Input-specific effects of acetylcholine on sensory and intracortical evoked responses in the “barrel cortex” in vivo

Oldford, E; Castro‐Alamancos, Manuel A.

doi:10.1016/s0306-4522(02)00663-2

Cited by 108 publications

(65 citation statements)

References 103 publications

(141 reference statements)

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“…In sensory systems, it is usually considered that cholinergic projections from the PPTg exert their modulatory action at thalamic level, where they enhance the relay of sensory messages during arousal (Kayama et al, 1986;McCormick and Prince, 1987;Hu et al, 1989;Deschênes and Hu, 1990;Curro Dossi et al, 1991;McCormick, 1992;Oldford and Castro-Alamancos, 2003;Mooney et al, 2004). In prethalamic stations, sensory transmission is traditionally thought not to be state-dependent, but in light of the present results, that view may now require revision.…”

Section: Functional Implicationsmentioning

confidence: 71%

Cholinergic Modulation of Vibrissal Receptive Fields in Trigeminal Nuclei

Timofeeva¹,

Dufresne²,

Sı́k³

et al. 2005

J. Neurosci.

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In sensory systems, it is usually considered that mesopontine cholinergic neurons exert their modulatory action in the thalamus by enhancing the relay of sensory messages during states of neural network desynchronization. Here, we report a projection heretofore unknown of these cholinergic cells to the interpolar division of the brainstem trigeminal complex in rats. After FluoroGold injection in the interpolar nucleus, a number of retrogradely labeled cells were found bilaterally in the pedunculopontine tegmental nucleus, and immunostaining revealed that the vast majority of these cells were also positive for choline acetyltransferase. Immunostaining for the acetylcholine vesicular transporter confirmed the presence of cholinergic terminals in the interpolar nucleus, where electron microscopy showed that they make symmetric and asymmetric synaptic contacts with dendrites and axon terminals. In agreement with these anatomical data, recordings in slices showed that the cholinergic agonist carbachol depolarizes large-sized interpolaris cells and increases their excitability. Local application of carbachol in vivo enhances responses to adjacent whiskers, whereas systemic administration of the cholinergic antagonist scopolamine produces an opposite effect. Together, these results show that mesopontine cholinergic neurons exert a direct, effective control over receptive field size at the very first relay stations of the vibrissal system in rodents. As far as receptive field synthesis in the lemniscal pathway relies on intersubnuclear projections from the spinal complex, it follows that cholinergic modulation of sensory transmission in the interpolar nucleus will have a direct bearing on the type of messages that is forwarded to the thalamus and cerebral cortex.

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Section: Functional Implicationsmentioning

confidence: 71%

Cholinergic Modulation of Vibrissal Receptive Fields in Trigeminal Nuclei

Timofeeva¹,

Dufresne²,

Sı́k³

et al. 2005

J. Neurosci.

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“…However, while such an increase can explain the larger amplitude of the evoked cortical sensory responses observed in vivo during high levels of intracortical ACH, it does not account for their increased SNR. The finding that presynaptic ACHRs selectively enhance sensory inputs over cortico-cortical feed-back inputs (17)(18)(19) has led to the hypothesis that such a mechanism could underlie the increase in SNR (14).…”

mentioning

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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“…ACh favours incoming thalamocortical sensory afferents relative to intracortical pathways [146,147], and combined BF and whisker stimulation increases whisker-evoked LFPs in the barrel cortex [148]. Interestingly, BF-ACh stimulation leads to activation of VIP-containing interneurons during locomotion in the visual cortex [149].…”

Section: (B) Basal Forebrain Cholinergic Pathway Stimulationevoked Nementioning

confidence: 99%

Neuronal networks and mediators of cortical neurovascular coupling responses in normal and altered brain states

Lecrux

Hamel

2016

Phil. Trans. R. Soc. B

101

103

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One contribution of 15 to a Theo Murphy meeting issue 'Interpreting BOLD: a dialogue between cognitive and cellular neuroscience'. Brain imaging techniques that use vascular signals to map changes in neuronal activity, such as blood oxygenation level-dependent functional magnetic resonance imaging, rely on the spatial and temporal coupling between changes in neurophysiology and haemodynamics, known as 'neurovascular coupling (NVC)'. Accordingly, NVC responses, mapped by changes in brain haemodynamics, have been validated for different stimuli under physiological conditions. In the cerebral cortex, the networks of excitatory pyramidal cells and inhibitory interneurons generating the changes in neural activity and the key mediators that signal to the vascular unit have been identified for some incoming afferent pathways. The neural circuits recruited by whisker glutamatergic-, basal forebrain cholinergic-or locus coeruleus noradrenergic pathway stimulation were found to be highly specific and discriminative, particularly when comparing the two modulatory systems to the sensory response. However, it is largely unknown whether or not NVC is still reliable when brain states are altered or in disease conditions. This lack of knowledge is surprising since brain imaging is broadly used in humans and, ultimately, in conditions that deviate from baseline brain function. Using the whisker-to-barrel pathway as a model of NVC, we can interrogate the reliability of NVC under enhanced cholinergic or noradrenergic modulation of cortical circuits that alters brain states.This article is part of the themed issue 'Interpreting BOLD: a dialogue between cognitive and cellular neuroscience'.

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Input-specific effects of acetylcholine on sensory and intracortical evoked responses in the “barrel cortex” in vivo

Cited by 108 publications

References 103 publications

Cholinergic Modulation of Vibrissal Receptive Fields in Trigeminal Nuclei

Cholinergic Modulation of Vibrissal Receptive Fields in Trigeminal Nuclei

Cholinergic filtering in the recurrent excitatory microcircuit of cortical layer 4

Neuronal networks and mediators of cortical neurovascular coupling responses in normal and altered brain states

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