Intracortical connectivity of layer VI pyramidal neurons in the somatosensory cortex of normal and barrelless mice

1. Two-hundred and seven neurons were examined for changes in their responsiveness during the iontophoretic administration of acetylcholine (ACh) in barbiturate-anesthetized cats. 2. The laminar locations of 78 cells were determined. Cholinoceptive neurons were found in all cortical layers and ranged from 50% of the cells tested in layer I to 78% in layer VI. 3. When the responsiveness of a neuron was measured by the magnitude of the discharge generated by a fixed dose of glutamate, 30 of 47 cases (64%) were potentiated, and 4 (8%) were depressed when ACh was administered during glutamate-induced excitation. 4. ACh administered during glutamate excitation was significantly more effective in altering neuronal responsiveness than was ACh administered alone (P less than 0.001). 5. When the responsiveness of a neuron was measured by the magnitude of the discharge generated by a standard somatic stimulus applied to the receptive field, 42 of 52 cases (81%) were potentiated during ACh application. This was again different from ACh treatment alone where only 4 of 27 tests (15%) resulted in subsequent enhancement of the response to somatic stimuli. 6. ACh generally increased the responsiveness of neurons with peripheral receptive fields and caused the appearance of a receptive field in some cells lacking one. 7. In many cases the changes in excitability, as measured by responses either to glutamate or to somatic stimulation, remained for prolonged time periods. When glutamate was used to test excitability, 34% (16 of 47) of the enhancements lasted more than 5 min. When somatic stimuli were used 29% (15 of 52) lasted more than 5 min. With both measures some neurons still displayed enhanced responses more than 1 h after the treatment with ACh. 8. ACh appears to act as a permissive agent that allows modification of the effectiveness with which previously existing afferent inputs drive somatosensory cortical neurons. 9. This mechanism to alter neuronal responsiveness has many of the characteristics necessary to account for the reorganization observed in somatosensory cortex following alterations in its afferent drive and may be related to some forms of learning and memory.

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High-order thalamic inputs to primary somatosensory cortex are stronger and longer lasting than cortical inputs

eLife ◽

10.7554/elife.44158 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 26

Author(s):

Wanying Zhang ◽

Randy M Bruno

Keyword(s):

Somatosensory Cortex ◽

Primary Motor Cortex ◽

Pyramidal Neurons ◽

Sensory Stimulation ◽

Primary Somatosensory Cortex ◽

Specific Substrate ◽

Medial Nucleus ◽

Posterior Medial Nucleus ◽

Cortical Inputs

Layer (L) 2/3 pyramidal neurons in the primary somatosensory cortex (S1) are sparsely active, spontaneously and during sensory stimulation. Long-range inputs from higher areas may gate L2/3 activity. We investigated their in vivo impact by expressing channelrhodopsin in three main sources of feedback to rat S1: primary motor cortex, secondary somatosensory cortex, and secondary somatosensory thalamic nucleus (the posterior medial nucleus, POm). Inputs from cortical areas were relatively weak. POm, however, more robustly depolarized L2/3 cells and, when paired with peripheral stimulation, evoked action potentials. POm triggered not only a stronger fast-onset depolarization but also a delayed all-or-none persistent depolarization, lasting up to 1 s and exhibiting alpha/beta-range oscillations. Inactivating POm somata abolished persistent but not initial depolarization, indicating a recurrent circuit mechanism. We conclude that secondary thalamus can enhance L2/3 responsiveness over long periods. Such timescales could provide a potential modality-specific substrate for attention, working memory, and plasticity.

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Noradrenergic enhancement of GABA-induced input resistance changes in layer V regular spiking pyramidal neurons of rat somatosensory cortex

Brain Research ◽

10.1016/0006-8993(95)00060-4 ◽

1995 ◽

Vol 675 (1-2) ◽

pp. 171-182 ◽

Cited By ~ 31

Author(s):

Francis M. Sessler ◽

Weimin Liu ◽

Michael L. Kirifides ◽

Robert D. Mouradian ◽

Rick C.-S. Lin ◽

...

Keyword(s):

Somatosensory Cortex ◽

Pyramidal Neurons ◽

Input Resistance ◽

Layer V ◽

Rat Somatosensory Cortex

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Glutamatergic Nonpyramidal Neurons From Neocortical Layer VI and Their Comparison With Pyramidal and Spiny Stellate Neurons

Journal of Neurophysiology ◽

10.1152/jn.91094.2008 ◽

2009 ◽

Vol 101 (2) ◽

pp. 641-654 ◽

Cited By ~ 38

Author(s):

Sofija Andjelic ◽

Thierry Gallopin ◽

Bruno Cauli ◽

Elisa L. Hill ◽

Lisa Roux ◽

...

Keyword(s):

Pyramidal Neurons ◽

Glutamate Transporter ◽

Gabaergic Interneuron ◽

Acid Decarboxylase ◽

Projection Neurons ◽

Heterogeneous Cluster ◽

Glutamatergic Neurons ◽

Layer V ◽

Nonpyramidal Neurons ◽

Layer Vi

The deeper part of neocortical layer VI is dominated by nonpyramidal neurons, which lack a prominent vertically ascending dendrite and predominantly establish corticocortical connections. These neurons were studied in rat neocortical slices using patch-clamp, single-cell reverse transcription–polymerase chain reaction, and biocytin labeling. The majority of these neurons expressed the vesicular glutamate transporter but not glutamic acid decarboxylase, suggesting that a high proportion of layer VI nonpyramidal neurons are glutamatergic. Indeed, they exhibited numerous dendritic spines and established asymmetrical synapses. Our sample of glutamatergic nonpyramidal neurons displayed a wide variety of somatodendritic morphologies and a subset of these cells expressed the Nurr1 mRNA, a marker for ipsilateral, but not commissural corticocortical projection neurons in layer VI. Comparison with spiny stellate and pyramidal neurons from other layers showed that glutamatergic neurons consistently exhibited a low occurrence of GABAergic interneuron markers and regular spiking firing patterns. Analysis of electrophysiological diversity using unsupervised clustering disclosed three groups of cells. Layer V pyramidal neurons were segregated into a first group, whereas a second group consisted of a subpopulation of layer VI neurons exhibiting tonic firing. A third heterogeneous cluster comprised spiny stellate, layer II/III pyramidal, and layer VI neurons exhibiting adaptive firing. The segregation of layer VI neurons in two different clusters did not correlate either with their somatodendritic morphologies or with Nurr1 expression. Our results suggest that electrophysiological similarities between neocortical glutamatergic neurons extend beyond layer positioning, somatodendritic morphology, and projection specificity.

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The postnatal development of layer VI pyramidal neurons in the cat's striate cortex, as visualized by intracellular Lucifer yellow injections in aldehyde-fixed tissue

Developmental Brain Research ◽

10.1016/0165-3806(89)90004-7 ◽

1989 ◽

Vol 45 (1) ◽

pp. 29-38 ◽

Cited By ~ 36

Author(s):

J. Lübke ◽

K. Albus

Keyword(s):

Postnatal Development ◽

Pyramidal Neurons ◽

Striate Cortex ◽

Lucifer Yellow ◽

Fixed Tissue ◽

Layer Vi

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Silent Synapses in the Immature Visual Cortex: Layer-Specific Developmental Regulation

Journal of Neurophysiology ◽

10.1152/jn.00443.2003 ◽

2004 ◽

Vol 91 (2) ◽

pp. 1097-1101 ◽

Cited By ~ 39

Author(s):

Simon Rumpel ◽

Gunnar Kattenstroth ◽

Kurt Gottmann

Keyword(s):

Visual Cortex ◽

Pyramidal Neurons ◽

Developmental Regulation ◽

Pyramidal Cells ◽

Cortical Plate ◽

Glutamatergic Synapses ◽

Silent Synapses ◽

Deep Layers ◽

Further Development ◽

Layer Vi

Central glutamatergic synapses are thought to initially form as immature, so-called silent synapses showing exclusively N-methyl-d-aspartate receptor-mediated synaptic transmission. Postsynaptic insertion of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors during further development leads to a conversion into functional, mature synapses. Here, we tested the hypothesis that, according to the “inside first–outside last” pattern of neocortical layer formation and synaptogenesis, pyramidal cells in the superficial layers might show a higher fraction of silent synapses compared with pyramidal cells in the deep layers. We performed an electrophysiological analysis of glutamatergic synapses in acute rat visual cortex slices during postnatal development. In layer VI pyramidal neurons the incidence of silent synapses was high during the first postnatal week and strongly declined during further development. Surprisingly, in superficial cortical plate pyramidal neurons (immature layers II/III), the fraction of silent synapses was initially very low and increased up to the second postnatal week. Thereafter, a similar decline as found in layer VI pyramidal neurons was observed. Thus the developmental regulation of silent synapses was clearly different in pyramidal neurons from different neocortical layers. The almost complete absence of silent synapses at early stages in layer II/III pyramidal neurons indicates that an initially formed subset of synapses is constitutively functional. This might be important to enable spontaneous activity and latter activity-dependent maturation of synapses.

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