The Journal of Neuroscience, 2002, 22:RC226:1-7

Semicircular Canal Afferents Similarly Encode Active and Passive Head-On-Body Rotations: Implications for the Role of Vestibular Efference
 
Kathleen E. Cullen¹ and Lloyd B. Minor<sup>2

1</sup> Aerospace Medical Research Unit, Department of Physiology, McGill University, Montreal, Quebec, Canada H3G 1Y6, and ² Department of Otolaryngology Head and Neck Surgery, Department of Biomedical Engineering, and Department of Neuroscience, The Johns Hopkins University, Baltimore, Maryland 21093

Two monkeys (a Macaca mulatta and a Macaca fasicularis) were prepared for chronic extracellular recording. The procedures recently described (Sylvestre and Cullen, 1999 ) were used for the surgical preparation of monkeys. A stainless steel recording chamber was positioned stereotaxically on the skull to record from the vestibular nerve at the point at which it emerged from the internal auditory meatus. We approached the vestibular nerve through the floccular complex, which was identified by its eye movement-related activity (Lisberger and Pavelko, 1986 ). Entry to the nerve was preceded by a silence, indicating that the electrode had left the cerebellum, and after exiting the nerve we were able to determine (as infrequently as possible) the location of the base of the skull by the abrupt appearance of 60 Hz noise. Before the recording experiments, the location of the nerve was confirmed in both monkeys as follows: first, a guide tube was advanced through an X-Y stage (Narishige, Tokyo, Japan), which was attached to the monkey's recording chamber, to a depth estimated to be 1.5 mm above the nerve. Second, the proximity of the guide tube to the internal auditory meatus was then verified by anesthetizing the monkeys and making x-ray images of their heads in the horizontal, sagittal, and frontal planes. In one animal, the location of the microelectrode within the vestibular nerve was later histologically confirmed. All experimental protocols complied with the guidelines of the Canadian Council on Animal Care and National Institutes of Health and were approved by the Animal Care Committee of McGill University and by the Animal Care and Use Committee of the Johns Hopkins University School of Medicine.

During the experiments, the monkey was seated in a primate chair. For six afferents, horizontal and vertical gaze and head movements were recorded using the magnetic search coil technique (Fuchs and Robinson, 1966 ). For the remaining afferents, horizontal, vertical, and torsional head movements were measured using two orthogonally placed coils that were secured to the animal's head implant. For vertical and horizontal canal units, we analyzed only those head movements for which the amplitude of the torsional component was <15% of the vertical or horizontal component, respectively. The extracellular recording techniques that were used have been recently described (Hullar and Minor, 1999 ; Sylvestre and Cullen, 1999 ). Monkeys generated voluntary eye-head movements to track a food target, which was alternatively presented on either side of an opaque screen facing the monkey (gaze shifts; Guitton et al., 1984 ), or which was slowly moved in front of the monkey to elicit eye-head pursuit. To investigate each the response of each afferent during passive head rotations, the experimenter manually rotated the animal's head on its neck to induce head-on-body movements with trajectories comparable to those generated during voluntary gaze shifts and pursuit (peak head velocity = ±100-400 °/sec and predominate frequency 0.5-1.5 Hz). Behavioral paradigms, target, head motion, and the storage of data were controlled by a UNIX-based real-time data acquisition program, and all data were recorded on a DAT tape for later playback and analysis. Off-line, gaze, and head position signals were low-pass filtered at 250 Hz (8 pole Bessel filter) and sampled at 1000 Hz. These signals were digitally filtered at 125 Hz and differentiated to produce velocity signals.