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

Abstract

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.

Sensorimotor Gating in Larval Zebrafish

“…We believe that this is consistent with SLCs being all-or-nothing responses dependent on Mauthner cell activity. In mammals, the magnitude of the startle response is determined by the fraction of the thousands of neurons in the pontine reticular nucleus caudal (PNc) activated by the startle stimulus (Lingenhohl and Friauf, 1994;Koch, 1999). PPI attenuates the magnitude of the startle response by reducing the fraction of PNc neurons activated.…”

“…Larval stage zebrafish display a robust startle response (supplemental movie 1, available at www.jneurosci.org as supplemental material), consisting of a "C-bend" of the body, followed by a smaller counter bend and swimming (Kimmel et al, 1974). The zebrafish startle response is mediated by reticulospinal neurons similar to the central elements underlying startle in higher vertebrates (Lingenhohl and Friauf, 1994;Liu and Fetcho, 1999;Gahtan et al, 2002). In zebrafish, fast responses initiated with a C-bend (C-start responses) require just three bilateral pairs of reticulospinal neurons including the Mauthner cells (Liu and Fetcho, 1999).…”

Serotonin transporter gene variation impacts innate fear processing: acoustic startle response and emotional startle

“…30 It is yet an open question whether the amygdala complex is not only involved in the emotional modulation of the startle response but also in the processing of startling stimuli per se. If the response signal within the usual time window (20-140 ms) integrates several serial projections from different brain nuclei to the PnC, 31 an early involvement of the amygdala complex in the processing of startling stimuli seems possible. 13 While in the model of a primary acoustic startle circuit, the PnC is the most important brainstem site for the evocation of the ASR, other brain nuclei than the PnC also play a role in mediating the ASR.…”

GABA in the Deep Layers of the Superior Colliculus/Mesencephalic Reticular Formation Mediates the Enhancement of Startle by the Dopamine D1Receptor Agonist SKF 82958 in Rats

“…Taken together, these results add to a body of work showing that GABAergic transmission at the level of the deep SC/Me is an important component in the regulation and expression of motor behaviors. Because the deep SC/Me is not part of the primary acoustic startle pathway (Lingenhöhl and Friauf, 1994;Lee et al, 1996), the results of the present study suggest that the deep SC/Me exerts a modulatory influence on this reflex. A recent report from our laboratory has identified a heavy ipsilateral innervation from the deep SC/Me to the part of the PnC critical for startle (Meloni and Davis, 1999b).…”