Muscarinic Modulation of SK2-Type K+ Channels Promotes Intrinsic Plasticity in L2/3 Pyramidal Neurons of the Mouse Primary Somatosensory Cortex

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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A-type K+channels encoded by Kv4.2, Kv4.3 and Kv1.4 differentially regulate intrinsic excitability of cortical pyramidal neurons

The Journal of Physiology ◽

10.1113/jphysiol.2012.229013 ◽

2012 ◽

Vol 590 (16) ◽

pp. 3877-3890 ◽

Cited By ~ 42

Author(s):

Yarimar Carrasquillo ◽

Andreas Burkhalter ◽

Jeanne M. Nerbonne

Keyword(s):

Pyramidal Neurons ◽

Intrinsic Excitability ◽

K Channels ◽

Type K ◽

Cortical Pyramidal Neurons

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In-depth characterization of layer 5 output neurons of the primary somatosensory cortex innervating the mouse dorsal spinal cord

10.1101/2020.04.02.021311 ◽

2020 ◽

Author(s):

N. Frezel ◽

E. Platonova ◽

F.F. Voigt ◽

J.M. Mateos ◽

R. Kastli ◽

...

Keyword(s):

Somatosensory Cortex ◽

Dorsal Horn ◽

Spinal Dorsal Horn ◽

Pyramidal Neurons ◽

Sensory Information ◽

Fine Tuning ◽

Primary Somatosensory Cortex ◽

Spinal Dorsal ◽

Factor C ◽

Postsynaptic Target

AbstractNeuronal circuits of the spinal dorsal horn integrate sensory information from the periphery with inhibitory and facilitating input from higher CNS areas. Most previous work focused on projections descending from the hindbrain. Less is known about inputs descending from the cerebral cortex. Here, we identified cholecystokinin (CCK) positive layer 5 pyramidal neurons of the primary somatosensory cortex (CCK+ S1-CST neurons) as a major source of input to the spinal dorsal horn. We combined intersectional genetics and virus-mediated gene transfer to characterize CCK+ S1-CST neurons and to define their presynaptic input and postsynaptic target neurons. We found that S1-CST neurons constitute a heterogeneous population that can be subdivided into distinct molecular subgroups. Rabies-based retrograde tracing revealed monosynaptic input from layer 2/3 pyramidal neurons, from parvalbumin (PV) positive cortical interneurons, and from thalamic relay neurons in the ventral posterolateral nucleus. WGA-based anterograde tracing identified postsynaptic target neurons in dorsal horn laminae III and IV. About 60% of these neurons were inhibitory and about 60% of all spinal target neurons expressed the transcription factor c-Maf. The heterogeneous nature of both S1-CST neurons and their spinal targets suggest complex roles in the fine-tuning of sensory processing.

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Cell size-dependent Nogo-A expression in layer V pyramidal neurons of the rat primary somatosensory cortex

Neuroscience Letters ◽

10.1016/j.neulet.2005.10.032 ◽

2006 ◽

Vol 394 (2) ◽

pp. 117-120 ◽

Cited By ~ 9

Author(s):

Jung-Won Shin ◽

Eun-Sep Shim ◽

Gwang-Ho Hwang ◽

Hyuck-Sang Jung ◽

Ji-Ho Park ◽

...

Keyword(s):

Somatosensory Cortex ◽

Cell Size ◽

Pyramidal Neurons ◽

Primary Somatosensory Cortex ◽

Size Dependent ◽

Layer V

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Changes in Intrinsic Properties of Pyramidal Neurons in Adult Rat S1 During Cortical Reorganization

Journal of Neurophysiology ◽

10.1152/jn.00924.2004 ◽

2005 ◽

Vol 94 (1) ◽

pp. 501-511 ◽

Cited By ~ 8

Author(s):

Peter W. Hickmott

Keyword(s):

Somatosensory Cortex ◽

Pyramidal Neurons ◽

Cortical Reorganization ◽

Primary Somatosensory Cortex ◽

Membrane Properties ◽

Intrinsic Properties ◽

Adult Rat ◽

Layer 2 ◽

Cortical Circuit

Peripheral denervation causes significant changes in the organization of developing or adult primary somatosensory cortex (S1). However, the basic mechanisms that underlie reorganization are not well understood. Most attention has been focused on possible synaptic mechanisms associated with reorganization. However, another important determinant of cortical circuit function is the intrinsic membrane properties of neurons in the circuit. Here we document changes in the intrinsic properties of pyramidal neurons in cortical layer 2/3 in adult rat primary somatosensory cortex (S1) after varying durations of forepaw denervation. Denervation of the forepaw induced a rapid and sustained shift in the location of the border between the forepaw and lower jaw representations of adult S1 (reorganization). Coronal slices from the reorganized region were maintained in vitro and the intrinsic properties of layer 2/3 pyramidal neurons of S1 were determined using whole cell recordings. In general, passive membrane properties were not affected by denervation; however, a variety of active properties were. The most robust changes were increases in the amplitudes of the fast and medium afterhyperpolarization (AHP) and an increase in the interval between action potentials (APs). Additional changes at some durations of denervation were observed for the AP threshold. These observations indicate that changes in intrinsic properties, mostly reflecting a decrease in overall excitation, may play a role in changes in cortical circuit properties during reorganization in adult S1, and suggest a possible role for AHPs in some of those changes.

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The mode of synaptic activation of pyramidal neurons in the cat primary somatosensory cortex: an intracellular HRP study

Experimental Brain Research ◽

10.1007/bf00228842 ◽

1990 ◽

Vol 80 (1) ◽

Cited By ~ 14

Author(s):

T. Yamamoto ◽

A. Samejima ◽

H. Oka

Keyword(s):

Somatosensory Cortex ◽

Pyramidal Neurons ◽

Primary Somatosensory Cortex ◽

Synaptic Activation ◽

Intracellular Hrp

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In-Depth Characterization of Layer 5 Output Neurons of the Primary Somatosensory Cortex Innervating the Mouse Dorsal Spinal Cord

Cerebral Cortex Communications ◽

10.1093/texcom/tgaa052 ◽

2020 ◽

Vol 1 (1) ◽

Author(s):

N Frezel ◽

E Platonova ◽

F F Voigt ◽

J M Mateos ◽

R Kastli ◽

...

Keyword(s):

Somatosensory Cortex ◽

Dorsal Horn ◽

Spinal Dorsal Horn ◽

Pyramidal Neurons ◽

Sensory Information ◽

Fine Tuning ◽

Primary Somatosensory Cortex ◽

Spinal Dorsal ◽

Factor C ◽

Postsynaptic Target

Abstract Neuronal circuits of the spinal dorsal horn integrate sensory information from the periphery with inhibitory and facilitating input from higher central nervous system areas. Most previous work focused on projections descending from the hindbrain. Less is known about inputs descending from the cerebral cortex. Here, we identified cholecystokinin (CCK) positive layer 5 pyramidal neurons of the primary somatosensory cortex (CCK + S1-corticospinal tract [CST] neurons) as a major source of input to the spinal dorsal horn. We combined intersectional genetics and virus-mediated gene transfer to characterize CCK+ S1-CST neurons and to define their presynaptic input and postsynaptic target neurons. We found that S1-CST neurons constitute a heterogeneous population that can be subdivided into distinct molecular subgroups. Rabies-based retrograde tracing revealed monosynaptic input from layer 2/3 pyramidal neurons, from parvalbumin positive cortical interneurons, and from thalamic relay neurons in the ventral posterolateral nucleus. Wheat germ agglutinin-based anterograde tracing identified postsynaptic target neurons in dorsal horn laminae III and IV. About 60% of these neurons were inhibitory and about 60% of all spinal target neurons expressed the transcription factor c-Maf. The heterogeneous nature of both S1-CST neurons and their spinal targets suggest complex roles in the fine-tuning of sensory processing.

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