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The Journal of Neurophysiology Vol. 85 No. 5 May 2001, pp. 2213-2223
Copyright ©2001 by the American Physiological Society
Department of Physiology and Pharmacology, Oregon Health Sciences University, Portland, Oregon 97201-3098
Doyle, Mark W. and
Michael C. Andresen.
Reliability of Monosynaptic Sensory Transmission in Brain Stem
Neurons In Vitro. J. Neurophysiol. 85: 2213-2223, 2001. The timing of events within the
nervous system is a critical feature of signal processing and
integration. In neurotransmission, the synaptic latency, the time
between stimulus delivery and appearance of the synaptic event, is
generally thought to be directly related to the complexity of that
pathway. In horizontal brain stem slices, we examined synaptic latency
and its shock-to-shock variability (synaptic jitter) in medial nucleus
tractus solitarius (NTS) neurons in response to solitary tract (ST)
electrical activation. Using a visualized patch recording approach, we
activated ST 1-3 mm from the recorded neuron with short trains
(50-200 Hz) and measured synaptic currents under voltage clamp.
Latencies ranged from 1.5 to 8.6 ms, and jitter values (SD of
intraneuronal latency) ranged from 26 to 764 µs (n = 49). Surprisingly, frequency of synaptic failure was not correlated
with either latency or jitter (P > 0.147;
n = 49). Despite conventional expectations, no clear
divisions in latency were found from the earliest arriving excitatory
postsynaptic currents (EPSCs) to late pharmacologically polysynaptic
responses. Shortest latency EPSCs (<3 ms) were mediated by
non-N-methyl-D-aspartate (non-NMDA) glutamate
receptors. Longer latency responses were a mix of excitatory and
inhibitory currents including non-NMDA EPSCs and GABAa
receptor-mediated currents (IPSC). All synaptic responses exhibited
prominent frequency-dependent depression. In a subset of neurons, we
labeled sensory boutons by the anterograde fluorescent tracer, DiA,
from aortic nerve baroreceptors and then recorded from anatomically
identified second-order neurons. In identified second-order NTS
neurons, ST activation evoked EPSCs with short to moderate latency
(1.9-4.8 ms) but uniformly minimal jitter (31 to 61 µs) that were
mediated by non-NMDA receptors but had failure rates as high as 39%.
These monosynaptic EPSCs in identified second-order neurons were
significantly different in latency and jitter than GABAergic IPSCs
(latency, 2.95 ± 0.71 vs. 5.56 ± 0.74 ms, mean ± SE, P = 0.027; jitter, 42.3 ± 6.5 vs. 416.3 ± 94.4 µs, P = 0.013, n = 4, 6, respectively), but failure rates were similar (27.8 ± 9.0 vs. 9.7 ± 4.4%, P = 0.08, respectively). Such
results suggest that jitter and not absolute latency or failure rate is
the most reliable discriminator of mono- versus polysynaptic pathways.
The results suggest that brain stem sensory pathways may differ in
their principles of integration compared with cortical models and that
this importantly impacts synaptic performance. The unique performance
properties of the sensory-NTS pathway may reflect stronger axosomatic
synaptic processing in brain stem compared with dendritically weighted
models typical in cortical structures and thus may reflect very
different strategies of spatio-temporal integration in this NTS region
and for autonomic regulation.
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