An intracellular study of time-dependent cardiovascular afferent interactions in nucleus tractus solitarius

S. W. Mifflin, R. B. Felder

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Abstract

1. We used a model of bilateral carotid sinus nerve (CSN) stimulation to investigate cardiovascular afferent interactions in nucleus tractus solitarius (NTS) in anesthetized cats. In some instances, interactions with afferent inputs from vagus or renal nerves were also examined. 2. Intracellular recordings were made from 88 NTS neurons activated by electrical stimulation of one or both CSNs. Excitatory (EPSPs), inhibitory (IPSPs), and combined excitatory and inhibitory (EPSP/IPSP) postsynaptic membrane potential responses to ipsilateral CSN stimulation were observed. The input from opposite CSN (30 of 34 neurons tested) or from other ipsilateral afferent sources (vagus nerve, 10 tested; renal nerve, 9 tested) was qualitatively the same as that from ipsilateral CSN. 3. Conditioning tests demonstrated that the response (EPSP, IPSP, or EPSP/IPSP) evoked by a test stimulus to one CSN was reduced in amplitude and/or duration by a prior stimulus (1-5 pulses) to the same 82 of 85 neurons) or to the opposite (30 or 37 neurons) CSN at conditioning intervals ranging from 50 to 550 ms. For cells in which CSN stimulation evoked an EPSP, this inhibitory interaction occurred with no change in resting membrane potential and no change in input resistance. For cells in which CSN stimulation evoked an IPSP, the inhibitory interaction persisted beyond the duration of CSN evoked IPSP. 4. We infrequently (3 cells) observed an excitatory interaction, in which the conditioning stimulus resulted in rhythmic depolarization of the neuron and a facilitated action potential response to an appropriately timed test stimulus. 5. During continuous CSN stimulation, postsynaptic potentials (PSPs) evoked by ipsilateral CSN were abolished in the steady state at stimulus frequencies of 5-20 Hz (n = 14). In cells that received a convergent input from contralateral CSN, the PSP evoked by contralateral CSN was usually (6 of 8 tested) abolished at lower stimulus frequencies (median difference = 5.0 Hz). 6. We conclude that individual NTS neurons frequently have the same PSP response to peripheral afferent inputs of different origins. Time-dependent interactions among cardiovascular afferent inputs that evoke PSPs of like kind may determine the nature of the integrated signal conveyed from NTS to subsequent cardiovascular related central nuclei. Both inhibitory and, less frequently, excitatory time-dependent interactions between cardiovascular afferent inputs occur. The absence of membrane potential changes associated with the inhibitory interaction suggests it may be mediated by disfacilitation.

Original languageEnglish
Pages (from-to)1798-1813
Number of pages16
JournalJournal of Neurophysiology
Volume59
Issue number6
DOIs
StatePublished - 1988

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