Integrative responses of neurons in nucleus tractus solitarius to visceral afferent stimulation and vestibular stimulation in vertical planes

Abstract

Anatomical studies have demonstrated that the vestibular nuclei project to nucleus tractus solitarius (NTS), but little is known about the effects of vestibular inputs on NTS neuronal activity. Furthermore, lesions of NTS abolish vomiting elicited by a variety of different triggering mechanisms, including vestibular stimulation, suggesting that emetic inputs may converge on the same NTS neurons. As such, an emetic stimulus that activates gastrointestinal (GI) receptors could alter the responses of NTS neurons to vestibular inputs. In the present study, we examined in decerebrate cats the responses of NTS neurons to rotations of the body in vertical planes before and after the intragastric administration of the emetic compound copper sulfate. The activity of more than one-third of NTS neurons was modulated by vertical vestibular stimulation, with most of the responsive cells having their firing rate altered by rotations in the head-up or head-down directions. These responses were aligned with head position in space, as opposed to the velocity of head movements. The activity of NTS neurons with baroreceptor, pulmonary, and GI inputs could be modulated by vertical plane rotations. However, injection of copper sulfate into the stomach did not alter the responses to vestibular stimulation of NTS neurons that received GI inputs, suggesting that the stimuli did not have additive effects. These findings show that the detection and processing of visceral inputs by NTS neurons can be altered in accordance with the direction of ongoing movements.

Integrative responses of neurons in parabrachial nuclei to a nauseogenic gastrointestinal stimulus and vestibular stimulation in vertical planes

“…Data were collected from 16 purpose-bred adult cats (Liberty Research, Waverly, NY) of either sex, weighing 2.6 to 4.9 kg. The design of the experiments was similar to that in a recent study from our laboratory (52); as such, the description of the methodology is abbreviated below.…”

“…Surgery was conducted under isoflurane anesthesia to intubate the trachea, cannulate both femoral veins, insert a transducer (Millar Instruments, Houston, TX) through the femoral artery into the abdominal aorta to record blood pressure, implant an intragastric catheter through an esophagostomy to administer copper sulfate, and secure both C5 phrenic nerves in bipolar silver cuff electrodes to record respiratory activity. The carotid arteries were dissected free of surrounding tissues and occluded bilaterally, and a ligature was placed around each artery to permit stretch of the carotid sinus (16,52). The animals were placed in a stereotaxic frame with the head pitched-down 30°to vertically align the vertical semicircular canals, and they were supported using hip pins and a clamp placed on the dorsal process of an upper thoracic vertebra.…”

“…When a unit was isolated, we first recorded its spontaneous activity along with blood pressure (sampled at 100 Hz) and phrenic nerve activity (amplified by a factor of 10,000, filtered with a band pass of 100 -10,000 Hz, integrated with a 10-ms time constant, full-wave rectified, and sampled at 1,000 Hz). We then recorded the unit's responses during the decrease in blood pressure elicited by mechanical stretch of the carotid sinus (16,52). We next examined the unit's activity while rotating the entire animal about the pitch (transverse) and roll (longitudinal) axes using a servo-controlled hydraulic tilt table (NeuroKinetics, Pittsburgh, PA), as described in detail in previous articles (32,59).…”

“…The amplitude of these stimuli was 2.5-5°at frequencies Ͼ0.2 Hz, and 5-10°at frequencies Յ0.2 Hz. As in previous studies, Bode plots generated from responses to fixed-plane stimuli were used to determine which vestibular end organs provided for the modulation of neuronal activity (16,32,42,43,52).…”

“…After the responses of a unit to vertical vestibular stimulation were characterized, 83 mg of copper sulfate dissolved in 10 ml of distilled water was injected into the stomach, as in a recent study (52). We recorded the effects of copper sulfate injection on the unit's firing rate for 5 min and then repeated the vestibular testing protocol outlined above.…”