Volume 2 Supplement 1
Integral-differential calculus computations by short-term potentiation and depression in NTS-pontine pathways
- C-S Poon1
© BioMed Central Ltd 2001
Received: 2 August 2001
Published: 17 August 2001
Neural integrators are a class of neural networks that afford extended temporal summation of neural activity or, equivalently, low-pass frequency filtering of neurotransmission . In the respiratory system, a biphasic neural integrator in the carotid chemoreflex response is demonstrated by the classic short-term potentiation (STP) and afterdischarge of phrenic activity . Recently, a new class of neural networks called neural differentiators, which afford high-pass frequency filtering of afferent inputs through short-term depression (STD) of neurotransmission, has been identified in the vagal-carotid control of the expiratory off-switch . The differentiator response is characterized by: 1) a habituation-like adaptation to the vagal Hering-Breuer (HB) reflex lengthening or carotid chemore-flex shortening of expiratory duration; 2) secondary adaptive effects in the form of pontine-mediated and NMDA receptor-dependent post-stimulus rebound and recovery of these vagal or carotid (or hypoxia ) mediated responses.
To elucidate the mechanism of the habituation of the HB reflex, we obtained extracellular field potentials (FPs) in the medial and commissural regions of the nucleus tractus solitarius (NTS) evoked by electrical vagal stimulation (1 min) in urethane-anesthetized, paralyzed and mechanically ventilated rats (n =17) in vivo. FPs from vagal A-fibers (stimulus current, 20–70 μA, response latency, 4–5 ms) revealed a stimulus frequency-dependent (20–80 Hz) STD similar to the synaptic accommodation observed in vitro  and the habituation of HB reflex in vivo . FPs from C-fibers (150–350 μA, 20–45 ms) also demonstrated a frequency-dependent (5–20 Hz) STD during afferent activation but their amplitude remained depressed for >50 s post-stimulation. Microinjection of the NMDA receptor antagonist D-APV abolished the short-term memory following C-fiber activation but not the frequency-dependent STD with A- or C-fibers. The characteristics of the vagal A-and C-fiber mediated responses are reminiscent of the type I and type II NTS neurons found in vitro .
To elucidate the mechanism of the pontine-mediated adaptation of the HB reflex, we obtained extracellular recordings of pontine neuronal activity simultaneously with phrenic nerve recording during electrical vagal stimulation (1.5×T, 80 Hz, 1 min). Neurons with tonic and respiratory modulated activity were found within or near the parabrachialis (PB) and Kölliker-Fuse (KF) complex. Most tonic neurons in KF (n = 11) were depressed during and/or shortly after vagal stimulation that elicited the characteristic biphasic adaptation of the HB reflex in the phrenic activity, whereas most tonic neurons in medial PB (n = 22) were not affected. Activity of respiratory modulated neurons (n = 4) recorded in KF remained in phase with phrenic activity during vagal stimulation. Results showed that vagal input induced STD of tonic neurotransmission in KF.
These findings support a dual-process nonassociative learning model of integral-differential calculus computations in the brain  through activity-dependent STP and STD of neurotransmission in primary and secondary afferent pathways.
Supported by U.S. National Institutes of Health grants 1R01HL60064 and 1F31MH12697
- McCormick DA: Brain calculus: neural integration and persistent activity. Nat Neurosci. 2001, 4: 113-114. 10.1038/83917.PubMedView ArticleGoogle Scholar
- Poon C-S, Siniaia MS, Young DL, Eldridge FL: Short-term potentiation of carotid chemoreflex: an NMDAR-dependent neural integrator. Neuroreport. 1999, 10: 2261-2265. 10.1097/00001756-199908020-00007.PubMedView ArticleGoogle Scholar
- Poon C-S, Young DL, Siniaia MS: High-pass filtering of carotid-vagal influences on expiration in rat: role of N-methyl-D-aspartate receptors. Neurosci Lett. 2000, 284: 5-8. 10.1016/S0304-3940(00)00993-9.PubMedView ArticleGoogle Scholar
- Siniaia MS, Young DL, Poon C-S: Habituation and desensitization of the Hering-Breuer reflex in rat. J Physiol. 2000, 523: 479-491. 10.1111/j.1469-7793.2000.t01-1-00479.x.PubMedPubMed CentralView ArticleGoogle Scholar
- Coles SK, Dick TE: Neurones in the ventrolateral pons are required for post-hypoxic frequency decline in rats. J Physiol. 1996, 497: 79-94.PubMedPubMed CentralView ArticleGoogle Scholar
- Zhou Z, Poon C-S: Field potential analysis of synaptic transmission in spiking neurons in a sparse and irregular neuronal structure in vitro. J Neurosci Methods. 2000, 94: 193-203. 10.1016/S0165-0270(99)00144-2.PubMedView ArticleGoogle Scholar
- Zhou Z, Champagnat J, Poon C-S: Phasic and long-term depression in brainstem nucleus tractus solitarius neurons: differing roles of AMPA receptor desensitization. J Neurosci. 1997, 17: 5349-5356.PubMedGoogle Scholar
- Young DL, Siniaia MS, Poon C-S: Society for Neuroscience Annual Meeting, San Diego, USA. 2001Google Scholar