to the pyramidal and nonpyramidal neuron types of the rat cerebral cortex. Clonally related neurons, marked by retrovirus injection at any day between E14 and E19, homogeneously expressed one or other phenotype and accordingly displayed glutamate or GABA immunoreactivity. This finding indicates that committed progenitor cells for pyramidal and nonpyramidal neurons are present in the ventricular zone before E16. To investigate whether lineage dictates other features in clonally related neurons, we performed an immunohistochemical analysis for the calcium- binding proteins calbindin, parvalbumin, and calretinin in clusters of clonally related nonpyramidal neurons. The same calcium-binding protein was rarely found in members of the same cluster, suggesting that lineage does not control the expression of calcium-binding proteins in cortical nonpyramidal neurons. As a result of examining a large number of clonally related neurons from brains injected at different ages, we observed remarkable differences in number and laminar distribution of pyramidal and nonpyramidal neurons marked with retrovirus. Clusters of nonpyramidal neurons were usually composed of two or three cells, and resided in the cortical layers that were just being generated at the time of injection. Clusters of pyramidal neurons were larger and dispersed in several layers in the earlier injections; their size and laminar distribution were progressively reduced for later injections. These observations suggest the existence of different mechanisms that generate the pyramidal and nonpyramidal neurons of the cerebral cortex.

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Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin

Cited by 465 publications

References 19 publications

Cannabidiol exerts antiepileptic effects by restoring hippocampal interneuron functions in a temporal lobe epilepsy model

Cannabidiol exerts antiepileptic effects by restoring hippocampal interneuron functions in a temporal lobe epilepsy model

Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat

Lineage analysis reveals neurotransmitter (GABA or glutamate) but not calcium-binding protein homogeneity in clonally related cortical neurons

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