Afferent renal nerve stimulation excites supraoptic vasopressin neurons

1985 ◽  
Vol 249 (3) ◽  
pp. R368-R371 ◽  
Author(s):  
T. A. Day ◽  
J. Ciriello

Single-unit recording experiments were performed in pentobarbital-anesthetized rats to investigate the effects of afferent renal nerve (ARN) stimulation on the activity of neurosecretory vasopressin cells of the supraoptic nucleus (SON). Neurosecretory SON cells were identified by antidromic invasion from the neurohypophysis and classified either as vasopressin (AVP) or oxytocin (OXY) secreting on the basis of their spontaneous activity patterns and response to activation of arterial baroreceptors. Fifty-three spontaneously active units were identified bilaterally in the SON: 40 putative AVP and 13 putative OXY neurons. Most putative AVP neurons (14/14 contralateral, 18/26 ipsilateral) were excited by ARN stimulation (mean onset latency 189 +/- 5 ms, mean response duration 237 +/- 17 ms). In contrast, ARN stimulation had no effect on the firing frequency of the 13 putative OXY neurons. These data indicate that sensory information originating in the kidney selectively alters the activity of SON AVP neurons and suggest that afferent information from the kidney is important in the coordination of neural and hormonal activity concerned with body fluid balance and the regulation of arterial pressure.

1988 ◽  
Vol 254 (3) ◽  
pp. R531-R543 ◽  
Author(s):  
M. M. Caverson ◽  
J. Ciriello

Experiments were done in alpha-chloralose-anesthetized, paralyzed, and artificially ventilated cats to determine the effect of afferent renal nerve (ARN) stimulation on the firing frequency of neurons in the paraventricular nucleus of the hypothalamus (PVH), whose axons project directly to the neurohypophysis (NH), and the contribution of these neurons to the pressor response elicited by ARN stimulation. In the first series of experiments, 474 single units were extracellularly recorded in the PVH region. Of these units 86 were antidromically excited by stimulation of the NH. Seventeen of the antidromic units (20%) responded orthodromically to ARN stimulation; 10 responded to ARN stimulation only, and 7 units responded to both ARN and buffer nerve stimulation. All PVH-NH-projecting neurons that responded to ARN stimulation were excited. In the second series the contribution of PVH neurons to the pressor response elicited by ARN stimulation was investigated in animals with the aortic depressor, carotid sinus, vagus, and cervical sympathetic nerves cut bilaterally. The ARN pressor response has previously been shown to be due to the activation of the sympathetic nervous system and to the release of arginine vasopressin (AVP). The primary and secondary (AVP component) components of the pressor response were attenuated by 51 and 69%, respectively, by bilateral injections of procaine hydrochloride into PVH or bilateral electrolytic lesions of PVH. Control injections of saline into PVH or electrolytic lesions of hypothalamic regions anterior, dorsal, or ventral to PVH did not alter the ARN pressor response. These experiments demonstrate that sensory information originating in renal receptors excites magnocellular neurosecretory neurons in PVH and suggest that this renal-paraventricular reflex loop may contribute to the elevated arterial pressure and AVP release during conditions when ARN are activated.


2015 ◽  
Vol 308 (9) ◽  
pp. H1103-H1111 ◽  
Author(s):  
Bo Xu ◽  
Hong Zheng ◽  
Xuefei Liu ◽  
Kaushik P. Patel

Renal denervation for the treatment of hypertension has proven to be successful; however, the underlying mechanism/s are not entirely clear. To determine if preautonomic neurons in the paraventricular nucleus (PVN) respond to afferent renal nerve (ARN) stimulation, extracellular single-unit recording was used to investigate the contribution of the rostral ventrolateral medulla (RVLM)-projecting PVN (PVN-RVLM) neurons to the response elicited during stimulation of ARN. In 109 spontaneously active neurons recorded in the PVN of anesthetized rats, 25 units were antidromically activated from the RVLM. Among these PVN-RVLM neurons, 84% (21/25) were activated by ARN stimulation. The baseline discharge rate was significantly higher in these neurons than those PVN-RVLM neurons not activated by ARN stimulation (16%, 4/25). The responsiveness of these neurons to baroreflex activation induced by phenylephrine and activation of cardiac sympathetic afferent reflex (CSAR) was also examined. Almost all of the PVN neurons that responded to ARN stimulation were sensitive to baroreflex (95%) and CSAR (100%). The discharge characteristics for nonevoked neurons (not activated by RVLM antidromic stimulation) showed that 23% of these PVN neurons responded to ARN stimulation. All the PVN neurons that responded to ARN stimulation were activated by N-methyl-d-aspartate, and these responses were attenuated by the glutamate receptor blocker AP5. These experiments demonstrated that sensory information originating in the kidney is integrated at the level of preautonomic neurons within the PVN, providing a novel mechanistic insight for use of renal denervation in the modulation of sympathetic outflow in disease states such as hypertension and heart failure.


1997 ◽  
Vol 272 (6) ◽  
pp. R1998-R2003 ◽  
Author(s):  
G. J. Kirouac ◽  
J. Ciriello

Extracellular single-unit recording experiments were done in alpha-chloralose-anesthetized, paralyzed, and artificially ventilated rats to investigate the effect of selective activation of arterial baroreceptors and stimulation of cardiovascular depressor sites in the nucleus of the solitary tract (NTS) on the discharge rate of neurons in the ventral tegmental area (VTA). Electrical stimulation of the aortic depressor nerve (ADN), which is known to carry aortic baroreceptor afferent fibers only, excited 12 of 21 (mean onset latency 42.4 +/- 8.8 ms) and inhibited 2 of 21 (mean onset latency 42.5 +/- 6.5 ms) single units in the VTA. The discharge rate of VTA units was also altered during the reflex activation of arterial baroreceptors by the acute rise in arterial pressure (AP) to systemic injections of phenylephrine (10 micrograms/kg i.v.): 12 of 44 units were excited and 15 of 44 were inhibited. Units that responded to either ADN stimulation or the reflex activation of the baroreflex also responded to stimulation of depressor sites in the NTS. An additional 12 units that were found in barodenervated controls to be responsive to NTS stimulation were nonresponsive to selective activation of arterial baroreceptors. These data indicate that cardiovascular afferent inputs modulate the activity of neurons in the VTA and suggest that changes in systemic AP may exert an effect on the activity of neurons involved in mesolimbic and mesocortical function.


2006 ◽  
Vol 96 (1) ◽  
pp. 71-85 ◽  
Author(s):  
J. Matthew Kittelberger ◽  
Bruce R. Land ◽  
Andrew H. Bass

Midbrain structures, including the periaqueductal gray (PAG), are essential nodes in vertebrate motor circuits controlling a broad range of behaviors, from locomotion to complex social behaviors such as vocalization. Few single-unit recording studies, so far all in mammals, have investigated the PAG's role in the temporal patterning of these behaviors. Midshipman fish use vocalization to signal social intent in territorial and courtship interactions. Evidence has implicated a region of their midbrain, located in a similar position as the mammalian PAG, in call production. Here, extracellular single-unit recordings of PAG neuronal activity were made during forebrain-evoked fictive vocalizations that mimic natural call types and reflect the rhythmic output of a known hindbrain–spinal pattern generator. The activity patterns of vocally active PAG neurons were mostly correlated with features related to fictive call initiation. However, spike trains in a subset of neurons predicted the duration of vocal output. Duration is the primary feature distinguishing call types used in different social contexts and these cells may play a role in directly establishing this temporal dimension of vocalization. Reversible, lidocaine inactivation experiments demonstrated the necessity of the midshipman PAG for fictive vocalization, whereas tract-tracing studies revealed the PAG's connectivity to vocal motor centers in the fore- and hindbrain comparable to that in mammals. Together, these data support the hypotheses that the midbrain PAG of teleosts plays an essential role in vocalization and is convergent in both its functional and structural organization to the PAG of mammals.


1998 ◽  
Vol 79 (4) ◽  
pp. 1746-1754 ◽  
Author(s):  
Andreas Scholz ◽  
Noboru Kuboyama ◽  
Gunter Hempelmann ◽  
Werner Vogel

Scholz, Andreas, Noboru Kuboyama, Gunter Hempelmann, and Werner Vogel. Complex blockade of TTX-resistant Na+ currents by lidocaine and bupivacaine reduce firing frequency in DRG neurons. J. Neurophysiol. 79: 1746–1754, 1998. Mechanisms of blockade of tetrodotoxin-resistant (TTXr) Na+ channels by local anesthetics in comparison with the sensitivity of tetrodotoxin-sensitive (TTXs) Na+ channels were studied by means of the patch-clamp technique in neurons of dorsal root ganglions (DRG) of rat. Half-maximum inhibitory concentration (IC50) for the tonic block of TTXr Na+ currents by lidocaine was 210 μmol/l, whereas TTXs Na+ currents showed five times lower IC50 of 42 μmol/l. Bupivacaine blocked TTXr and TTXs Na+ currents more potently with IC50 of 32 and 13 μmol/l, respectively. In the inactivated state, TTXr Na+ channel block by lidocaine showed higher sensitivities (IC50 = 60 μmol/l) than in the resting state underlying tonic blockade. The time constant τ1 of recovery of TTXr Na+ channels from inactivation at −80 mV was slowed from 2 to 5 ms after addition of 10 μmol/l bupivacaine, whereas the τ2 value of ∼500 ms remained unchanged. The use-dependent block of TTXr Na+ channels led to a progressive reduction of current amplitudes with increasing frequency of stimulation, which was ≤53% block at 20 Hz in 10 μmol/l bupivacaine and 81% in 100 μmol lidocaine. The functional importance of the use-dependent block was confirmed in current-clamp experiments where 30 μmol/l of lidocaine or bupivacaine did not suppress the single action potential but clearly reduced the firing frequency of action potentials again with stronger potency of bupivacaine. Because it was found that TTXr Na+ channels predominantly occur in smaller sensory neurons, their blockade might underlie the suppression of the sensation of pain. Different sensitivities and varying proportions of TTXr and TTXs Na+ channels could explain the known differential block in spinal anesthesia. We suggest that the frequency reduction at low local anesthetic concentrations may explain the phenomenon of paresthesia where sensory information are suppressed gradually during spinal anesthesia.


2019 ◽  
Vol 7 (2) ◽  
pp. 8 ◽  
Author(s):  
DiLoreto ◽  
Chute ◽  
Bryce ◽  
Srinivasan

The complete structure and connectivity of the Caenorhabditis elegans nervous system (“mind of a worm”) was first published in 1986, representing a critical milestone in the field of connectomics. The reconstruction of the nervous system (connectome) at the level of synapses provided a unique perspective of understanding how behavior can be coded within the nervous system. The following decades have seen the development of technologies that help understand how neural activity patterns are connected to behavior and modulated by sensory input. Investigations on the developmental origins of the connectome highlight the importance of role of neuronal cell lineages in the final connectivity matrix of the nervous system. Computational modeling of neuronal dynamics not only helps reconstruct the biophysical properties of individual neurons but also allows for subsequent reconstruction of whole-organism neuronal network models. Hence, combining experimental datasets with theoretical modeling of neurons generates a better understanding of organismal behavior. This review discusses some recent technological advances used to analyze and perturb whole-organism neuronal function along with developments in computational modeling, which allows for interrogation of both local and global neural circuits, leading to different behaviors. Combining these approaches will shed light into how neural networks process sensory information to generate the appropriate behavioral output, providing a complete understanding of the worm nervous system.


2018 ◽  
Vol 29 (7) ◽  
pp. 2815-2831 ◽  
Author(s):  
Y Audrey Hay ◽  
Jérémie Naudé ◽  
Philippe Faure ◽  
Bertrand Lambolez

Abstract Sensory processing relies on fast detection of changes in environment, as well as integration of contextual cues over time. The mechanisms by which local circuits of the cerebral cortex simultaneously perform these opposite processes remain obscure. Thalamic “specific” nuclei relay sensory information, whereas “nonspecific” nuclei convey information on the environmental and behavioral contexts. We expressed channelrhodopsin in the ventrobasal specific (sensory) or the rhomboid nonspecific (contextual) thalamic nuclei. By selectively activating each thalamic pathway, we found that nonspecific inputs powerfully activate adapting (slow-responding) interneurons but weakly connect fast-spiking interneurons, whereas specific inputs exhibit opposite interneuron preference. Specific inputs thereby induce rapid feedforward inhibition that limits response duration, whereas, in the same cortical area, nonspecific inputs elicit delayed feedforward inhibition that enables lasting recurrent excitation. Using a mean field model, we confirm that cortical response dynamics depends on the type of interneuron targeted by thalamocortical inputs and show that efficient recruitment of adapting interneurons prolongs the cortical response and allows the summation of sensory and contextual inputs. Hence, target choice between slow- and fast-responding inhibitory neurons endows cortical networks with a simple computational solution to perform both sensory detection and integration.


2021 ◽  
Author(s):  
Luigi Prisco ◽  
Stephan Hubertus Deimel ◽  
Hanna Yeliseyeva ◽  
Andre Fiala ◽  
Gaia Tavosanis

To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral neuron (APL) in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic Kenyon cells (KCs). Combining EM data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the Kenyon cells requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Luigi Prisco ◽  
Stephan Hubertus Deimel ◽  
Hanna Yeliseyeva ◽  
André Fiala ◽  
Gaia Tavosanis

To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral neuron (APL) in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic Kenyon cells (KCs). Combining EM data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the Kenyon cells requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.


2002 ◽  
Vol 87 (5) ◽  
pp. 2531-2541 ◽  
Author(s):  
Dongyuan Yao ◽  
Kensuke Yamamura ◽  
Noriyuki Narita ◽  
Ruth E. Martin ◽  
Gregory M. Murray ◽  
...  

The present study was undertaken to determine the firing patterns and the mechanoreceptive field (RF) properties of neurons within the face primary motor cortex (face-MI) in relation to chewing and other orofacial movements in the awake monkey. Of a total of 107 face-MI neurons recorded, 73 of 74 tested had activity related to chewing and 47 of 66 neurons tested showed activity related to a trained tongue task. Of the 73 chewing-related neurons, 52 (71.2%) showed clear rhythmic activity during rhythmic chewing. A total of 32 (43.8%) also showed significant alterations in activity in relation to the swallowing of a solid food (apple) bolus. Many of the chewing-related neurons (81.8% of 55 tested) had an orofacial RF, which for most was on the tongue dorsum. Tongue protrusion was evoked by intracortical microstimulation (ICMS) at most (63.6%) of the recording sites where neurons fired during the rhythmic jaw-opening phase, whereas tongue retraction was evoked by ICMS at most (66.7%) sites at which the neurons firing during the rhythmic jaw-closing phase were recorded. Of the 47 task-related neurons, 21 of 22 (95.5%) examined also showed chewing-related activity and 29 (61.7%) demonstrated significant alteration in activity in relation to the swallowing of a juice reward. There were no significant differences in the peak firing frequency among neuronal activities related to chewing, swallowing, or the task. These findings provide further evidence that face-MI may play an important role not only in trained orofacial movements but also in chewing as well as swallowing, including the control of tongue and jaw movements that occur during the masticatory sequence.


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