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1.
J Neurosci ; 44(25)2024 Jun 19.
Article in English | MEDLINE | ID: mdl-38769008

ABSTRACT

Rapid eye movement (REM) sleep, also referred to as paradoxical sleep for the striking resemblance of its electroencephalogram (EEG) to the one observed in wakefulness, is characterized by the occurrence of transient events such as limb twitches or facial and rapid eye movements. Here, we investigated the local activity of the primary somatosensory or barrel cortex (S1) in naturally sleeping head-fixed male mice during REM. Through local field potential recordings, we uncovered local appearances of spindle waves in the barrel cortex during REM concomitant with strong delta power, challenging the view of a wakefulness-like activity in REM. We further performed extra- and intracellular recordings of thalamic cells in head-fixed mice. Our data show high-frequency thalamic bursts of spikes and subthreshold spindle oscillations in approximately half of the neurons of the ventral posterior medial nucleus which further confirmed the thalamic origin of local cortical spindles in S1 in REM. Cortical spindle oscillations were suppressed, while thalamus spike firing increased, associated with rapid mouse whisker movements and S1 cortical activity transitioned to an activated state. During REM, the sensory thalamus and barrel cortex therefore alternate between high (wake-like) and low (non-REM sleep-like) activation states, potentially providing a neuronal substrate for mnemonic processes occurring during this paradoxical sleep stage.


Subject(s)
Electroencephalography , Sleep, REM , Somatosensory Cortex , Thalamus , Animals , Mice , Sleep, REM/physiology , Somatosensory Cortex/physiology , Male , Thalamus/physiology , Mice, Inbred C57BL , Vibrissae/physiology , Vibrissae/innervation , Wakefulness/physiology , Neural Pathways/physiology
2.
J Neurosci ; 2022 May 12.
Article in English | MEDLINE | ID: mdl-35552234

ABSTRACT

GABAergic inhibitory neurons, through their molecular, anatomic and physiological diversity, provide a substrate for the modulation of ongoing cortical circuit activity throughout the sleep-wake cycle. Here, we investigated neuronal activity dynamics of parvalbumin (PV), vasoactive intestinal polypeptide (VIP) and somatostatin (SST) neurons in naturally-sleeping head-restrained mice at the level of layer 2/3 of the primary somatosensory barrel cortex of mice. Through calcium-imaging and targeted single-unit loose-patch or whole-cell recordings, we found that PV action potential (AP) firing activity was largest during both NREM (non-rapid eye movement) and REM sleep stages, that VIP neurons were most active during REM sleep and that the overall activity of SST neurons remained stable throughout the sleep/wake cycle. Analysis of neuronal activity dynamics uncovered rapid decreases in PV cell firing at wake onset followed by a progressive recovery during wake. Simultaneous local field potential (LFP) recordings further revealed that, except for SST neurons, a large proportion of neurons were modulated by ongoing delta and theta oscillations. During NREM sleep spindles, PV and SST activity increased and decreased, respectively. Finally, we uncovered the presence of whisking behavior in mice during REM sleep and show that the activity of VIP and SST is differentially modulated during awake and sleeping whisking bouts, which may provide a neuronal substrate for internal brain representations occurring during sleep.SIGNIFICANCE STATEMENTIn the sensory cortex, the balance between excitation and inhibition is believed to be highly dynamic throughout the sleep/wake cycle, shaping the response of cortical circuits to external stimuli, while allowing the formation of newly encoded memory. Using in vivo two-photon calcium imaging or targeted single-unit recordings combined with local field potential recordings, we describe the vigilance state and whisking-behavior -dependent activity of excitatory pyramidal and inhibitory GABAergic neurons in the supragranular layers of mouse somatosensory cortex. Interneuronal activity was found to be differentially modulated by ongoing delta and theta waves, sleep spindles and a novel type of whisking observed during Rapid Eye Movement (REM sleep), potentially providing a neuronal substrate for internal brain representations occurring during sleep.

3.
Cell Rep ; 26(6): 1443-1457.e5, 2019 02 05.
Article in English | MEDLINE | ID: mdl-30726730

ABSTRACT

The thalamus plays a central role in sleep rhythms in the mammalian brain and, yet, surprisingly little is known about its function and interaction with local cortical oscillations during NREM sleep (NREM). We investigated the neuronal correlates of cortical barrel activity in the two corresponding thalamic nuclei, the ventral posterior medial (VPM), and the posterior medial (Pom) nuclei during natural NREM in mice. Our data reveal (1) distinct modulations of VPM and Pom activity throughout NREM episodes, (2) a thalamic nucleus-specific phase-locking to cortical slow and spindle waves, (3) cell-specific subthreshold spindle oscillations in VPM neurons that only partially overlap with cortical spindles, and (4) that spindle features evolve throughout NREM episodes and vary according to the post-NREM state. Taken together, our results suggest that, during natural sleep, the barrel cortex exerts a leading role in the generation and transfer of slow rhythms to the somatosensory thalamus and reciprocally for spindle oscillations.


Subject(s)
Action Potentials , Neurons/physiology , Sleep , Somatosensory Cortex/physiology , Thalamus/physiology , Animals , Male , Mice , Mice, Inbred C57BL , Somatosensory Cortex/cytology , Thalamus/cytology
4.
Cell Rep ; 13(4): 647-656, 2015 Oct 27.
Article in English | MEDLINE | ID: mdl-26489463

ABSTRACT

The thalamus transmits sensory information to the neocortex and receives neocortical, subcortical, and neuromodulatory inputs. Despite its obvious importance, surprisingly little is known about thalamic function in awake animals. Here, using intracellular and extracellular recordings in awake head-restrained mice, we investigate membrane potential dynamics and action potential firing in the two major thalamic nuclei related to whisker sensation, the ventral posterior medial nucleus (VPM) and the posterior medial group (Pom), which receive distinct inputs from brainstem and neocortex. We find heterogeneous state-dependent dynamics in both nuclei, with an overall increase in action potential firing during active states. Whisking increased putative lemniscal and corticothalamic excitatory inputs onto VPM and Pom neurons, respectively. A subpopulation of VPM cells fired spikes phase-locked to the whisking cycle during free whisking, and these cells may therefore signal whisker position. Our results suggest differential processing of whisking comparing thalamic nuclei at both sub- and supra-threshold levels.


Subject(s)
Membrane Potentials/physiology , Thalamus/physiology , Vibrissae/physiology , Action Potentials/physiology , Animals , Electroencephalography , Electromyography , Male , Mice , Mice, Inbred C57BL , Neocortex/cytology , Neocortex/physiology , Neurons/cytology , Neurons/physiology , Thalamus/cytology
5.
J Neurosci ; 33(17): 7130-44, 2013 Apr 24.
Article in English | MEDLINE | ID: mdl-23616523

ABSTRACT

The frequency and pattern of activity in the reciprocally connected GABAergic external globus pallidus (GPe) and glutamatergic subthalamic nucleus (STN) are closely related to motor function. Although phasic, unitary GPe-STN inputs powerfully pattern STN activity ex vivo, correlated GPe-STN activity is not normally observed in vivo. To test the hypothesis that the GPe's influence is constrained by short-term synaptic depression, unitary GPe-STN inputs were stimulated in rat and mouse brain slices at rates and in patterns that mimicked GPe activity in vivo. Together with connectivity estimates these data were then used to simulate GPe-STN transmission. Unitary GPe-STN synaptic connections initially generated large conductances and transmitted reliably. However, the amplitude and reliability of transmission declined rapidly (τ = 0.6 ± 0.5 s) to <10% of their initial values when connections were stimulated at the mean rate of GPe activity in vivo (33 Hz). Recovery from depression (τ = 17.3 ± 18.9 s) was also longer than pauses in tonic GPe activity in vivo. Depression was the result of the limited supply of release-ready vesicles and was in sharp contrast to Calyx of Held transmission, which exhibited 100% reliability. Injection of simulated GPe-STN conductances revealed that synaptic depression caused tonic, nonsynchronized GPe-STN activity to disrupt rather than abolish autonomous STN activity. Furthermore, synchronous inhibition of tonically active GPe-STN neurons or phasic activity of GPe-STN neurons reliably patterned STN activity through disinhibition and inhibition, respectively. Together, these data argue that the frequency and pattern of GPe activity profoundly influence its transmission to the STN.


Subject(s)
Globus Pallidus/physiology , Subthalamic Nucleus/physiology , Synaptic Transmission/physiology , Animals , Male , Mice , Mice, Inbred C57BL , Organ Culture Techniques , Random Allocation , Rats , Rats, Sprague-Dawley , Time Factors
6.
J Neurosci ; 30(5): 1832-8, 2010 Feb 03.
Article in English | MEDLINE | ID: mdl-20130192

ABSTRACT

Trigeminal sensory nuclei that give rise to ascending pathways of vibrissal information are heavily linked by intersubnuclear connections. This is the case, for instance, of the principal trigeminal nucleus, which receives strong inhibitory input from the caudal sector of the interpolaris subnucleus. Because this inhibitory input can gate the relay of sensory messages through the lemniscal pathway, a central issue in vibrissal physiology is how brain regions that project to the interpolaris control the activity of inhibitory cells. In the present study, we examined how corticotrigeminal neurons of the primary and second somatosensory cortical areas control the excitability of interpolaris cells. Results show that these two cortical areas exert a differential control over the excitability of projection cells and intersubnuclear interneurons, and that this control also involves the recruitment of inhibitory cells in the caudalis subnucleus. These results provide a basic circuitry for a mechanism of disinhibition through which the cerebral cortex can control the relay of sensory messages in the lemniscal pathway. It is proposed that top-down control of brainstem circuits is prompted by motor strategies, expectations, and motivational states of the animal.


Subject(s)
Motor Cortex/physiology , Somatosensory Cortex/physiology , Trigeminal Nuclei/physiology , Vibrissae/physiology , Animals , Interneurons/physiology , Male , Neural Pathways/physiology , Neurons/physiology , Rats , Rats, Sprague-Dawley
7.
Neuron ; 56(4): 714-25, 2007 Nov 21.
Article in English | MEDLINE | ID: mdl-18031687

ABSTRACT

Higher-order thalamic nuclei receive input from both the cerebral cortex and prethalamic sensory pathways. However, at rest these nuclei appear silent due to inhibitory input from extrathalamic regions, and it has therefore remained unclear how sensory gating of these nuclei takes place. In the rodent, the ventral division of the zona incerta (ZIv) serves as a relay station within the paralemniscal thalamocortical projection pathway for whisker-driven motor activity. Most, perhaps all, ZIv neurons are GABAergic, and recent studies have shown that these cells participate in a feedforward inhibitory circuit that blocks sensory transmission in the thalamus. The present study provides evidence that the stimulation of the vibrissa motor cortex suppresses vibrissal responses in ZIv via an intra-incertal GABAergic circuit. These results provide support for the proposal that sensory transmission operates via a top-down disinhibitory mechanism that is contingent on motor activity.


Subject(s)
Motor Cortex/physiology , Movement/physiology , Posterior Thalamic Nuclei/physiology , Subthalamus/physiology , Touch/physiology , Vibrissae/physiology , Action Potentials/physiology , Animals , Axons/physiology , Axons/ultrastructure , Biotin/analogs & derivatives , Dendrites/physiology , Dendrites/ultrastructure , Dextrans , Female , Male , Motor Cortex/anatomy & histology , Neural Inhibition/physiology , Neural Pathways/anatomy & histology , Neural Pathways/physiology , Neurons/cytology , Neurons/metabolism , Physical Stimulation , Posterior Thalamic Nuclei/anatomy & histology , Rats , Rats, Sprague-Dawley , Reaction Time/physiology , Somatosensory Cortex/physiology , Subthalamus/anatomy & histology , Synaptic Transmission/physiology , gamma-Aminobutyric Acid/metabolism
8.
J Neurosci ; 27(45): 12407-12, 2007 Nov 07.
Article in English | MEDLINE | ID: mdl-17989305

ABSTRACT

Three ascending pathways of information processing have been identified so far in the vibrissal system of rodents. In the ventral posterior medial nucleus of the thalamus, two of these pathways convey information through the core and tail of barrel-associated structures, called barreloids. The other pathway transits through the posterior group nucleus. The present study provides anatomical and electrophysiological evidence for the existence of an additional pathway that passes through the head of the barreloids. This pathway arises from multiwhisker-responsive cells in the principal trigeminal nucleus and differs from the classic lemniscal pathway, in that constituent thalamic cells have multiwhisker receptive field and receive corticothalamic input from lamina 6 of the vibrissa motor cortex. It is suggested that this pathway might be involved in relaying signals encoding phase of whisker motion during free whisking.


Subject(s)
Motor Cortex/physiology , Thalamus/physiology , Vibrissae/physiology , Animals , Male , Motor Cortex/chemistry , Neural Pathways/chemistry , Neural Pathways/physiology , Rats , Rats, Sprague-Dawley , Thalamus/chemistry , Vibrissae/chemistry
9.
Neuropsychopharmacology ; 32(6): 1232-41, 2007 Jun.
Article in English | MEDLINE | ID: mdl-17151599

ABSTRACT

Dopamine is involved in motivation, memory, and reward processing. However, it is not clear whether the activity of dopamine neurons is related or not to vigilance states. Using unit recordings in unanesthetized head restrained rats we measured the firing pattern of dopamine neurons of the ventral tegmental area across the sleep-wake cycle. We found these cells were activated during paradoxical sleep (PS) via a clear switch to a prominent bursting pattern, which is known to induce large synaptic dopamine release. This activation during PS was similar to the activity measured during the consumption of palatable food. Thus, as it does during waking in response to novelty and reward, dopamine could modulate brain plasticity and thus participate in memory consolidation during PS. By challenging the traditional view that dopamine is the only aminergic group not involved in sleep physiology, this study provides an alternative perspective that may be crucial for understanding the physiological function of PS and dream mentation.


Subject(s)
Dopamine/physiology , Neurons/physiology , Sleep, REM/physiology , Ventral Tegmental Area/physiology , Animals , Arousal/physiology , Dopamine/metabolism , Eating/physiology , Electroencephalography , Male , Neurons/metabolism , Rats , Rats, Sprague-Dawley , Sleep Stages/physiology , Ventral Tegmental Area/cytology , Ventral Tegmental Area/metabolism , Wakefulness/physiology
10.
J Physiol ; 573(Pt 3): 679-95, 2006 Jun 15.
Article in English | MEDLINE | ID: mdl-16613874

ABSTRACT

Through their widespread projections to the entire brain, dorsal raphe cells participate in many physiological functions and are associated with neuropsychiatric disorders. In previous studies, the width of action potentials was used as a criterion to identify putative serotonergic neurons, and to demonstrate that cells with broad spikes were more active in wakefulness, slowed down their activity in slow wave sleep and became virtually silent during paradoxical sleep. However, recent studies reported that about half of these presumed serotonergic cells were not immunoreactive for tyrosine hydroxylase. Here, we re-examine the electrophysiological properties of dorsal raphe cells across the sleep-wake cycle in rats by the extracellular recording of a large sample of single units (n = 770). We identified two major types of cells, which differ in spike waveform: a first population characterized by broad, mostly positive spikes, and a second one displaying symmetrical positive-negative spikes with a large distribution of spike durations (0.6-3.2 ms). Although we found classical broad-spike cells that were more active in wakefulness, we also found that about one-third of these cells increased or did not change their firing rate during sleep compared with wakefulness. Moreover, 62% of the latter cells were active in paradoxical sleep when most of raphe cells were silent. Such a diversity in the neuronal firing behaviour is important in the light of the recent controversy regarding the neurochemical identity of dorsal raphe cells exhibiting broad spikes. Our results also suggest that the dorsal raphe contains subpopulations of neurons with reciprocal activity across the sleep-wake cycle.


Subject(s)
Raphe Nuclei/physiology , Sleep/physiology , Wakefulness/physiology , Action Potentials , Animals , Electroencephalography , Electromyography , Electrophysiology , Male , Neck Muscles/innervation , Neck Muscles/physiology , Neurons/classification , Neurons/metabolism , Neurons/physiology , Raphe Nuclei/cytology , Raphe Nuclei/metabolism , Rats , Rats, Sprague-Dawley , Serotonin/metabolism , Sleep, REM , Time Factors
11.
J Neurosci ; 25(33): 7489-98, 2005 Aug 17.
Article in English | MEDLINE | ID: mdl-16107636

ABSTRACT

Sensory stimuli evoke strong responses in thalamic relay cells, which ensure a faithful relay of information to the neocortex. However, relay cells of the posterior thalamic nuclear group in rodents, despite receiving significant trigeminal input, respond poorly to vibrissa deflection. Here we show that sensory transmission in this nucleus is impeded by fast feedforward inhibition mediated by GABAergic neurons of the zona incerta. Intracellular recordings of posterior group neurons revealed that the first synaptic event after whisker deflection is a prominent inhibition. Whisker-evoked EPSPs with fast rise time and longer onset latency are unveiled only after lesioning the zona incerta. Excitation survives barrel cortex lesion, demonstrating its peripheral origin. Electron microscopic data confirm that trigeminal axons make large synaptic terminals on the proximal dendrites of posterior group cells and on the somata of incertal neurons. Thus, the connectivity of the system allows an unusual situation in which inhibition precedes ascending excitation resulting in efficient shunting of the responses. The dominance of inhibition over excitation strongly suggests that the paralemniscal pathway is not designed to relay inputs triggered by passive whisker deflection. Instead, we propose that this pathway operates through disinhibition, and that the posterior group forwards to the cerebral cortex sensory information that is contingent on motor instructions.


Subject(s)
Neural Inhibition/physiology , Neurons, Afferent/physiology , Thalamic Nuclei/physiology , Action Potentials/physiology , Afferent Pathways/physiology , Animals , Electric Stimulation/methods , Male , Rats , Rats, Sprague-Dawley , Time Factors , Vibrissae/physiology
12.
Eur J Neurosci ; 20(2): 392-402, 2004 Jul.
Article in English | MEDLINE | ID: mdl-15233749

ABSTRACT

The subthalamic nucleus (STN) has been implicated in movement disorders observed in Parkinson's disease because of its pathological mixed burst firing mode and hyperactivity. In physiological conditions, STN bursty pattern has been shown to be dependent on slow wave cortical activity. Indeed, cortical ablation abolished STN bursting activity in urethane-anaesthetized intact or dopamine depleted rats. Thus, glutamate afferents might be involved in STN bursting activity during slow wave sleep (SWS) when thalamic and cortical cells oscillate in a low-frequency range. The present work was aimed to test, on non-anaesthetized rats, if it was possible to regularize the SWS STN bursty pattern by microiontophoresis of kynurenate, a broad-spectrum glutamate ionotropic receptors antagonist. As glutamatergic effects might be masked by GABAergic inputs arriving tonically and during the entire sleep-wake cycle on STN neurons, kynurenate was also co-iontophoresed with bicuculline, a GABA(A) receptors antagonist. Kynurenate iontophoretic applications had a weak inhibitory effect on the discharge rate of STN neurons whatever the vigilance state, and did not regularize the SWS STN bursty pattern. But, the robust bursty bicuculline-induced pattern was impaired by kynurenate, which elicited the emergence of single spikes between remaining bursts. These data indicate that the bursty pattern exhibited by STN neurons specifically in SWS, does not seem to exclusively depend on glutamatergic inputs to STN cells. Furthermore, GABA(A) receptors may play a critical role in regulating the influence of excitatory inputs on STN cells.


Subject(s)
Action Potentials/drug effects , Excitatory Amino Acid Antagonists/pharmacology , Kynurenic Acid/pharmacology , Neurons/drug effects , Sleep/drug effects , Subthalamic Nucleus/cytology , Animals , Bicuculline/pharmacology , Dose-Response Relationship, Drug , Drug Interactions , Electroencephalography/drug effects , Electromyography/drug effects , GABA Antagonists/pharmacology , Glutamic Acid/pharmacology , Iontophoresis/methods , Male , Neurons/physiology , Rats , Rats, Sprague-Dawley , Sleep/physiology
13.
Eur J Pharmacol ; 459(1): 17-26, 2003 Jan 10.
Article in English | MEDLINE | ID: mdl-12505530

ABSTRACT

The aim of the present study was to compare, in chloral-hydrate anaesthetized rats, the alpha(2)-adrenergic properties of the selective 5-HT(1A) receptor agonist, alnespirone (S-20499), with those of buspirone, a 5-HT(1A) receptor agonist exhibiting potent alpha(2)-adrenoceptor antagonist properties via its principal metabolite, 1-(2-pyrimidinyl)-piperazine. Both locus coeruleus spontaneous firing activity and noradrenaline release in the medial prefrontal cortex were potently inhibited by the alpha(2)-adrenoceptor agonist clonidine, at a dose of 40 microg/kg (i.p.). Such an inhibition was neither prevented nor reversed by alnespirone (10 mg/kg, i.p.), while buspirone, at the same dose, potently antagonized the locus coeruleus inhibitory effects of clonidine. These data demonstrate that, in contrast with some aryl-piperazine compounds (such as buspirone), alnespirone, either on its own or via a possible metabolite such as buspirone, is devoid in vivo of significant alpha(2)-adrenoceptor antagonist properties.


Subject(s)
Buspirone/pharmacology , Locus Coeruleus/drug effects , Neurons/drug effects , Receptors, Serotonin/drug effects , Serotonin Receptor Agonists/pharmacology , Spiro Compounds/pharmacology , Animals , Clonidine/pharmacology , Electrophysiology , Locus Coeruleus/cytology , Locus Coeruleus/physiology , Male , Microdialysis , Neurons/physiology , Norepinephrine/metabolism , Prefrontal Cortex/drug effects , Prefrontal Cortex/metabolism , Rats , Rats, Sprague-Dawley , Receptors, Serotonin/physiology , Receptors, Serotonin, 5-HT1 , Time Factors
14.
J Neurosci ; 22(19): 8665-75, 2002 Oct 01.
Article in English | MEDLINE | ID: mdl-12351741

ABSTRACT

The subthalamic nucleus (STN) powerfully controls basal ganglia outputs and has been implicated in movement disorders observed in Parkinson's disease because of its pathological mixed burst firing mode and hyperactivity. A recent study suggested that reciprocally connected glutamatergic STN and GABAergic globus pallidus (GP) neurons act in vitro as a generator of bursting activity in basal ganglia. In vivo, we reported that GP neurons increased their firing rate in wakefulness (W) compared with slow-wave sleep (SWS) without any change in their random pattern. In contrast, STN neurons exhibited similar firing rates in W and SWS, with an irregular pattern in W and a bursty one in SWS. Thus, the pallidal GABAergic tone might control the STN pattern. This hypothesis was tested by mimicking such variations with microiontophoresis of GABA receptor ligands. GABA agonists specifically decreased the STN firing rate but did not affect its firing pattern. GABA(A) (but not GABA(B)) antagonists strongly enhanced the STN mean discharge rate during all vigilance states up to three to five times its basal activity. However, such applications did not change the typical W random pattern. When applied during SWS, GABA(A) antagonists strongly reinforced the spontaneous bursty pattern into a particularly marked one with instantaneous frequencies reaching 500-600 Hz. SWS-W transitions occurring during ongoing antagonist iontophoresis invariably disrupted the bursty pattern into a random one. Thus GABA(A) receptors play a critical, but not exclusive, role in regulating the excitatory STN influence on basal ganglia outputs.


Subject(s)
Neurons/physiology , Subthalamic Nucleus/physiology , Synaptic Transmission/physiology , gamma-Aminobutyric Acid/metabolism , Action Potentials/drug effects , Action Potentials/physiology , Animals , Circadian Rhythm/physiology , Electroencephalography/drug effects , Electromyography , GABA Agonists/pharmacology , GABA Antagonists/pharmacology , GABA-A Receptor Agonists , GABA-A Receptor Antagonists , GABA-B Receptor Agonists , GABA-B Receptor Antagonists , Iontophoresis , Male , Neurons/drug effects , Periodicity , Rats , Rats, Sprague-Dawley , Receptors, GABA-A/metabolism , Sleep/physiology , Subthalamic Nucleus/cytology , Subthalamic Nucleus/drug effects , Synaptic Transmission/drug effects , Wakefulness/physiology , gamma-Aminobutyric Acid/administration & dosage
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