scholarly journals Physiological and anatomical properties of intramedullary projection neurons in rat rostral nucleus of the solitary tract

2013 ◽  
Vol 110 (5) ◽  
pp. 1130-1143 ◽  
Author(s):  
James A. Corson ◽  
Robert M. Bradley

The rostral nucleus of the solitary tract (rNTS), the first-order relay of gustatory information, not only transmits sensory information to more rostral brain areas but also connects to various brain stem sites responsible for orofacial reflex activities. While much is known regarding ascending projections to the parabrachial nucleus, intramedullary projections to the reticular formation (which regulate oromotor reflexive behaviors) remain relatively unstudied. The present study examined the intrinsic firing properties of these neurons as well as their morphological properties and synaptic connectivity with primary sensory afferents. Using in vitro whole cell patch-clamp recording, we found that intramedullary projection neurons respond to depolarizing current injection with either tonic or bursting action potential trains and subsets of these groups of neurons express A-type potassium, H-like, and postinhibitory rebound currents. Approximately half of the intramedullary projection neurons tested received monosynaptic innervation from primary afferents, while the rest received polysynaptic innervation, indicating that at least a subpopulation of these neurons can be directly activated by incoming sensory information. Neuron morphological reconstructions revealed that many of these neurons possessed numerous dendritic spines and that neurons receiving monosynaptic primary afferent input have a greater spine density than those receiving polysynaptic primary afferent input. These results reveal that intramedullary projection neurons represent a heterogeneous class of rNTS neurons and, through both intrinsic voltage-gated ion channels and local circuit interactions, transform incoming gustatory information into signals governing oromotor reflexive behaviors.

2018 ◽  
Vol 119 (3) ◽  
pp. 771-785
Author(s):  
Alison Boxwell ◽  
David Terman ◽  
Marion Frank ◽  
Yuchio Yanagawa ◽  
Joseph B. Travers

Neurons in the rostral nucleus of the solitary tract (rNST) convey taste information to both local circuits and pathways destined for forebrain structures. This nucleus is more than a simple relay, however, because rNST neurons differ in response rates and tuning curves relative to primary afferent fibers. To systematically study the impact of convergence and inhibition on firing frequency and breadth of tuning (BOT) in rNST, we constructed a mathematical model of its two major cell types: projection neurons and inhibitory neurons. First, we fit a conductance-based neuronal model to data derived from whole cell patch-clamp recordings of inhibitory and noninhibitory neurons in a mouse expressing Venus under the control of the VGAT promoter. We then used in vivo chorda tympani (CT) taste responses as afferent input to modeled neurons and assessed how the degree and type of convergence influenced model cell output frequency and BOT for comparison with in vivo gustatory responses from the rNST. Finally, we assessed how presynaptic and postsynaptic inhibition impacted model cell output. The results of our simulations demonstrated 1) increasing numbers of convergent afferents (2–10) result in a proportional increase in best-stimulus firing frequency but only a modest increase in BOT, 2) convergence of afferent input selected from the same best-stimulus class of CT afferents produced a better fit to real data from the rNST compared with convergence of randomly selected afferent input, and 3) inhibition narrowed the BOT to more realistically model the in vivo rNST data. NEW & NOTEWORTHY Using a combination of in vivo and in vitro neurophysiology together with conductance-based modeling, we show how patterns of convergence and inhibition interact in the rostral (gustatory) solitary nucleus to maintain signal fidelity. Although increasing convergence led to a systematic increase in firing frequency, tuning specificity was maintained with a pattern of afferent inputs sharing the best-stimulus compared with random inputs. Tonic inhibition further enhanced response fidelity.


2000 ◽  
Vol 84 (6) ◽  
pp. 3043-3055 ◽  
Author(s):  
DeForest Mellon

Intracellular electrophysiological studies of lateral protocerebral interneurons (LPIs) in the crayfish Procambarus clarkii have revealed convergence of multimodal sensory information onto these higher-level cells of the crustacean central olfactory pathway. Antennular stimulation by odors or electrical shocks generates excitatory-inhibitory sequences in some LPIs as does electrical or hydrodynamic stimulation of the antennae. Photic stimulation of the ipsilateral compound eye generates excitatory responses in LPIs, usually in the form of trains of impulse bursts that are timed to the peaks of the spontaneous oscillatory activity that characterizes these neurons. Focal electrical stimulation of the olfactory lobe, the termination point of antennular afferent input, or the accessory lobe, where higher-level visual and tactile inputs converge, also generates brief excitation and a delayed, prolonged inhibition in LPIs. Both phases of this activity are thought to be transmitted to the lateral protocerebrum via deutocerebral projection neurons, which have extensive dendritic arborizations in the olfactory lobe and the accessory lobe. The excitatory pathway is thought to synapse directly with target LPIs, whereas the inhibitory pathway is probably indirect and mediated through GABAergic interneurons within the lateral protocerebrum. There is evidence that both presynaptic and postsynaptic inhibition suppress activity in LPIs. Preliminary observations suggest that a small cluster of neurons adjacent to the hemi-ellipsoid body are inhibitory to LPI activity. Multimodal inhibitory and excitatory modulation of LPI activity may play a part in the contextual identification of odors in the crayfish olfactory system.


Author(s):  
Joseph B. Travers ◽  
Susan P. Travers

Gustatory and somatosensory information from the oral cavity is carried by afferent fibers in the fifth, seventh, and ninth cranial nerves to synapse in the rostral nucleus of the solitary tract (rNST). Incoming taste afferents from the three cranial nerves follow a rostral-caudal gradient within the nucleus, characterized by a gradual transition from neurons with anterior-to-posterior mouth receptive fields. This organization predisposes a pattern of convergence onto second-order neurons of afferents innervating adjacent or apposing receptors, while maintaining an orotopic representation. Although evidence for convergence between the seventh and ninth nerves is relatively infrequent in extracellular recordings, high-magnification confocal microscopy and patch recordings suggest the potential for considerable interaction between these cranial nerves. Overall, the convergence of afferent input functions to increase the overall firing rate, receptive field size, and responsiveness to a wider range of taste stimuli of second-order neurons than peripheral fibers.


2000 ◽  
Vol 84 (6) ◽  
pp. 2984-2997 ◽  
Author(s):  
Per Jenmalm ◽  
Seth Dahlstedt ◽  
Roland S. Johansson

Most objects that we manipulate have curved surfaces. We have analyzed how subjects during a prototypical manipulatory task use visual and tactile sensory information for adapting fingertip actions to changes in object curvature. Subjects grasped an elongated object at one end using a precision grip and lifted it while instructed to keep it level. The principal load of the grasp was tangential torque due to the location of the center of mass of the object in relation to the horizontal grip axis joining the centers of the opposing grasp surfaces. The curvature strongly influenced the grip forces required to prevent rotational slips. Likewise the curvature influenced the rotational yield of the grasp that developed under the tangential torque load due to the viscoelastic properties of the fingertip pulps. Subjects scaled the grip forces parametrically with object curvature for grasp stability. Moreover in a curvature-dependent manner, subjects twisted the grasp around the grip axis by a radial flexion of the wrist to keep the desired object orientation despite the rotational yield. To adapt these fingertip actions to object curvature, subjects could use both vision and tactile sensibility integrated with predictive control. During combined blindfolding and digital anesthesia, however, the motor output failed to predict the consequences of the prevailing curvature. Subjects used vision to identify the curvature for efficient feedforward retrieval of grip force requirements before executing the motor commands. Digital anesthesia caused little impairment of grip force control when subjects had vision available, but the adaptation of the twist became delayed. Visual cues about the form of the grasp surface obtained before contact was used to scale the grip force, whereas the scaling of the twist depended on visual cues related to object movement. Thus subjects apparently relied on different visuomotor mechanisms for adaptation of grip force and grasp kinematics. In contrast, blindfolded subjects used tactile cues about the prevailing curvature obtained after contact with the object for feedforward adaptation of both grip force and twist. We conclude that humans use both vision and tactile sensibility for feedforward parametric adaptation of grip forces and grasp kinematics to object curvature. Normal control of the twist action, however, requires digital afferent input, and different visuomotor mechanisms support the control of the grasp twist and the grip force. This differential use of vision may have a bearing to the two-stream model of human visual processing.


2008 ◽  
Vol 99 (3) ◽  
pp. 1267-1273 ◽  
Author(s):  
Takeshi Suwabe ◽  
Hideyuki Fukami ◽  
Robert M. Bradley

Salivary secretion results from reflex stimulation of autonomic neurons via afferent sensory information relayed to neurons in the rostral nucleus of the solitary tract (rNST), which synapse with autonomic neurons of the salivatory nuclei. We investigated the synaptic properties of the afferent sensory connection to neurons in the inferior salivatory nucleus (ISN) controlling the parotid and von Ebner salivary glands. Mean synaptic latency recorded from parotid gland neurons was significantly shorter than von Ebner gland neurons. Superfusion of GABA and glycine resulted in a concentration-dependent membrane hyperpolarization. Use of glutamate receptor antagonists indicated that both AMPA and N-methyl-d-aspartate (NMDA) receptors are involved in the evoked excitatory postsynaptic potentials (EPSPs). Inhibitory postsynaptic potential (IPSP) amplitude increased with higher intensity ST stimulation. Addition of the glycine antagonist strychnine did not affect the amplitude of the IPSPs significantly. The GABAA receptor antagonist, bicuculline (BMI) or mixture of strychnine and BMI abolished the IPSPs in all neurons. IPSP latency was longer than EPSP latency, suggesting that more than one synapse is involved in the inhibitory pathway. Results show that ISN neurons receive both excitatory and inhibitory afferent input mediated by glutamate and GABA respectively. The ISN neuron response to glycine probably derives from descending connections. Difference in the synaptic characteristics of ISN neurons controlling the parotid and von Ebner glands may relate to the different function of these two glands.


Development ◽  
1994 ◽  
Vol 120 (1) ◽  
pp. 13-24
Author(s):  
F. Johnson ◽  
S. W. Bottjer

Forebrain nuclei that control learned vocal behavior in zebra finches are anatomically distinct and interconnected by a simple pattern of axonal pathways. In the present study, we examined afferent regulation of neuronal survival during development of the robust nucleus of the archistriatum (RA). RA projection neurons form the descending motor pathway of cortical vocal-control regions and are believed to be directly involved in vocal production. RA receives afferent inputs from two other cortical regions, the lateral magnocellular nucleus of the anterior neostriatum (lMAN) and the higher vocal center (HVC). However, because the ingrowth of HVC afferent input is delayed, lMAN projection neurons provide the majority of afferent input to RA during early vocal learning. lMAN afferent input to RA is of particular interest because lMAN is necessary for vocal learning only during a restricted period of development. By making lesions of lMAN in male zebra finches at various stages of vocal development (20-60 days of age) and in adults (>90-days old), we asked whether the survival of RA neurons depends on lMAN afferent input, and if so whether such dependence changes over the course of vocal learning. The results showed that removal of lMAN afferent input induced the loss of over 40% of RA neurons among birds in early stages of vocal development (20 days of age). However, lMAN lesions lost the ability to induce RA neuron death among birds in later stages of vocal development (40 days of age and older). These findings indicate that many RA neurons require lMAN afferent input for their survival during early vocal learning, whereas the inability of lMAN lesions to induce RA neuron death in older birds may indicate a reduced requirement for afferent input or perhaps the delayed ingrowth of HVC afferent input (at approx. 35 days of age) provides an alternate source of afferent support. Removal of lMAN afferent input also dramatically increased the incidence of mitotic figures in RA, but only among 20-day-old birds at 2 days post-lesion. The early, acute nature of the mitotic events raises the possibility that cell division in RA may be regulated by lMAN afferent input.


1997 ◽  
Vol 272 (5) ◽  
pp. R1540-R1551 ◽  
Author(s):  
A. M. Schreihofer ◽  
G. E. Hoffman ◽  
A. F. Sved

Elimination of baroreceptor afferent input to the brain produced by chronic lesion of nucleus of the solitary tract (NTS) does not alter vasopressin (VP) release during hypotensive hemorrhage in conscious rats. To investigate whether the kidneys play a critical role in stimulating VP release during hemorrhage in chronic NTS-lesioned rats, we examined the effects of removing potential signals arising from the kidneys. In NTS-lesioned rats, nephrectomy or renal denervation, but not captopril injection, markedly attenuated (but did not abolish) hemorrhage-induced VP release. In contrast, none of these manipulations attenuated the VP response in NTS-intact rats. Hemorrhage increased plasma renin activity in control and NTS-lesioned rats, and this response was not altered by renal denervation. In rats with NTS lesions and renal denervation, hemorrhage induced the expression of Fos in hypothalamic magnocellular VP neurons in a pattern similar to that of hemorrhage in intact rats. Collectively, these results indicate that in chronic NTS-lesioned rats an afferent signal arising from the kidneys stimulates VP release during hemorrhage, possibly through renal nerves. However, with the NTS intact or after the selective removal of arterial baroreceptor inputs, such a role for the kidneys is not apparent. Furthermore, in the absence of the NTS and renal nerves, another signal generated by hypotensive hemorrhage continues to stimulate VP neurons.


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