Neural basis for eye velocity generation in the vestibular nuclei of alert monkeys during off-vertical axis rotation

Abstract

Activity of "vestibular only" (VO) and "vestibular plus saccade" (VPS) units was recorded in the rostral part of the medial vestibular nucleus and caudal part of the superior vestibular nucleus of alert rhesus monkeys. By estimating the "null axes" of recorded units (n = 79), the optimal plane of activation was approximately the mean plane of reciprocal semicircular canals, i.e., lateral canals, left anterior-right posterior (LARP) canals or right anterior-left posterior (RALP) canals. All units were excited by rotation in a direction that excited a corresponding ipsilateral semicircular canal. Thus, they all displayed a "type I" response. With the animal upright, there were rapid changes in firing rates of both VO and VPS units in response to steps of angular velocity about a vertical axis. The units were bidirectionally activated during vestibular nystagmus (VN), horizontal optokinetic nystagmus (OKN), optokinetic after-nystagmus (OKAN) and off-vertical axis rotation (OVAR). The rising and falling time constants of the responses to rotation indicated that they were closely linked to velocity storage. There were differences between VPS and VO neurons in that activity of VO units followed the expected time course in response to a stimulus even during periods of drowsiness, when eye velocity was reduced. Firing rates of VPS units, on the other hand, were significantly reduced in the drowsy state. Lateral canal-related units had average firing rates that were linearly related to the bias or steady state level of horizontal eye velocity during OVAR over a range of +/- 60 deg/s. These units could be further divided into two classes according to whether they were modulated during OVAR. Non-modulated units (n = 5) were VO types and all modulated units (n = 5) were VPS types. There was no significant difference between the bias level sensitivities relative to eye velocity of the units with and without modulation (P > 0.05). The modulated units had no sustained change in firing rate in response to static head tilts and their phases relative to head position varied from unit to unit. The phase did not appear to be linked to the modulation of horizontal eye velocity during OVAR. The sensitivities of unit activity to eye velocity were similar during all stimulus modalities despite the different gains of eye velocity vs stimulus velocity during VN, OKN and OVAR. Therefore, VO and VPS units are likely to carry an eye velocity signal related to velocity storage.(ABSTRACT TRUNCATED AT 400 WORDS)

Spatial Properties of Central Vestibular Neurons of Monkeys After Bilateral Lateral Canal Nerve Section

“…3 of Cohen et al 1983). Whether the VO cells disappeared or were disfacilitated is not known, but the data support the idea that activity of horizontal VO neurons is dependent on intact input from the lateral canals (Reisine and Raphan 1992).…”

“…What was unexpected was that we failed to find vertical canal-related neurons in this area. Most units recorded in the rostral part of the MVN are related to the horizontal aVOR in the normal animal (Cheron et al 1996;Chubb et al 1984;Fuchs and Kimm 1975;Furuya and Markham 1981;Ishizuka et al 1980;Keller and Kamath 1975;McCrea et al 1980McCrea et al , 1987Newlands and Perachio 2003;Reisine and Raphan 1992;Scudder and Fuchs 1992;Searles and Barnes 1977) but also have a convergent input from at least one vertical semicircular canal or the otolith organs (Baker et al 1984a,b;Brettler and Baker 2001;Curthoys and Markham 1971;Dickman and Angelaki 2002;Fukushima et al 1990;Markham and Curthoys 1972;Sato et al 2002;Yakushin et al 2005). Microscopic inspection of MVN did not reveal a loss of neurons nor was there heavy gliosis that might have accompanied neuronal death.…”

“…It has been postulated that these cells are responsible for generation of horizontal velocity storage in the vestibular system (Reisine and Raphan 1992;Yokota et al 1992;Yakushin et al 2005). Only the yaw component of velocity storage disappears when the lateral canal nerves are sectioned with the animals tested in an upright position, and it reappears when the animals are tilted forward or back (Fig.…”

“…Analog data were digitized at 600 Hz with 12-bit resolution. The time of the standard pulse occurrence was measured relative to the sampling clock rate (Reisine and Raphan 1992). We assumed that only one spike would occur within the sampling interval of 1.67 ms, which is equal to a peak firing frequency of 600 Hz.…”

“…These lay in SVN. We also searched through areas of MVN where vestibular-only (VO) neurons are typically located (Chubb et al 1984;Dickman and Angelaki 2002;Fuchs and Kimm 1975;Keller and Kamath 1975;McCrea et al 1987;Reisine and Raphan 1992;Scudder and Fuchs 1992;Yakushin et al 2005). No horizontal canal-related neurons were encountered in this region.…”