Time-dependent inhibition of hindlimb somatic afferent transmission within nucleus tractus solitarius: An in vivo intracellular recording study

G. M. Toney, Steve Wayne Mifflin

Research output: Contribution to journalArticle

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Abstract

In a previous study we demonstrated that hindlimb somatic afferent stimulation evokes excitatory responses from neurons in nucleus tractus solitarius. When paired electrical stimuli were delivered to hindlimb somatic afferents, the unit response to the second stimulus was significantly reduced compared with responses to the first. This temporal response pattern has been termed time-dependent inhibition since responses to the second stimulus recover as the interval separating the first and second stimuli is increased. To examine possible synaptic mechanisms for somatic afferent-evoked time-dependent inhibition, intracellular recordings were made from nucleus tractus solitarius neurons in anesthetized, paralysed rats. Skeletal muscle afferent fibers were activated by electrically stimulating the right tibial nerve in the hindlimb and neuronal responses recorded in the contralateral nucleus of the solitary tract. Time-dependent inhibition of tibial nerve-evoked unit discharge was studied using a conditioning-test stimulation procedure, with the first (conditioning) and second (test) stimuli separated by intervals of 50, 150 and 250 ms. In 49 units that responded to tibial nerve stimulation, 46 were excited and three were inhibited. Among units excited, 25 displayed a unimodal response that had an onset latency of 21.3 ± 5.9 ms. The remaining 21 units responded with a bimodal discharge pattern characterized by both a short-latency and a long-latency response. The onset latency of the early response was 23.7 ± 5.3 ms and was not statistically different from the unimodal response onset latency. The onset latency of the late response was 143 ± 23.9 ms. Conditioning-test stimulation protocols revealed that short-latency tibial nerve-evoked unit responses to test stimuli were significantly reduced when identical conditioning stimuli were delivered 50 ms earlier. In contrast, the long-latency component of the bimodal response was unaffected by conditioning stimuli. Conditioning-test intervals ≥150 ms were without inhibitory effect. Inhibitions observed in this study occurred without significant membrane hyperpolarization. Furthermore, the magnitude (area) and rate of depolarization of evoked excitatory postsynaptic potentials were both significantly reduced, to 50.7 ± 14.2 and 65.5 ± 15.5% of the control, respectively, at the 50 ms conditioning-test interval. In the present study, time-dependent inhibition of neuronal responses elicited by somatic afferent inputs to neurons in the nucleus of the solitary tract occurred without membrane hyperpolarization. Similar results have been reported, but only for visceral afferent inputs. The consistency of membrane responses to somatic and visceral inputs suggests that a similar synaptic mechanism(s) likely mediates time-dependent inhibition of both classes of afferent inputs. Thus, time-dependent inhibition, which appears to be a rather stereotype response among neurons in the nucleus of the solitary tract, could provide a mechanism for integrating functionally heterogenous inputs.

Original languageEnglish
Pages (from-to)445-453
Number of pages9
JournalNeuroscience
Volume68
Issue number2
DOIs
StatePublished - 1 Jan 1995

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Solitary Nucleus
Hindlimb
Tibial Nerve
Reaction Time
Neurons
Membranes
Visceral Afferents
Excitatory Postsynaptic Potentials
Skeletal Muscle Fibers
Conditioning (Psychology)
Inhibition (Psychology)

Cite this

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title = "Time-dependent inhibition of hindlimb somatic afferent transmission within nucleus tractus solitarius: An in vivo intracellular recording study",
abstract = "In a previous study we demonstrated that hindlimb somatic afferent stimulation evokes excitatory responses from neurons in nucleus tractus solitarius. When paired electrical stimuli were delivered to hindlimb somatic afferents, the unit response to the second stimulus was significantly reduced compared with responses to the first. This temporal response pattern has been termed time-dependent inhibition since responses to the second stimulus recover as the interval separating the first and second stimuli is increased. To examine possible synaptic mechanisms for somatic afferent-evoked time-dependent inhibition, intracellular recordings were made from nucleus tractus solitarius neurons in anesthetized, paralysed rats. Skeletal muscle afferent fibers were activated by electrically stimulating the right tibial nerve in the hindlimb and neuronal responses recorded in the contralateral nucleus of the solitary tract. Time-dependent inhibition of tibial nerve-evoked unit discharge was studied using a conditioning-test stimulation procedure, with the first (conditioning) and second (test) stimuli separated by intervals of 50, 150 and 250 ms. In 49 units that responded to tibial nerve stimulation, 46 were excited and three were inhibited. Among units excited, 25 displayed a unimodal response that had an onset latency of 21.3 ± 5.9 ms. The remaining 21 units responded with a bimodal discharge pattern characterized by both a short-latency and a long-latency response. The onset latency of the early response was 23.7 ± 5.3 ms and was not statistically different from the unimodal response onset latency. The onset latency of the late response was 143 ± 23.9 ms. Conditioning-test stimulation protocols revealed that short-latency tibial nerve-evoked unit responses to test stimuli were significantly reduced when identical conditioning stimuli were delivered 50 ms earlier. In contrast, the long-latency component of the bimodal response was unaffected by conditioning stimuli. Conditioning-test intervals ≥150 ms were without inhibitory effect. Inhibitions observed in this study occurred without significant membrane hyperpolarization. Furthermore, the magnitude (area) and rate of depolarization of evoked excitatory postsynaptic potentials were both significantly reduced, to 50.7 ± 14.2 and 65.5 ± 15.5{\%} of the control, respectively, at the 50 ms conditioning-test interval. In the present study, time-dependent inhibition of neuronal responses elicited by somatic afferent inputs to neurons in the nucleus of the solitary tract occurred without membrane hyperpolarization. Similar results have been reported, but only for visceral afferent inputs. The consistency of membrane responses to somatic and visceral inputs suggests that a similar synaptic mechanism(s) likely mediates time-dependent inhibition of both classes of afferent inputs. Thus, time-dependent inhibition, which appears to be a rather stereotype response among neurons in the nucleus of the solitary tract, could provide a mechanism for integrating functionally heterogenous inputs.",
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Time-dependent inhibition of hindlimb somatic afferent transmission within nucleus tractus solitarius : An in vivo intracellular recording study. / Toney, G. M.; Mifflin, Steve Wayne.

In: Neuroscience, Vol. 68, No. 2, 01.01.1995, p. 445-453.

Research output: Contribution to journalArticle

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