Generation of the masticatory central pattern and its modulation by sensory feedback

doi:10.1016/j.pneurobio.2012.01.011

Progress in Neurobiology

Volume 96, Issue 3, March 2012, Pages 340-355

This review is dedicated to the memory of James P. Lund (1942–2009) whose tremendous contribution to the field will remain a monument.

https://doi.org/10.1016/j.pneurobio.2012.01.011 Get rights and content

Abstract

The basic pattern of rhythmic jaw movements produced during mastication is generated by a neuronal network located in the brainstem and referred to as the masticatory central pattern generator (CPG). This network composed of neurons mostly associated to the trigeminal system is found between the rostral borders of the trigeminal motor nucleus and facial nucleus. This review summarizes current knowledge on the anatomical organization, the development, the connectivity and the cellular properties of these trigeminal circuits in relation to mastication. Emphasis is put on a population of rhythmogenic neurons in the dorsal part of the trigeminal sensory nucleus. These neurons have intrinsic bursting capabilities, supported by a persistent Na⁺ current (I_NaP), which are enhanced when the extracellular concentration of Ca²⁺ diminishes. Presented evidence suggest that the Ca²⁺ dependency of this current combined with its voltage-dependency could provide a mechanism for cortical and sensory afferent inputs to the nucleus to interact with the rhythmogenic properties of its neurons to adjust and adapt the rhythmic output. Astrocytes are postulated to contribute to this process by modulating the extracellular Ca²⁺ concentration and a model is proposed to explain how functional microdomains defined by the boundaries of astrocytic syncitia may form under the influence of incoming inputs.

Highlights

► A population of rhythmically bursting neurons in the main sensory nucleus could form the core of the masticatory CPG. ► Bursting in these neurons depends on a persistent Na⁺ conductance modulated by the extracellular [Ca²⁺]. ► By controlling the extracellular [Ca²⁺], astrocytes could contribute to setting up conditions for bursting. ► Astrocytes of the main sensory nucleus respond to stimulation of afferent fibres and to NMDA application. ► Astrocytes could help synchronizing populations of neurons within functional domains defined by boundaries of their syncitia.

Introduction

Like many rhythmical movements, mastication is a vital function. It prepares food for digestion by breaking it down into pieces that can be swallowed. Masticatory deficiencies lead to poor digestion and inadequate dietary selection which in turn are associated to a number of cardiovascular, physical and cognitive problems. In addition to this obvious function, masticatory movements have also been associated to a number of other functions including mood control and learning and memory. Although, seemingly simple, the rhythmic orofacial movements produced during mastication require coordination of several jaw, facial and tongue muscles. As in other cyclic vital functions (e.g. respiration and locomotion), the basic rhythmic activity of these muscles is determined by a neuronal network referred to as central pattern generator (CPG). By definition, CPGs are capable of producing such rhythmic network activity even in absence of rhythmic inputs from descending or sensory afferents. That is not to say that these inputs do not play an important role in shaping the motor output. The masticatory CPG is located in the brainstem and involves mostly neurons in the vicinity of the trigeminal system. Although this has been known since the early 1970s, the precise organization of the trigeminal circuits that are involved and the basic mechanisms governing interactions between the cellular components remain largely unknown. Here, we will first describe the anatomical organization of these circuits, their inputs and outputs, and the factors controlling their development. We will then review recent findings on the cellular mechanisms governing rhythm generation and network operations in different contexts.

Section snippets

Anatomical organization of the trigeminal complex

Innervation of the orofacial area and masticatory muscles is insured by the Vth, VIIth, IXth and XIIth cranial nerves. The most important of these for chewing is the trigeminal nerve with its associated sensory, motor and premotor nuclei. Most of trigeminal primary sensory afferents have their cell bodies located in the trigeminal ganglion. Only those innervating jaw closing muscle spindles and about half of the mechanoreceptors innervating the periodontal ligaments are located centrally in the

Genetic factors

The nuclei described above all participate to some extent to the masticatory circuitry. During development, these nuclei expand from the 2nd to the 5th rhombomeres. In all vertebrates, early development of the hindbrain and segmentation into distinct rhombomeres (r) is under the influence of the Hox genes (Fraser et al., 1990, Kiecker and Lumsden, 2005, Lumsden, 1990, Lumsden and Keynes, 1989, Oury et al., 2006). Hoxa2 is expressed all along the hindbrain, except in r1, and only weakly in r2,

Cortical and sensory inputs to the central pattern generator

Although mastication is often considered to be stereotyped, there is a great deal of variability from cycle to cycle. Dellow and Lund (1971) have shown long ago that the basic pattern could be generated by the brainstem alone in a decerebrate paralysed animal. However, this variability of the movement envelope that occurs in physiological conditions can only be explained if one assumes that the brainstem circuits responsible for generating the basic rhythmic activity are subjected to some sort

Elements of the rhythm generator

The above mentioned transections studies in the “en bloc” brainstem preparations of neonate rats clearly show that a bloc extending from the rostral pole of NVmot to the rostral pole of NVII can still produce rhythmic activity in the trigeminal nerves upon addition of NMDA to the bath (Kogo et al., 1996, Tanaka et al., 1999). We have examined the intrinsic properties and connectivity of neurons comprised within this region and identified only one population of neurons with intrinsic properties

Network operation

We have now reviewed existing knowledge regarding inputs and outputs of the CPG and intrinsic properties of at least some of its rhythm generating neurons. However, we are still far from fully understanding how all of this is brought together to generate an adapted behaviour. How are the sensory and/or cortical inputs integrated to the intrinsic properties of the rhythmogenic neurons? How are the rhythmogenic neurons synchronized? Is the same population of rhythmogenic neurons active for all

Acknowledgements

This work was supported by Grants from the Canadian Institutes of Health Research and an infrastructure grant from the Fonds de la Recherche en Santé du Québec.

References (225)

D.S. Auld et al.
Glial cells and neurotransmission: an inclusive view of synaptic function
Neuron
(2003)
C.S. Ayer-Le Lievre et al.
The early development of cranial sensory ganglia and the potentialities of their component cells studied in quail–chick chimeras
Dev. Biol.
(1982)
K.V. Bayev et al.
Primary afferent depolarization evoked by the activity of spinal scratching generator
Neuroscience
(1981)
C. Buisseret-Delmas et al.
Projection from trigeminal nuclei to neurons of the mesencephalic trigeminal nucleus in rat
Neurosci. Lett.
(1997)
Z. Chang et al.
Distribution of premotoneurons for jaw-closing and jaw-opening motor nucleus receiving contacts from axon terminals of primary somatosensory cortical neurons in rats
Brain Res.
(2009)
J.C. Copray et al.
Dopaminergic afferents to the mesencephalic trigeminal nucleus of the rat: a light and electron microscope immunocytochemistry study
Brain Res.
(1990)
C.A. Del Negro et al.
Synaptically activated burst-generating conductances may underlie a group-pacemaker mechanism for respiratory rhythm generation in mammals
Prog. Brain Res.
(2010)
L. Devoize et al.
Organization of projections from the spinal trigeminal subnucleus oralis to the spinal cord in the rat: a neuroanatomical substrate for reciprocal orofacial–cervical interactions
Brain Res.
(2010)
R. Dubuc et al.
Rhythmic antidromic discharges of single primary afferents recorded in cut dorsal root filaments during locomotion in the cat
Brain Res.
(1985)
S. Enomoto et al.
The effects of cortical ablation on mastication in the rabbit
Neurosci. Lett.
(1987)

C.A. Fornal et al.

A subgroup of dorsal raphe serotonergic neurons in the cat is strongly activated during oral–buccal movements

Brain Res.

(1996)

P. Gilardi et al.

Krox-20: a candidate gene for the regulation of pattern formation in the hindbrain

Biochimie

(1991)

R.M. Harris-Warrick

General principles of rhythmogenesis in central pattern generator networks

Prog. Brain Res.

(2010)

N. Hatanaka et al.

Direct projections from the magnocellular division of the basal nucleus of the amygdala to the principal part of the cortical masticatory area in the macaque monkey

Brain Res.

(2000)

S. Hockfield et al.

An anatomical demonstration of projections to the medullary dorsal horn (trigeminal nucleus caudalis) from rostral trigeminal nuclei and the contralateral caudal medulla

Brain Res.

(1982)

C. Iida et al.

Corticofugal direct projections to primary afferent neurons in the trigeminal mesencephalic nucleus of rats

Neuroscience

(2010)

N. Inagaki et al.

The histaminergic innervation of the mesencephalic nucleus of the trigeminal nerve in rat brain: a light and electron microscopical study

Brain Res.

(1987)

A. Iriki et al.

Feeding behavior in mammals: corticobulbar projection is reorganized during conversion from sucking to chewing

Brain Res. Dev. Brain Res.

(1988)

K. Ishihama et al.

Oral-motor patterns of rhythmic trigeminal activity generated in fetal rat brainstem in vitro

Brain Res. Dev. Brain Res.

(2003)

K. Ishihama et al.

NR3 protein expression in trigeminal neurons during postnatal development

Brain Res.

(2006)

T.D. Jacquin et al.

Reorganization of pontine rhythmogenic neuronal networks in Krox-20 knockout mice

Neuron

(1996)

R.S. Johansson et al.

Microelectrode recordings from human oral mechanoreceptors

Brain Res.

(1976)

C. Kanaka et al.

The differential expression patterns of messenger RNAs encoding K–Cl cotransporters (KCC1,2) and Na–K–2Cl cotransporter (NKCC1) in the rat nervous system

Neuroscience

(2001)

H. Koizumi et al.

Differential discharge patterns of rhythmical activity in trigeminal motoneurons during fictive mastication and respiration in vitro

Brain Res. Bull.

(2002)

A. Kolta et al.

Modulation of rhythmogenic properties of trigeminal neurons contributing to the masticatory CPG

Prog. Brain Res.

(2010)

W.M. al-Ghoul et al.

Orderly migration of neurons to the principal sensory nucleus of the trigeminal nerve of the rat

J. Comp. Neurol.

(1993)

C. Alzheimer et al.

Postnatal development of a persistent Na⁺ current in pyramidal neurons from rat sensorimotor cortex

J. Neurophysiol.

(1993)

F. Amzica et al.

Spatial buffering during slow and paroxysmal sleep oscillations in cortical networks of glial cells in vivo

J. Neurosci.

(2002)

K. Appenteng et al.

Behavior of cutaneous mechanoreceptors recorded in mandibular division of Gasserian ganglion of the rabbit during movements of lower jaw

J. Neurophysiol.

(1982)

G.M. Ardran et al.

A cineradiographic study of bottle feeding

Br. J. Radiol.

(1958)

D. Arsenault et al.

Developmental remodelling of the lemniscal synapse in the ventral basal thalamus of the mouse

J. Physiol.

(2006)

T. Athanassiadis et al.

Physiological characterization, localization and synaptic inputs of bursting and nonbursting neurons in the trigeminal principal sensory nucleus of the rat

Eur. J. Neurosci.

(2005)

R. Azouz et al.

Ionic basis of spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells

J. Physiol.

(1996)

L. Ballerini et al.

Pharmacological block of the electrogenic sodium pump disrupts rhythmic bursting induced by strychnine and bicuculline in the neonatal rat spinal cord

J. Neurophysiol.

(1997)

Y. Ben-Ari

Excitatory actions of gaba during development: the nature of the nurture

Nat. Rev. Neurosci.

(2002)

K.M. Bennett et al.

Corticomotoneuronal contribution to the fractionation of muscle activity during precision grip in the monkey

J. Neurophysiol.

(1996)

A.P. Bernier et al.

Effect of the stimulation of sensory inputs on the firing of neurons of the trigeminal main sensory nucleus in the rat

J. Neurophysiol.

(2010)

M.J. Bourque et al.

Properties and interconnections of trigeminal interneurons of the lateral pontine reticular formation in the rat

J. Neurophysiol.

(2001)

I.A. Boyd

The histological structure of the receptors in the knee-joint of the cat correlated with their physiological response

J. Physiol.

(1954)

F. Bremer

Physiologie nerveuse de la mastication chez le chat et le lapin

Arch. Int. Physiol.

(1923)

F. Brocard et al.

Emergence of intrinsic bursting in trigeminal sensory neurons parallels the acquisition of mastication in weanling rats

J. Neurophysiol.

(2006)

T. Brown

The intrinsic factors in the act of progression in the mammal

Proc. R. Soc. Lond. B Biol. Sci.

(1911)

T.G. Brown

On the nature of the fundamental activity of the nervous centres: together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system

J. Physiol.

(1914)

N.F. Capra et al.

Central connections of trigeminal primary afferent neurons: topographical and functional considerations

Crit. Rev. Oral Biol. Med.

(1992)

N.F. Capra et al.

Distribution and central projections of primary afferent neurons that innervate the masseter muscle and mandibular periodontium: a double-label study

J. Comp. Neurol.

(1989)

M.B. Carpenter

The dorsal trigeminal tract in the rhesus monkey

J. Anat.

(1957)

S. Chen et al.

A transitional period of Ca²⁺-dependent spike afterdepolarization and bursting in developing rat CA1 pyramidal cells

J. Physiol.

(2005)

S. Chevallier et al.

Cholinergic control of excitability of spinal motoneurones in the salamander

J. Physiol.

(2006)

J.R. Colley et al.

Sucking and swallowing in infants

Br. Med. J.

(1958)

W.E. Crill

Persistent sodium current in mammalian central neurons

Annu. Rev. Physiol.

(1996)

Cited by (95)

Sensorimotor integration in cranial muscles tested by short- and long-latency afferent inhibition
2024, Clinical Neurophysiology
To compressively investigate sensorimotor integration in the cranial-cervical muscles in healthy adults.
Short- (SAI) and long-latency afferent (LAI) inhibition were probed in the anterior digastric (AD), the depressor anguli oris (DAO) and upper trapezius (UT) muscles. A transcranial magnetic stimulation pulse over primary motor cortex was preceded by peripheral stimulation delivered to the trigeminal, facial and accessory nerves using interstimulus intervals of 15–25 ms and 100–200 ms for SAI and LAI respectively.
In the AD, both SAI and LAI were detected following trigeminal nerve stimulation, but not following facial nerve stimulation. In the DAO, SAI was observed only following trigeminal nerve stimulation, while LAI depended only on facial nerve stimulation, only at an intensity suprathreshold for the compound motor action potential (cMAP). In the UT we could only detect LAI following accessory nerve stimulation at an intensity suprathreshold for a cMAP.
The results suggest that integration of sensory inputs with motor output is profoundly influenced by the type of sensory afferent involved and by the functional role played by the target muscle.
Data indicate the importance of taking into account the sensory receptors involved as well as the function of the target muscle when studying sensorimotor integration, both in physiological and neurological conditions.
The coordination of chewing
2023, Current Opinion in Neurobiology
Feeding behavior involves a complex organization of neural circuitry and interconnected pathways between the cortex, the brainstem, and muscles. Elevated synchronicity is required starting from the moment the animal brings the food to its mouth, chews, and initiates subsequent swallowing. Moreover, orofacial sensory and motor systems are coordinated in a way to optimize movement patterns as a result of integrating information from premotor neurons. Recent studies have uncovered significant discoveries employing various and creative techniques in order to identify key components in these vital functions. Here, we attempt to provide a brief overview of our current knowledge on orofacial systems. While our focus will be on recent breakthroughs regarding the masticatory machinery, we will also explore how it is sometimes intertwined with other functions, such as swallowing and limb movement.
Administration of amyloid-β oligomer to the buccal ganglia may reduce food intake and cholinergic synaptic responses within the feeding neural circuit in Aplysia kurodai
2023, Neuroscience Research
Anorexia is a behavioral change caused by functional brain disorders in patients with Alzheimer’s disease (AD). Amyloid-β (1–42) oligomers (o-Aβ) are possible causative agents of AD that impair signaling via synaptic dysfunction. In this study, we used Aplysia kurodai to study functional disorders of the brain through o-Aβ. Administration of o-Aβ to the buccal ganglia (feeding brain for oral movements) by surgical treatment significantly reduced food intake for at least five days. Furthermore, we explored the effects of o-Aβ on the synaptic function in the feeding neural circuit, focusing on a specific inhibitory synaptic response in jaw-closing motor neurons produced by cholinergic buccal multi-action neurons because we recently found that this cholinergic response decreases with aging, which is consistent with the cholinergic hypothesis for aging. Administration of o-Aβ to the buccal ganglia significantly reduced the synaptic response within minutes, whereas administration of amyloid-β (1–42) monomers did not. These results suggest that o-Aβ may impair the cholinergic synapses, even in Aplysia, which is consistent with the cholinergic hypothesis for AD.
Intrinsic properties and synaptic connectivity of Phox2b-expressing neurons in rat rostral parvocellular reticular formation
2022, Neuroscience Research
The paired-like homeobox 2b gene (Phox2b) is critical for the development of the autonomic nervous system. We have previously demonstrated the distinct characteristics of Phox2b-expressing (Phox2b⁺) neurons in the reticular formation dorsal to the trigeminal motor nucleus (RdV), which are likely related to jaw movement regulation. In this study, we focused on Phox2b⁺ neurons in the rostral parvocellular reticular formation (rPCRt), a critical region for controlling orofacial functions, using 2–11-day-old Phox2b-EYFP rats. Most Phox2b⁺ rPCRt neurons were glutamatergic, but not GABAergic or glycinergic. Approximately 65 % of Phox2b⁺ rPCRt neurons fired at a low frequency, and approximately 24 % of Phox2b⁺ rPCRt neurons fired spontaneously, as opposed to Phox2b⁺ RdV neurons. Stimulation of the RdV evoked inward postsynaptic currents in more than 50 % of Phox2b⁺ rPCRt neurons, while only one Phox2b⁺ rPCRt neuron responded to stimulation of the nucleus of the solitary tract. Five of the 10 Phox2b⁺ neurons sent their axons that ramified within the trigeminal motor nucleus (MoV). Of these, the axons of the two neurons terminated within both the MoV and rPCRt. Our findings suggest that Phox2b⁺ rPCRt neurons have distinct electrophysiological and synaptic properties that may be involved in the motor control of feeding behavior.
Pathophysiological mechanisms of oromandibular dystonia
2022, Clinical Neurophysiology
Citation Excerpt :
Table 3 reports the different forms of OMD according to the etiological axis of dystonia classification (Albanese et al., 2013) (Table 3). The muscles involved in OMD include jaw-closing (masseter, temporal, lateral, and medial pterygoid) and jaw-opening (digastric) muscles innervated by trigeminal nerves (Morquette et al., 2012). The motor nucleus of trigeminal nerves (Devoize et al., 2010; Guy et al., 2005; Westberg et al., 1998; Yatim et al., 1996; Zhang, 1998) receives input from bilateral corticobulbar fibers and interneurons from the peritrigeminal area (Morquette et al., 2012).
Oromandibular dystonia (OMD) is a rare form of focal idiopathic dystonia. OMD was clinically identified at the beginning of the 20th century, and the main clinical features have been progressively described over the years. However, OMD has several peculiarities that still remain unexplained, including the high rate of oral trauma, which is often related to the onset of motor symptoms. The purpose of this paper was to formulate a hypothesis regarding the pathophysiology of OMD, starting from the neuroanatomical basis of the masticatory and facial systems and highlighting the features that differentiate this condition from other forms of focal idiopathic dystonia. We provide a brief review of the clinical and etiological features of OMD as well as neurophysiological and neuroimaging findings obtained from studies in patients with OMD. We discuss possible pathophysiological mechanisms underlying OMD and suggest that abnormalities in sensory input processing may play a prominent role in OMD pathophysiology, possibly triggering a cascade of events that results in sensorimotor cortex network dysfunction. Finally, we identify open questions that future studies should address, including the effect of abnormal sensory input processing and oral trauma on the peculiar neurophysiological abnormalities observed in OMD.
Postnatal Maturation of Glutamatergic Inputs onto Rat Jaw-closing and Jaw-opening Motoneurons
2022, Neuroscience
Motoneurons that innervate the jaw-closing and jaw-opening muscles play a critical role in oro-facial behaviors, including mastication, suckling, and swallowing. These motoneurons can alter their physiological properties through the postnatal period during which feeding behavior shifts from suckling to mastication; however, the functional synaptic properties of developmental changes in these neurons remain unknown. Thus, we explored the postnatal changes in glutamatergic synaptic transmission onto the motoneurons that innervate the jaw-closing and jaw-opening musculatures during early postnatal development in rats. We measured miniature excitatory postsynaptic currents (mEPSCs) mediated by non-NMDA receptors (non-NMDA mEPSCs) and NMDA receptors in the masseter and digastric motoneurons. The amplitude, frequency, and rise time of non-NMDA mEPSCs remained unchanged among postnatal day (P)2–5, P9–12, and P14–17 age groups in masseter motoneurons, whereas the decay time dramatically decreased with age. The properties of the NMDA mEPSCs were more predominant at P2–5 masseter motoneurons, followed by reduction as neurons matured. The decay time of NMDA mEPSCs of masseter motoneurons also shortened remarkably across development. Furthermore, the proportion of NMDA/non-NMDA EPSCs induced in response to the electrical stimulation of the supratrigeminal region was quite high in P2–5 masseter motoneurons, and then decreased toward P14–17. In contrast to masseter motoneurons, digastric motoneurons showed unchanged properties in non-NMDA and NMDA EPSCs throughout postnatal development. Our results suggest that the developmental patterns of non-NMDA and NMDA receptor-mediated inputs vary among jaw-closing and jaw-opening motoneurons, possibly related to distinct roles of respective motoneurons in postnatal development of feeding behavior.

View all citing articles on Scopus

View full text

Generation of the masticatory central pattern and its modulation by sensory feedback

Abstract

Highlights

Introduction

Section snippets

Anatomical organization of the trigeminal complex

Genetic factors

Cortical and sensory inputs to the central pattern generator

Elements of the rhythm generator

Network operation

Acknowledgements

Neuron

Dev. Biol.

Neuroscience

Neurosci. Lett.

Brain Res.

Brain Res.

Prog. Brain Res.

Brain Res.

Brain Res.

Neurosci. Lett.

Brain Res.

Biochimie

Prog. Brain Res.

Brain Res.

Brain Res.

Neuroscience

Brain Res.

Brain Res. Dev. Brain Res.

Brain Res. Dev. Brain Res.

Brain Res.

Neuron

Brain Res.

Neuroscience

Brain Res. Bull.

Prog. Brain Res.

Orderly migration of neurons to the principal sensory nucleus of the trigeminal nerve of the rat

J. Comp. Neurol.

Postnatal development of a persistent Na+ current in pyramidal neurons from rat sensorimotor cortex

J. Neurophysiol.

Spatial buffering during slow and paroxysmal sleep oscillations in cortical networks of glial cells in vivo

J. Neurosci.

Behavior of cutaneous mechanoreceptors recorded in mandibular division of Gasserian ganglion of the rabbit during movements of lower jaw

J. Neurophysiol.

A cineradiographic study of bottle feeding

Br. J. Radiol.

Developmental remodelling of the lemniscal synapse in the ventral basal thalamus of the mouse

J. Physiol.

Physiological characterization, localization and synaptic inputs of bursting and nonbursting neurons in the trigeminal principal sensory nucleus of the rat

Eur. J. Neurosci.

Ionic basis of spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells

J. Physiol.

Pharmacological block of the electrogenic sodium pump disrupts rhythmic bursting induced by strychnine and bicuculline in the neonatal rat spinal cord

J. Neurophysiol.

Excitatory actions of gaba during development: the nature of the nurture

Nat. Rev. Neurosci.

Corticomotoneuronal contribution to the fractionation of muscle activity during precision grip in the monkey

J. Neurophysiol.

Effect of the stimulation of sensory inputs on the firing of neurons of the trigeminal main sensory nucleus in the rat

J. Neurophysiol.

Properties and interconnections of trigeminal interneurons of the lateral pontine reticular formation in the rat

J. Neurophysiol.

The histological structure of the receptors in the knee-joint of the cat correlated with their physiological response

J. Physiol.

Physiologie nerveuse de la mastication chez le chat et le lapin

Arch. Int. Physiol.

Emergence of intrinsic bursting in trigeminal sensory neurons parallels the acquisition of mastication in weanling rats

J. Neurophysiol.

The intrinsic factors in the act of progression in the mammal

Proc. R. Soc. Lond. B Biol. Sci.

On the nature of the fundamental activity of the nervous centres: together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system

J. Physiol.

Central connections of trigeminal primary afferent neurons: topographical and functional considerations

Crit. Rev. Oral Biol. Med.

Distribution and central projections of primary afferent neurons that innervate the masseter muscle and mandibular periodontium: a double-label study

J. Comp. Neurol.

The dorsal trigeminal tract in the rhesus monkey

J. Anat.

A transitional period of Ca2+-dependent spike afterdepolarization and bursting in developing rat CA1 pyramidal cells

J. Physiol.

Postnatal development of a persistent Na⁺ current in pyramidal neurons from rat sensorimotor cortex

A transitional period of Ca²⁺-dependent spike afterdepolarization and bursting in developing rat CA1 pyramidal cells