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Journal of Neuroscience, Vol 14, 1176-1194, Copyright © 1994 by Society for Neuroscience
Giant neurons in the rat reticular formation: a sensorimotor interface in the elementary acoustic startle circuit?
K Lingenhohl and E Friauf
Department of Animal Physiology, University of Tubingen, Germany.
The mammalian acoustic startle response (ASR) is a relatively simple motor
response that can be elicited by sudden and loud acoustic stimuli. The ASR
shows several forms of plasticity, such as habituation, sensitization, and
prepulse inhibition, thereby making it an interesting model for studying
the underlying neuronal mechanisms. Among the neurons that compose the
elementary startle circuit are giant neurons in the caudal pontine
reticular nucleus (PnC), which may be good candidates for analyzing the
neuronal basis of mammalian behavior. In a first step of this study, we
employed retrograde and anterograde tracing techniques to identify the
possible sources of input and the efferent targets of these neurons. In a
second step, we performed intracellular recordings in vivo, followed by
subsequent injections of HRP for morphological identification, thereby
investigating whether characteristic features of the ASR are reflected by
physiological properties of giant PnC neurons. Our observations demonstrate
convergent, bilateral input from several auditory brainstem nuclei to the
PnC, predominantly originating from neurons in the cochlear nuclear complex
and the superior olivary complex. Almost no input neurons were found in the
nuclei of the lateral lemniscus. As the relatively long neuronal response
latencies in several of these auditory nuclei appear to be incompatible
with the primary ASR, we conclude that neurons in the cochlear root nuclei
most likely provide the auditory input to PnC neurons that is required to
elicit the ASR. The giant PnC neurons have a remarkable number of
physiological features supporting the hypothesis that they may be a neural
correlate of the ASR: (1) they receive short- latency auditory input, (2)
they have high firing thresholds and broad frequency tuning, (3) they are
sensitive to changes in stimulus rise time and to paired-pulse stimulation,
(4) repetitive acoustic stimulation results in habituation of their
response, and (5) amygdaloid activity enhances their response to acoustic
stimuli. Anterograde tracing showed that most giant PnC neurons are
reticulospinal cells. Axon collaterals and terminal arbors were found in
the reticular formation as well as in cranial and spinal motoneuron pools.
The results of this study indicate that giant PnC neurons form a
sensorimotor interface between the cochlear nuclear complex and cranial and
spinal motoneurons. This neuronal pathway implies that the elementary
acoustic startle circuit is composed of only three central relay stations
and thus appears to be organized more simply than assumed in the past.
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