Time-dependent inhibition of hindlimb somatic afferent inputs to nucleus tractus solitarius

G. M. Toney, Steve Wayne Mifflin

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Abstract

1. In the present investigation, experiments were performed in anesthetized, paralyzed rats (n = 40) to 1) identify and characterize responses of nucleus tractus solitarius (NTS) neurons to hind-limb somatic afferent inputs; 2) determine if hindlimb somatic inputs to NTS undergo time- dependent inhibition similar to that observed among visceral afferent inputs; and 3) determine if somatic afferent-evoked NTS unit discharge is altered by activation of baroreceptor afferent inputs. 2. Extracellular discharge was recorded from single NTS units following electrical stimulation (~500 μA) of the contralateral tibial nerve (TN) (skeletal muscle afferents), sural nerve (SN) (cutaneous afferents), and the ipsilateral aortic nerve (AN) (baroreceptor afferents). To identify possible time-dependent interactions; a paired pulse or conditioning-test stimulation procedure was employed. The activity of NTS neurons was recorded in response to test stimuli delivered to either TN or SN first in the absence and then in the presence of conditioning stimuli delivered to TN, SN, or AN 50, 150, and 250 ms before the test stimuli. 3. The results indicate that among 31 NTS cells activated by somatic nerve stimulation, 14 (~50%) received convergent inputs from both the TN and SN, 9 responded to TN stimulation only and 2 were activated by SN stimulation only. These cells were not spontaneously active but showed two distinct patterns of evoked discharge. Some had only a short latency, unimodal response that averaged 25.5 ± 2.0 (SE) ms for TN inputs (n = 21) and 27.9 ± 2.8 ms for SN inputs (n = 8). The remaining units responded with a bimodal discharge pattern consisting of an early or short latency response and a late or long latency response. The latency-to-peak discharge for the early response was 27.6 ± 1.5 ms for TN-evoked discharge and 27.8 ± 1.7 ms for SN-evoked activity, while the peak latency for the late response was 166.6 ± 20.4 ms for TN inputs and 160.4 ± 10.4 ms for SN inputs. Four other cells received convergent excitatory inputs from both TN and AN, and two cells were activated by TN, SN, and AN stimulation. The tonic level of activity among these 6 cells was significantly greater than that of units that did not receive an excitatory AN input. However, this spontaneous discharge showed no inherent rhythmicity nor was its pattern synchronous with the arterial pressure pulse. 4. Among NTS units activated by TN stimulation, the short latency excitatory response was significantly reduced (P < 0.05) by both TN (-75%) and SN (-50%) conditioning stimuli when the conditioning and test pulses were separated by 50 ms. In contrast, NTS unit responses to conditioning and test stimuli at intervals of 150 ms or longer were not significantly different. In contrast, conditioning stimuli had no effect on the long latency test response regardless of the time interval separating the conditioning and test stimuli. Nearly identical results were obtained for NTS unit responses to SN test stimuli. 5. NTS neuronal responses to TN (n = 7) and SN (n = 7) test stimuli were significantly reduced by conditioning stimuli applied to the AN. NTS unit activity evoked by SN stimulation was significantly reduced by AN stimulation at both the 50 ms (-34%) and 150 ms (-37%) conditioning-test intervals. Likewise, TN-evoked NTS unit discharge (n = 7) was significantly attenuated (-32%) following AN conditioning stimuli but only at the 50 ms interval. In contrast, conditioning stimuli applied to TN (n = 9) and SN (n = 7) had no effect on NTS discharge evoked by AN test stimuli. 6. These results indicate a significant degree of convergence among skeletal muscle and cutaneous afferents within NTS and demonstrate that time- dependent inhibition occurs among these somatic nerve inputs. Furthermore, baroreceptor afferent input to NTS can elicit time-dependent inhibition of somatic-nerve evoked NTS neuronal discharge. Taken together these data support the concept that NTS neurons act to integrate functionally distinct signals from a variety of receptive fields and could therefore participate in the production of integrated reflex responses to somatic afferent stimulation.

Original languageEnglish
Pages (from-to)63-71
Number of pages9
JournalJournal of neurophysiology
Volume72
Issue number1
DOIs
Publication statusPublished - 1 Jan 1994

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