Frequency-specific response facilitation of supra and infragranular barrel cortical neurons depends on NMDA receptor activation in rats

Barros-Zulaica, Natalí; Castejon, Carlos; Núñez, Ángel

doi:10.1016/j.neuroscience.2014.09.057

Cited by 12 publications

(13 citation statements)

References 61 publications

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“…Accordingly, clustering techniques applied to unit recordings of BF neurons during different attentional tasks have revealed a large number of distinct categories of task-phase-specific activity patterns in these BF neurons (Tingley et al, 2014 ). Consequently, anatomical and optogenetic results strongly suggest the existence of cholinergic neuronal populations in the BF that are involved in the modulation of sensory cortical response, as has been published recently in the somatosensory cortex (Barros-Zulaica et al, 2014 ; Martin-Cortecero and Núñez, 2014 ).…”

Section: Discussionsupporting

confidence: 52%

“…These findings suggest that a large network of synaptically-related cholinergic BF neurons is involved in cortical activation which is probably caused by reductions in potassium conductances (McCormick, 1992 ; Oldford and Castro-Alamancos, 2003 ). However, cholinergic modulation of precise sensory responses may be controlled by specific groups of neurons through modulation of glutamatergic cortical receptors (Carr and Surmeier, 2007 ; Núñez et al, 2012 ; Barros-Zulaica et al, 2014 ). In agreement with the existence of two functional roles for cholinergic BF pathways, microdialysis studies in the medial prefrontal cortex have reported a tonic ACh increase during attention-related performance tasks (Passetti et al, 2000 ) that may promote a general state of cortical arousal (EEG desynchronization).…”

Section: Discussionmentioning

confidence: 99%

“…Acetylcholine (ACh) is essential to normal central nervous system (CNS) function, modulating the activity of the thalamocortical network in many important brain functions, such as arousal (e.g., Buzsáki et al, 1988 ; Détári, 2000 ; Szymusiak et al, 2000 ; Lee et al, 2004 ; Goard and Dan, 2009 ), attention (Chiba et al, 1999 ; Sarter et al, 2003 ), learning (Wilson and Rolls, 1990a , b ; Mayse et al, 2015 ) and memory (Pauli and O’Reilly, 2008 ; Hasselmo and Sarter, 2011 ; Luchicchi et al, 2014 ; Sarter et al, 2014 ). Moreover, ACh enhances synaptic plasticity in the hippocampus (Doralp and Leung, 2008 ; Fernández de Sevilla et al, 2008 ; Navarrete et al, 2012 ) and neocortex (Metherate and Ashe, 1993 ; Kuo et al, 2009 ; Bueno-Junior et al, 2012 ; Núñez et al, 2012 ; Barros-Zulaica et al, 2014 ; Martin-Cortecero and Núñez, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

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Modulation of Specific Sensory Cortical Areas by Segregated Basal Forebrain Cholinergic Neurons Demonstrated by Neuronal Tracing and Optogenetic Stimulation in Mice

Chaves-Coira

Barros-Zulaica

Rodrigo-Angulo

et al. 2016

Front. Neural Circuits

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Neocortical cholinergic activity plays a fundamental role in sensory processing and cognitive functions. Previous results have suggested a refined anatomical and functional topographical organization of basal forebrain (BF) projections that may control cortical sensory processing in a specific manner. We have used retrograde anatomical procedures to demonstrate the existence of specific neuronal groups in the BF involved in the control of specific sensory cortices. Fluoro-Gold (FlGo) and Fast Blue (FB) fluorescent retrograde tracers were deposited into the primary somatosensory (S1) and primary auditory (A1) cortices in mice. Our results revealed that the BF is a heterogeneous area in which neurons projecting to different cortical areas are segregated into different neuronal groups. Most of the neurons located in the horizontal limb of the diagonal band of Broca (HDB) projected to the S1 cortex, indicating that this area is specialized in the sensory processing of tactile stimuli. However, the nucleus basalis magnocellularis (B) nucleus shows a similar number of cells projecting to the S1 as to the A1 cortices. In addition, we analyzed the cholinergic effects on the S1 and A1 cortical sensory responses by optogenetic stimulation of the BF neurons in urethane-anesthetized transgenic mice. We used transgenic mice expressing the light-activated cation channel, channelrhodopsin-2, tagged with a fluorescent protein (ChR2-YFP) under the control of the choline-acetyl transferase promoter (ChAT). Cortical evoked potentials were induced by whisker deflections or by auditory clicks. According to the anatomical results, optogenetic HDB stimulation induced more extensive facilitation of tactile evoked potentials in S1 than auditory evoked potentials in A1, while optogenetic stimulation of the B nucleus facilitated either tactile or auditory evoked potentials equally. Consequently, our results suggest that cholinergic projections to the cortex are organized into segregated pools of neurons that may modulate specific cortical areas.

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Section: Discussionsupporting

confidence: 52%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Modulation of Specific Sensory Cortical Areas by Segregated Basal Forebrain Cholinergic Neurons Demonstrated by Neuronal Tracing and Optogenetic Stimulation in Mice

Chaves-Coira

Barros-Zulaica

Rodrigo-Angulo

et al. 2016

Front. Neural Circuits

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“…It is known that short-latency spikes evoked by whisker stimulation in the barrel cortex are mainly mediated through non-NMDA receptors while NMDA receptors are implicated mainly in spikes generated later after them [ 72 ]. Studies from our laboratory confirmed the implication of NMDA receptors in the late component of cortical tactile responses [ 57 , 58 ]. A recent study suggest that POm associated synaptic pathways in barrel cortex are responsible for these mediating whisker-evoked NMDA receptor dependent spikes [ 73 ], in agreement with our results.…”

Section: Discussionmentioning

confidence: 73%

“…However, this reduction was not homogeneous along the sensory response ( Fig 2E and 2F ). Previous reports from our laboratory have described two different components of tactile responses and the relevant implication of N-methyl-D-aspartate (NMDA) receptors manly in the late component of the response [ 57 , 58 ]. Accordingly, here we divided each PSTH in two components: the first (from onset to 20 ms) and the second (from 20 ms to offset) components.…”

Section: Resultsmentioning

confidence: 99%

Control of Somatosensory Cortical Processing by Thalamic Posterior Medial Nucleus: A New Role of Thalamus in Cortical Function

2016

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Current knowledge of thalamocortical interaction comes mainly from studying lemniscal thalamic systems. Less is known about paralemniscal thalamic nuclei function. In the vibrissae system, the posterior medial nucleus (POm) is the corresponding paralemniscal nucleus. POm neurons project to L1 and L5A of the primary somatosensory cortex (S1) in the rat brain. It is known that L1 modifies sensory-evoked responses through control of intracortical excitability suggesting that L1 exerts an influence on whisker responses. Therefore, thalamocortical pathways targeting L1 could modulate cortical firing. Here, using a combination of electrophysiology and pharmacology in vivo, we have sought to determine how POm influences cortical processing. In our experiments, single unit recordings performed in urethane-anesthetized rats showed that POm imposes precise control on the magnitude and duration of supra- and infragranular barrel cortex whisker responses. Our findings demonstrated that L1 inputs from POm imposed a time and intensity dependent regulation on cortical sensory processing. Moreover, we found that blocking L1 GABAergic inhibition or blocking P/Q-type Ca2+ channels in L1 prevents POm adjustment of whisker responses in the barrel cortex. Additionally, we found that POm was also controlling the sensory processing in S2 and this regulation was modulated by corticofugal activity from L5 in S1. Taken together, our data demonstrate the determinant role exerted by the POm in the adjustment of somatosensory cortical processing and in the regulation of cortical processing between S1 and S2. We propose that this adjustment could be a thalamocortical gain regulation mechanism also present in the processing of information between cortical areas.

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Posterior thalamic nucleus axon terminals have different structure and functional impact in the motor and somatosensory vibrissal cortices

et al. 2019

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Rodents extract information about nearby objects from the movement of their whiskers through dynamic computations that are carried out by a network of forebrain structures that includes the thalamus and the primary sensory (S1BF) and motor (M1wk) whisker cortices. The posterior nucleus (Po), a higher order thalamic nucleus, is a key hub of this network, receiving cortical and brainstem sensory inputs and innervating both motor and sensory whisker-related cortical areas. In a recent study in rats, we showed that Po inputs differently impact sensory processing in S1BF and M1wk. Here, in C57BL/6 mice, we measured Po synaptic bouton layer distribution and size, compared cortical unit response latencies to "in vivo" Po activation, and pharmacologically examined the glutamatergic receptor mechanisms involved. We found that, in S1BF, a large majority (56%) of Po axon varicosities are located in layer (L)5a and only 12% in L2-L4, whereas in M1wk this proportion is inverted to 18% and 55%, respectively. Light and electron microscopic measurements showed that Po synaptic boutons in M1wk layers 3-4 are significantly larger (~ 50%) than those in S1BF L5a. Electrical Po stimulation elicits different areaspecific response patterns. In S1BF, responses show weak or no facilitation, and involve both ionotropic and metabotropic glutamate receptors, whereas in M1wk, unit responses exhibit facilitation to repetitive stimulation and involve ionotropic NMDA glutamate receptors. Because of the different laminar distribution of axon terminals, synaptic bouton size and receptor mechanisms, the impact of Po signals on M1wk and S1BF, although simultaneous, is likely to be markedly different.

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Frequency-specific response facilitation of supra and infragranular barrel cortical neurons depends on NMDA receptor activation in rats

Cited by 12 publications

References 61 publications

Modulation of Specific Sensory Cortical Areas by Segregated Basal Forebrain Cholinergic Neurons Demonstrated by Neuronal Tracing and Optogenetic Stimulation in Mice

Modulation of Specific Sensory Cortical Areas by Segregated Basal Forebrain Cholinergic Neurons Demonstrated by Neuronal Tracing and Optogenetic Stimulation in Mice

Control of Somatosensory Cortical Processing by Thalamic Posterior Medial Nucleus: A New Role of Thalamus in Cortical Function

Posterior thalamic nucleus axon terminals have different structure and functional impact in the motor and somatosensory vibrissal cortices

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