Excitatory and inhibitory neurons express c-Fos in barrel-related columns after exploration of a novel environment

Staiger, Jochen F.; Masanneck, Carmen; Bisler, S.; Schleicher, Axel; Zuschratter, Werner; Zilles, Karl

doi:10.1016/s0306-4522(01)00501-2

Cited by 88 publications

(61 citation statements)

References 61 publications

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“…2C). This excluded c-Fos as a marker of recruited microglial cells under sensory stimulation, as shown before for astrocytes (Staiger et al, 2002) and confirmed here by the lack of GFAP/ c-Fos double-labeled astrocytes (data not shown).…”

Section: Contralateral Barrel Cortex Activation By Vibrissal Stimulationsupporting

confidence: 88%

“…Notwithstanding the dominant labeling of pyramidal and spiny stellate cells (Filipkowski et al, 2000;Staiger et al, 2000Staiger et al, , 2002, our doubleimmunohistochemical data established that numerous recruited cells, located mainly in layers II/III, corresponded to COX-2 pyramidal cells. Consistent with the direct thalamic afferent input (Staiger et al, 1996b) of the overlapping populations of VIP-and ChAT-expressing GABA interneurons (Chédotal et al, 1994), we observed robust c-Fos induction in these cells throughout layers Figure 6.…”

Section: Identity Of the Cortical Neuronal Circuitry Recruited By Whimentioning

confidence: 53%

“…Wang et al, 2006), their activation cannot be probed by c-Fos induction (Staiger et al, 2002; this study). Consequently, we first explored their implication as cellular intermediary in neurovascular coupling (Carmignoto and Gó mez-Gonzalo, 2010) Stringer, 2004;Zielke et al, 2007) (Fig.…”

Section: Astroglial Messengers As Intermediaries For Both Inhibitory mentioning

confidence: 78%

“…Because c-Fos expression in PV and calbindin interneurons is induced by exploration of a novel environment (Bertini et al, 2002;Staiger et al, 2002), our experimental paradigm in pretrained and restrained or anesthetized rats may be unsuited for c-Fos upregulation in these interneurons (Staiger, 2006). Additionally, the lack of c-Fos in PV and SOM/NOS interneurons could result from their silencing by the inhibitory drive imposed by the recruited VIP cells that innervate both PV and calbindin interneurons (Staiger et al, 2004;Dávid et al, 2007) (Fig.…”

Section: Identity Of the Cortical Neuronal Circuitry Recruited By Whimentioning

confidence: 99%

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Pyramidal Neurons Are "Neurogenic Hubs" in the Neurovascular Coupling Response to Whisker Stimulation

Lecrux

Toussay

Kocharyan

et al. 2011

Journal of Neuroscience

150

165

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The whisker-to-barrel cortex is widely used to study neurovascular coupling, but the cellular basis that underlies the perfusion changes is still largely unknown. Here, we identified neurons recruited by whisker stimulation in the rat somatosensory cortex using double immunohistochemistry for c-Fos and markers of glutamatergic and GABAergic neurons, and investigated in vivo their contribution along with that of astrocytes in the evoked perfusion response. Whisker stimulation elicited cerebral blood flow (CBF) increases concomitantly with c-Fos upregulation in pyramidal cells that coexpressed cyclooxygenase-2 (COX-2) and GABA interneurons that coexpressed vasoactive intestinal polypeptide and/or choline acetyltransferase, but not somatostatin or parvalbumin. The evoked CBF response was decreased by blockade of NMDA (MK-801, Ϫ37%), group I metabotropic glutamate (MPEPϩLY367385, Ϫ40%), and GABA-A (picrotoxin, Ϫ31%) receptors, but not by GABA-B, VIP, or muscarinic receptor antagonism. Picrotoxin decreased stimulus-induced somatosensory evoked potentials and CBF responses. Combined blockade of GABA-A and NMDA receptors yielded an additive decreasing effect (Ϫ61%) of the evoked CBF compared with each antagonist alone, demonstrating cooperation of both excitatory and inhibitory systems in the hyperemic response. Blockade of prostanoid synthesis by inhibiting COX-2 (indomethacin, NS-398), expressed by ϳ40% of pyramidal cells but not by astrocytes, impaired the CBF response (Ϫ50%). The hyperemic response was also reduced (Ϫ40%) after inhibition of astroglial oxidative metabolism or epoxyeicosatrienoic acids synthesis. These results demonstrate that changes in pyramidal cell activity, sculpted by specific types of inhibitory GABA interneurons, drive the CBF response to whisker stimulation and, further, that metabolically active astrocytes are also required.

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Section: Contralateral Barrel Cortex Activation By Vibrissal Stimulationsupporting

confidence: 88%

Section: Identity Of the Cortical Neuronal Circuitry Recruited By Whimentioning

confidence: 53%

Section: Astroglial Messengers As Intermediaries For Both Inhibitory mentioning

confidence: 78%

Section: Identity Of the Cortical Neuronal Circuitry Recruited By Whimentioning

confidence: 99%

See 2 more Smart Citations

Pyramidal Neurons Are "Neurogenic Hubs" in the Neurovascular Coupling Response to Whisker Stimulation

Lecrux

Toussay

Kocharyan

et al. 2011

Journal of Neuroscience

150

165

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“…GAD, the synthesizing enzyme of GABA, is thought to be a reliable marker of GABAergic neurons (e.g., [22][23][24]. We correlated GAD67 antigenicity with staining against GABA by immunolabeling 50-μm-thick slices for NeuN, GABA, and GAD67 (Fig.…”

Section: Resultsmentioning

confidence: 99%

Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A

Meyer

Schwarz

Wimmer

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

208

170

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Although physiological data on microcircuits involving a few inhibitory neurons in the mammalian cerebral cortex are available, data on the quantitative relation between inhibition and excitation in cortical circuits involving thousands of neurons are largely missing. Because the distribution of neurons is very inhomogeneous in the cerebral cortex, it is critical to map all neurons in a given volume rather than to rely on sparse sampling methods. Here, we report the comprehensive mapping of interneurons (INs) in cortical columns of rat somatosensory cortex, immunolabeled for neuron-specific nuclear protein and glutamate decarboxylase. We found that a column contains ∼2,200 INs (11.5% of ∼19,000 neurons), almost a factor of 2 less than previously estimated. The density of GABAergic neurons was inhomogeneous between layers, with peaks in the upper third of L2/3 and in L5A. IN density therefore defines a distinct layer 2 in the sensory neocortex. In addition, immunohistochemical markers of IN subtypes were layer-specific. The "hot zones" of inhibition in L2 and L5A match the reported low stimulus-evoked spiking rates of excitatory neurons in these layers, suggesting that these inhibitory hot zones substantially suppress activity in the neocortex.F or a quantitative understanding of the interaction between excitatory and inhibitory synaptic transmission in the neocortex, it is crucial to obtain data on the absolute numbers and the relative distribution of excitatory and inhibitory (mostly GABAergic) neurons [interneurons (INs)] in a cortical column. Only on the basis of such prevalence numbers is it possible to interpret data on single-cell physiology (1-8) and synaptic connections of pairs of neurons (9-12) at the circuit level. The distribution of cortical neurons and INs has therefore been the objective of several studies over the past decades (13-15). Statistical sampling methods were used because mapping tens of thousands of neurons was not feasible. Although the nominal error bounds of such methods are in the range of 10-20%, the reported absolute numbers differed strongly among studies, especially for sparse neuron populations, such as INs and their subtypes. The ratio of INs reported for the somatosensory cortex varied between 15% and 25%, thus by almost a factor of 2 (13,16,17). Data on possible differences in IN density between layers in a cortical column were contradictory (13,15,16,18,19).To resolve these substantial discrepancies, we undertook the complete mapping of INs in entire cortical columns using the cytoarchitectonic barrels in L4 as a reference frame for the thalamocortical innervation volume (20) in postnatal day (P) 25-36 rat vibrissal cortex. Our data show that the overall prevalence of inhibitory neurons was previously overestimated by almost a factor of 2. We find a unique substructure of the distribution of INs in a cortical column that can explain the layer-specific differences in the excitability in neocortex. The distribution of INs defines layer 2 as a distinct neocortical layer.

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Cortical and brainstem neurons containing calcium‐binding proteins in a murine model of Duchenne's muscular dystrophy: Selective changes in the sensorimotor cortex

Carretta

Santarelli²,

Vanni

et al. 2002

J of Comparative Neurology

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In the muscular dystrophic (mdx) mouse, which is characterized by deficient dystrophin expression and provides a model of Duchenne's muscular dystrophy, we previously demonstrated marked central nervous system alterations and in particular a quantitative reduction of corticospinal and rubrospinal neurons and pathologic changes of these cells. Prompted by these findings and in view of the relations between calcium ions and dystrophin, we analyzed with immunohistochemistry the neurons containing the calcium-binding proteins parvalbumin, calbindin D28k, and calretinin in cortical areas and brainstem nuclei of mdx mice. In the sensorimotor cortex, parvalbumin-positive and calbindin-positive neurons, which represent a subset of cortical interneurons, were significantly more numerous in mdx mice than in wild-type ones. In addition, the laminar distribution of parvalbumin-positive neurons in the motor and somatosensory cortical areas of mdx mice was altered with respect to wild-type animals. No alterations in the number and distribution were found in the parvalbumin- or calbindin-expressing cell populations of the visual and anterior cingulate cortices of mdx mice. The pattern of calretinin immunoreactivity was normal in all investigated cortical areas. The cell populations containing either calcium-binding protein were similar in brainstem nuclei of mdx and wild-type mice. The present findings demonstrated selective changes of subsets of interneurons in the motor and somatosensory cortical areas of mdx mice. Therefore, the data showed that, in the cortices of these mutant animals, the previously demonstrated pathologic changes of corticospinal cell populations are accompanied by marked alterations in the local circuitry.

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Excitatory and inhibitory neurons express c-Fos in barrel-related columns after exploration of a novel environment

Cited by 88 publications

References 61 publications

Pyramidal Neurons Are "Neurogenic Hubs" in the Neurovascular Coupling Response to Whisker Stimulation

Pyramidal Neurons Are "Neurogenic Hubs" in the Neurovascular Coupling Response to Whisker Stimulation

Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A

Cortical and brainstem neurons containing calcium‐binding proteins in a murine model of Duchenne's muscular dystrophy: Selective changes in the sensorimotor cortex

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