Giant neurons in the rat reticular formation: a sensorimotor interface in the elementary acoustic startle circuit?

• Published in: The Journal of neuroscience 1994-03, Vol.14 (3), p.1176-1194
• Main Authors: Lingenhohl, K, Friauf, E
• Format: Article
• Language: English
• Subjects: Acoustic Stimulation; Amygdala - physiology; Animals; Auditory Pathways - physiology; Auditory Perception - physiology; Biological and medical sciences; Brain Stem - physiology; Ear and associated structures. Auditory pathways and centers. Hearing. Vocal organ. Phonation. Sound production. Echolocation; Electric Stimulation; Evoked Potentials, Auditory, Brain Stem - physiology; Female; Fundamental and applied biological sciences. Psychology; Habituation, Psychophysiologic - physiology; Neurons - physiology; Neurons, Afferent - physiology; Neurons, Efferent - physiology; Rats; Reflex, Startle - physiology; Reticular Formation - physiology; Synaptic Transmission - physiology; Vertebrates: nervous system and sense organs
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/jneurosci.14-03-01176.1994

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