Layer‐ and cell‐type‐specific suprathreshold stimulus representation in rat primary somatosensory cortex

Kock, De; Bruno, Randy M.; Spors, Hartwig; Sakmann, Bert

doi:10.1113/jphysiol.2006.124321

Cited by 313 publications

(429 citation statements)

References 69 publications

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“…S3.). Thus, because i) it is unlikely that volume transmission of ACH reaches concentrations in the millimolar range in vivo, ii) both the spontaneous and sensoryevoked spiking activity of S1 PCs in vivo are low (36)(37)(38), iii) only less than half the PCs are transiently hyperpolarized, and iv) the transient hyperpolarization represents only a minor part of the biphasic effect of ACH (Ϸ2.4% of total duration in L5, Ϸ5.2% in L2/3; Ϸ21% of peak depolarization in L5, Ϸ45% in L2/3), we conclude that the effect of ACH is predominantly excitatory in L2/3 and L5 of S1. The presence of a different mACHR subtype in L4-SNs than in the L2/3 and L5 PCs further supports the idea of a layerspecific effect of ACH.…”

Section: Discussionmentioning

confidence: 99%

Cholinergic filtering in the recurrent excitatory microcircuit of cortical layer 4

Eggermann

Feldmeyer

2009

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

101

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Neocortical acetylcholine (ACH) release is known to enhance signal processing by increasing the amplitude and signal-to-noise ratio (SNR) of sensory responses. It is widely accepted that the larger sensory responses are caused by a persistent increase in the excitability of all cortical excitatory neurons. Here, contrary to this concept, we show that ACH persistently inhibits layer 4 (L4) spiny neurons, the main targets of thalamocortical inputs. Using whole-cell recordings in slices of rat primary somatosensory cortex, we demonstrate that this inhibition is specific to L4 and contrasts with the ACH-induced persistent excitation of pyramidal cells in L2/3 and L5. We find that this inhibition is induced by postsynaptic M 4 -muscarinic ACH receptors and is mediated by the opening of inwardly rectifying potassium (K ir ) channels. Pair recordings of L4 spiny neurons show that ACH reduces synaptic release in the L4 recurrent microcircuit. We conclude that ACH has a differential layer-specific effect that results in a filtering of weak sensory inputs in the L4 recurrent excitatory microcircuit and a subsequent amplification of relevant inputs in L2/3 and L5 excitatory microcircuits. This layer-specific effect may contribute to improve cortical SNR.

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Section: Discussionmentioning

confidence: 99%

Cholinergic filtering in the recurrent excitatory microcircuit of cortical layer 4

Eggermann

Feldmeyer

2009

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

101

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“…Doublets or triplets of presynaptic APs (which occur in response to whisker stimulation in vivo) (cf. Brecht and Sakmann, 2002;de Kock et al, 2007) thus significantly reduced the probability of transmission failure in these connections.…”

Section: Synaptic Short-term Dynamicsmentioning

confidence: 96%

“…The convergence estimate was larger than the estimate derived from the experimental success rate (on average, 5-15 L4 neurons had to be tested before a synaptic connection was found for a given L2/3 interneuron, corresponding to a convergence of 7-20%; this measure is however sensitive to several experimental biases) (see Materials and Methods). During a whisker stimulus, ϳ0.1-0.4 APs per stimulus have been measured in vivo (Brecht and Sakmann, 2002;de Kock et al 2007). Thus, after a whisker stimulus, unitary EPSPs evoked by 100 -400 APs can be expected to converge on a L2/3 interneuron.…”

Section: Signal Flow In a Cortical Columnmentioning

confidence: 99%

Efficient Recruitment of Layer 2/3 Interneurons by Layer 4 Input in Single Columns of Rat Somatosensory Cortex

Helmstaedter¹,

Staiger²,

Sakmann³

et al. 2008

J. Neurosci.

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108

109

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Interneurons in layers 2/3 are excited by pyramidal cells within the same layer (Reyes et al., 1998; Gupta et al., 2000), but little is known about translaminar innervation of these interneurons by spiny neurons in the main cortical input layer 4 (L4). Here, we investigated (1) how efficiently L4 spiny neurons excite L2/3 interneurons via monosynaptic connections, (2) whether glutamate release from axon terminals of L4 spiny neurons depends on the identity of the postsynaptic interneuron, and (3) how L4-to-L2/3 interneuron connections compare with L4-to-L2/3 pyramidal neuron connections. We recorded from pairs of L4 spiny neurons and L2/3 interneurons in acute slices of rat barrel cortex of postnatal day 20 (P20) to P29 rats. The L4-to-L2/3 interneuron connections had an average unitary EPSP of 1.2 Ϯ 1.1 mV. We found an average of 2.3 Ϯ 0.8 contacts per connection, and the L4-to-L2/3 interneuron innervation domains were mostly column restricted. Unitary EPSP amplitudes and paired-pulse ratios in the L4-to-L2/3 interneuron connections depended on the "group" of the postsynaptic interneuron. Averaged over all L4-to-L2/3 interneuron connections, unitary EPSP amplitudes were 1.8-fold higher than in the translaminar L4-to-L2/3 pyramidal cell connections. Our results suggest that L4 spiny neurons may more efficiently recruit L2/3 interneurons than L2/3 pyramidal neurons, and that glutamate release from translaminar boutons of L4 spiny neuron axons is target cell specific.

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“…VPM inputs to the cortex (42) activate L6 during whisker stimulation (25,43), suggesting that tactile activity itself is important for L6-mediated gating of frequency cues. In this manner, L6 may provide a top-down attentional signal that turns on a fine-detail examination mode critical for behavioral tasks such as texture discrimination.…”

Section: Discussionmentioning

confidence: 99%

Cortical control of adaptation and sensory relay mode in the thalamus

Mease

Krieger

Groh

2014

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

116

183

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A major synaptic input to the thalamus originates from neurons in cortical layer 6 (L6); however, the function of this cortico-thalamic pathway during sensory processing is not well understood. In the mouse whisker system, we found that optogenetic stimulation of L6 in vivo results in a mixture of hyperpolarization and depolarization in the thalamic target neurons. The hyperpolarization was transient, and for longer L6 activation (>200 ms), thalamic neurons reached a depolarized resting membrane potential which affected key features of thalamic sensory processing. Most importantly, L6 stimulation reduced the adaptation of thalamic responses to repetitive whisker stimulation, thereby allowing thalamic neurons to relay higher frequencies of sensory input. Furthermore, L6 controlled the thalamic response mode by shifting thalamo-cortical transmission from bursting to single spiking. Analysis of intracellular sensory responses suggests that L6 impacts these thalamic properties by controlling the resting membrane potential and the availability of the transient calcium current I T , a hallmark of thalamic excitability. In summary, L6 input to the thalamus can shape both the overall gain and the temporal dynamics of sensory responses that reach the cortex. S ensory signals en route to the cortex undergo profound signal transformations in the thalamus. One important thalamic transformation is sensory adaptation. Adaptation is a common characteristic of sensory systems in which neural output adjusts to the statistics and dynamics of past stimuli, thereby better encoding small stimulus changes across a wide range of scales despite the limited range of possible neural outputs (1-3). Thalamic sensory adaptation is characterized by a steep decrease in action potential (AP) activity during sustained sensory stimulation (4-7), decreasing the efficacy at which subsequent sensory stimuli are transmitted to the cortex.The widely reported duality of thalamic response mode is another key property of thalamic information processing which further affects how sensory input reaches the cortex. In burst mode, sensory inputs are relayed as short, rapid clusters of APs; in contrast, in tonic mode the same inputs are translated into single APs. Both tonic and burst modes have been described during anesthesia/sleep and wakefulness/behavior, with a pronounced shift toward the tonic mode during alertness (8-12).Although the exact information content of thalamic bursts is not yet clear, it has been suggested that bursting may signal novel stimuli to the cortex, whereas the tonic mode enables linear encoding of fine stimulus details, e.g., when an object is examined (13,14). One issue hampering the interpretation of burst/ tonic responses is that currently it is unknown if the cortex itself is involved in the rapid changes in firing modes seen in the awake and anesthetized animal (15, 16) and which mechanisms initiate these shifts in vivo.On the biophysical level, the response mode depends on the resting membrane potential (RMP), which controls...

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Layer‐ and cell‐type‐specific suprathreshold stimulus representation in rat primary somatosensory cortex

Cited by 313 publications

References 69 publications

Cholinergic filtering in the recurrent excitatory microcircuit of cortical layer 4

Cholinergic filtering in the recurrent excitatory microcircuit of cortical layer 4

Efficient Recruitment of Layer 2/3 Interneurons by Layer 4 Input in Single Columns of Rat Somatosensory Cortex

Cortical control of adaptation and sensory relay mode in the thalamus

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