Contributions of the vestibular nucleus and vestibulospinal tract to the startle reflex

The startle reflex is elicited by strong and sudden acoustic, vestibular or trigeminal stimuli. The caudal pontine reticular nucleus, which mediates acoustic startle via the reticulospinal tract, receives further anatomical connections from vestibular and trigeminal nuclei, and can be activated by vestibular and tactile stimuli, suggesting that this pontine reticular structure could mediate vestibular and trigeminal startle. The vestibular nucleus, however, also projects to the spinal cord directly via the vestibulospinal tracts, and therefore may mediate vestibular startle via additional faster routes without a synaptic relay in the hindbrain. In the present study, the timing properties of the vestibular efferent pathways mediating startle-like responses were examined in rats using electrical stimulation techniques. Transient single- or twin-pulse electrical stimulation of the vestibular nucleus evoked bilateral, startle-like responses with short refractory periods. In chloral hydrate-anesthetized rats, hindlimb electromyogram latencies recorded from the anterior biceps femoris muscle were shorter than those for stimulation of the trigeminal nucleus, and similar to those for stimulation of the caudal pontine reticular nucleus or ventromedial medulla. In awake rats, combining vestibular nucleus stimulation with either acoustic stimulation or trigeminal nucleus stimulation enhanced the whole-body startle-like responses and led to strong cross-modal summation without collision effects. In both chloral hydrate-anesthetized and awake rats, combining vestibular nucleus stimulation with ventromedial medulla stimulation produced a symmetrical collision effect, i.e. a loss of summation at the same positive and negative stimulus intervals, indicating a continuous connection between the vestibular nucleus and ventromedial medulla in mediating vestibular startle. By contrast, combining trigeminal nucleus stimulation with ventromedial medulla stimulation resulted in an asymmetric collision effect when the trigeminal nucleus stimulation preceded ventromedial medulla stimulation by 0.5 ms, suggesting that a monosynaptic connection between the trigeminal nucleus and ventromedial medulla mediates trigeminal startle. We propose that the vestibulospinal tracts participate strongly in mediating startle produced by activation of the vestibular nucleus. The convergence of the vestibulospinal tracts with the reticulospinal tract within the spinal cord therefore provides the neural basis of cross-modal summation of startling stimuli.