Inhibitory Interneuron Classes Express Complementary AMPA-Receptor Patterns in Macaque Primary Visual Cortex

Kooijmans, Roxana N; Self, Matthew W.; Wouterlood, Floris G.; Beliën, Jeroen A.M.; Roelfsema, Pieter R.

doi:10.1523/jneurosci.3188-13.2014

Cited by 20 publications

(27 citation statements)

References 60 publications

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“…Although many AMPA and NMDA receptors are localized at thalamo-cortical and cortico-cortical synapses, the co-localization of these receptors with interneurons is of special importance for the analysis of local signal processing within cortical microcircuits and layers. The co-localization of AMPA and NMDA receptor subunits with calcium binding protein expressing inhibitory interneurons was immunohistochemically studied in macaque primary visual cortex (Kooijmans et al, 2014 ; Kooijmans, 2016 ). The co-localizations of parvalbumin with GluA1 or GluA4 AMPA receptor subunits in the fast spiking chandelier and basket cells was found to be minor, in contrast to a higher co-localization of parvalbumin and GluA2 or GluA3.…”

Section: Discussionmentioning

confidence: 99%

Multiple Transmitter Receptors in Regions and Layers of the Human Cerebral Cortex

2017

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We measured the densities (fmol/mg protein) of 15 different receptors of various transmitter systems in the supragranular, granular and infragranular strata of 44 areas of visual, somatosensory, auditory and multimodal association systems of the human cerebral cortex. Receptor densities were obtained after labeling of the receptors using quantitative in vitro receptor autoradiography in human postmortem brains. The mean density of each receptor type over all cortical layers and of each of the three major strata varies between cortical regions. In a single cortical area, the multi-receptor fingerprints of its strata (i.e., polar plots, each visualizing the densities of multiple different receptor types in supragranular, granular or infragranular layers of the same cortical area) differ in shape and size indicating regional and laminar specific balances between the receptors. Furthermore, the three strata are clearly segregated into well definable clusters by their receptor fingerprints. Fingerprints of different cortical areas systematically vary between functional networks, and with the hierarchical levels within sensory systems. Primary sensory areas are clearly separated from all other cortical areas particularly by their very high muscarinic M2 and nicotinic α4β2 receptor densities, and to a lesser degree also by noradrenergic α2 and serotonergic 5-HT2 receptors. Early visual areas of the dorsal and ventral streams are segregated by their multi-receptor fingerprints. The results are discussed on the background of functional segregation, cortical hierarchies, microstructural types, and the horizontal (layers) and vertical (columns) organization in the cerebral cortex. We conclude that a cortical column is composed of segments, which can be assigned to the cortical strata. The segments differ by their patterns of multi-receptor balances, indicating different layer-specific signal processing mechanisms. Additionally, the differences between the strata-and area-specific fingerprints of the 44 areas reflect the segregation of the cerebral cortex into functionally and topographically definable groups of cortical areas (visual, auditory, somatosensory, limbic, motor), and reveals their hierarchical position (primary and unimodal (early) sensory to higher sensory and finally to multimodal association areas).Highlights Densities of transmitter receptors vary between areas of human cerebral cortex.Multi-receptor fingerprints segregate cortical layers.The densities of all examined receptor types together reach highest values in the supragranular stratum of all areas.The lowest values are found in the infragranular stratum.Multi-receptor fingerprints of entire areas and their layers segregate functional systemsCortical types (primary sensory, motor, multimodal association) differ in their receptor fingerprints.

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Section: Discussionmentioning

confidence: 99%

Multiple Transmitter Receptors in Regions and Layers of the Human Cerebral Cortex

2017

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“…In an immunolabelling study of monkey visual cortex (Kooijmans et al . ), Pvalb‐positive INs were reported to label strongly for both GluA2 and GluA3, whereas Sst‐positive INs showed little or no GluA2 labelling (Kooijmans et al . ).…”

Section: Discussionmentioning

confidence: 99%

“…), Pvalb‐positive INs were reported to label strongly for both GluA2 and GluA3, whereas Sst‐positive INs showed little or no GluA2 labelling (Kooijmans et al . ). This is the opposite to the findings of the present study obtained in the mouse.…”

Section: Discussionmentioning

confidence: 99%

Synapse‐specific expression of calcium‐permeable AMPA receptors in neocortical layer 5

Lalanne

Oyrer

Mancino

et al. 2015

The Journal of Physiology

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Key points In the hippocampus, calcium‐permeable AMPA receptors have been found in a restricted subset of neuronal types that inhibit other neurons, although their localization in the neocortex is less well understood.In the present study, we looked for calcium‐permeable AMPA receptors in two distinct populations of neocortical inhibitory neurons: basket cells and Martinotti cells. We found them in the former but not in the latter. Furthermore, in basket cells, these receptors were associated with particularly fast responses.Computer modelling predicted (and experiments verified) that fast calcium‐permeable AMPA receptors enable basket cells to respond rapidly, such that they promptly inhibit neighbouring cells and shut down activity.The results obtained in the present study help our understanding of pathologies such as stroke and epilepsy that have been associated with disordered regulation of calcium‐permeable AMPA receptors. AbstractAMPA‐type glutamate receptors (AMPARs) lacking an edited GluA2 subunit are calcium‐permeable (CP) and contribute to synaptic plasticity in several hippocampal interneuron types, although their precise role in the neocortex is not well described. We explored the presence of CP‐AMPARs at pyramidal cell (PC) inputs to Martinotti cells (MCs) and basket cells (BCs) in layer 5 of the developing mouse visual cortex (postnatal days 12–21). GluA2 immunolabelling was stronger in MCs than in BCs. A differential presence of CP‐AMPARs at PC‐BC and PC‐MC synapses was confirmed electrophysiologically, based on measures of spermine‐dependent rectification and CP‐AMPAR blockade by 1‐naphtyl acetyl spermine using recordings from synaptically connected cell pairs, NPEC‐AMPA uncaging and miniature current recordings. In addition, CP‐AMPAR expression in BCs was correlated with rapidly decaying synaptic currents. Computer modelling predicted that this reduces spike latencies and sharpens suprathreshold responses in BCs, which we verified experimentally using the dynamic clamp technique. Thus, the synapse‐specific expression of CP‐AMPARs may critically influence both plasticity and information processing in neocortical microcircuits.

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“…Vickers et al () find that 32% of the PARV‐positive cells and 28% of the CALB‐positive cells contain GluA2/3. However, a recent report indicated that the fast‐spiking PARV‐containing interneurons in monkey cortex express mainly GluA2/GluA3 and little GluA1/GluA4 (Kooijmans et al, ). The reason for this discrepancy from earlier studies is not known, and with regard to physiology thalamic afferents activate PARV neurons via GluA2‐lacking calcium‐permeable receptors to evoke a fail‐safe feedforward inhibition.…”

Section: Discussionmentioning

confidence: 99%

Ionotropic glutamate receptors: Which ones, when, and where in the mammalian neocortex

Hadžić

Jack

Wahle

2016

J of Comparative Neurology

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A multitude of 18 iGluR receptor subunits, many of which are diversified by splicing and RNA editing, localize to >20 excitatory and inhibitory neocortical neuron types defined by physiology, morphology, and transcriptome in addition to various types of glial, endothelial, and blood cells. Here we have compiled the published expression of iGluR subunits in the areas and cell types of developing and adult cortex of rat, mouse, carnivore, bovine, monkey, and human as determined with antibody- and mRNA-based techniques. iGluRs are differentially expressed in the cortical areas and in the species, and all have a unique developmental pattern. Differences are quantitative rather than a mere absence/presence of expression. iGluR are too ubiquitously expressed and of limited use as markers for areas or layers. A focus has been the iGluR profile of cortical interneuron types. For instance, GluK1 and GluN3A are enriched in, but not specific for, interneurons; moreover, the interneurons expressing these subunits belong to different types. Adressing the types is still a major hurdle because type-specific markers are lacking, and the frequently used neuropeptide/CaBP signatures are subject to regulation by age and activity and vary as well between species and areas. RNA-seq reveals almost all subunits in the two morphofunctionally characterized interneuron types of adult cortical layer I, suggesting a fairly broad expression at the RNA level. It remains to be determined whether all proteins are synthesized, to which pre- or postsynaptic subdomains in a given neuron type they localize, and whether all are involved in synaptic transmission. J. Comp. Neurol. 525:976-1033, 2017. © 2016 Wiley Periodicals, Inc.

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Inhibitory Interneuron Classes Express Complementary AMPA-Receptor Patterns in Macaque Primary Visual Cortex

Cited by 20 publications

References 60 publications

Multiple Transmitter Receptors in Regions and Layers of the Human Cerebral Cortex

Multiple Transmitter Receptors in Regions and Layers of the Human Cerebral Cortex

Synapse‐specific expression of calcium‐permeable AMPA receptors in neocortical layer 5

Ionotropic glutamate receptors: Which ones, when, and where in the mammalian neocortex

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