Characteristics of near response cells projecting to the oculomotor nucleus

Abstract

1. Previous work has shown neurons just dorsal and lateral to the oculomotor nucleus that increase their firing rate with increases in the angle of ocular convergence. It has been suggested that the output of these midbrain near response cells might provide the vergence command needed by the medial rectus motoneurons. However, lens accommodation ordinarily accompanies convergence, and a subsequent study showed that only about one-half of these midbrain near response cells carried a signal related exclusively to vergence. One hypothesis suggested by this finding is that this subgroup of neurons might have a unique role in providing a "pure" vergence signal to the medial rectus motoneurons. 2. In the present study extracellular recordings were made from midbrain near response cells in monkeys while eye position and lens accommodation were measured. The monkeys viewed targets through an optical system that allowed the accommodative and ocular vergence demands to be manipulated independently. This approach was used to produce a partial dissociation of accommodative and vergence responses, so that an accommodative and vergence coefficient could be determined for each cell, by the use of the following equation FR = R0 + kda x AR + kdv x CR where FR is the firing rate of the near response cell, R0 is the predicted firing rate for a distant target, kda is the (dissociated) accommodation coefficient, AR is the accommodative response, kdv is the (dissociated) vergence coefficient, and CR is the convergence response. 3. The vergence and accommodation coefficients were determined for a large number of midbrain near response cells, including a subset that could be antidromically activated from the medial rectus subdivisions of the oculomotor nucleus. Some near response neurons were found with signals related exclusively to convergence (i.e., kdv greater than 0 and kda = 0), whereas several others had signals related exclusively to lens accommodation (i.e., kda greater than 0 and kdv = 0). The majority of the near response cells had signals related to both responses (i.e., kda not equal to 0 and kdv not equal to 0). Furthermore, the vergence and accommodation coefficients of near response cells appeared to be continuously distributed. Some cells had negative accommodation or vergence coefficients. 4. The 17 near response cells that could be antidromically activated from the oculomotor nucleus presumably provide vergence signals to the medial rectus motoneurons. Although all had positive vergence coefficients, only four of these cells carried signals that were related exclusively to vergence.(ABSTRACT TRUNCATED AT 400 WORDS)

The Brain Stem Saccadic Burst Generator Encodes Gaze in Three-Dimensional Space

“…The results of recent behavioral studies, which have shown that saccade dynamics are an important determinant of the dynamics of vergence facilitation, have led to the rejection of the two most influential models: the "Multiply Model" and the "Saccade-Related Vergence Burst Neuron Model" (Busettini and Mays 2005b;Zee et al 1992;Zhang et al 1992). Accordingly, to account for the correlation between conjugate and vergence movements, these investigators have proposed that SBNs exclusively encode conjugate saccadic dynamics and that projections from these conjugate SBNs to the vergence premotor pathway underlie the vergence facilitation during disconjugate saccades.…”

Dynamic Coding of Vertical Facilitated Vergence by Premotor Saccadic Burst Neurons

“…Thus this suggests that, whereas the SBNs function to rapidly drive the eyes to a new position, an additional vergence command is required to ensure accurate binocular realignment of gaze (King and Zhou 2000). Notably, neurons encoding slow vergence, which have been described near the abducens nucleus (Gnadt et al 1988) and oculomotor nucleus (Judge and Cumming 1986;Mays 1984;Zhang et al 1991Zhang et al , 1992, are likely candidates to drive such eye movements. Further work will be required to understand how neural circuits in the brain stem and cerebellum interact with descending control pathways to ensure the accurate control of gaze in three dimensions.…”

“…Traditionally, disconjugate saccades were thought to be controlled by linear summation of premotor commands from two distinct neural control pathways that separately encode the conjugate and vergence components of eye motion: 1) a conjugate saccadic subsystem, which commands a rapid but yoked movement of the two eyes in a given direction; and 2) a separate vergence subsystem, which rotates the eyes in opposite directions to ensure accurate binocular positioning (Hering 1977; Mays 1984Mays , 1998. Accordingly, the premotor circuitry involved in generating horizontal saccades (e.g., the saccadic burst neurons [SBNs] of the paramedian pontine reticular formation [PPRF]) was generally assumed to provide the command to drive the horizontal conjugate component of such movements, whereas a specific subpopulation of neurons in the mesencephalic reticular formation (MRF), which encode a signal proportional to viewing distance, were thought to produce the required vergence command (Busettini and Mays 2005b;Gamlin 2002;Gamlin et al 1989;Mays et al 1986;Zhang et al 1992).…”

“…Traditionally, disconjugate saccades were thought to be controlled by linear summation of premotor commands from two distinct neural control pathways that separately encode the conjugate and vergence components of eye motion: 1) a conjugate saccadic subsystem, which commands a rapid but yoked movement of the two eyes in a given direction; and 2) a separate vergence subsystem, which rotates the eyes in opposite directions to ensure accurate binocular positioning (Hering 1977; Mays 1984Mays , 1998. Accordingly, the premotor circuitry involved in generating horizontal saccades (e.g., the saccadic burst neurons [SBNs] of the paramedian pontine reticular formation [PPRF]) was generally assumed to provide the command to drive the horizontal conjugate component of such movements, whereas a specific subpopulation of neurons in the mesencephalic reticular formation (MRF), which encode a signal proportional to viewing distance, were thought to produce the required vergence command (Busettini and Mays 2005b;Gamlin 2002;Gamlin et al 1989;Mays et al 1986;Zhang et al 1992).The summation of commands from two distinct premotor pathways, however, cannot account for a number of observations that have been made regarding disconjugate saccades. Notably, vergence velocities reach values greater during disconjugate saccades than would be predicted by the linear summation of commands from separate saccadic and vergence premotor pathways (Busettini and Mays 2005b;Collewijn et al 1997;Enright 1984Enright , 1992Maxwell and King 1992;Ono et al 1978;Oohira 1993;van Leeuwen et al 1998;Zee et al 1992).…”

The horizontal angular vestibulo-ocular reflex: A non-linear mechanism for context-dependent responses

“…Thus an ipsilateral eye position efference copy is available from PH, while binocular information or at least contralateral eye position is also available to the EHV cells through commissural pathways and interneuron connections. Another source could be through projections from the socalled vergence neurons in the midbrain reticular formation that discharge proportionally to the vergence angle [25]; however, to date the exact anatomical projections of these neurons remain unknown [26]. Access to cells with such characteristics is essential to tune the nonlinear gain of EHV cells for different target distances and eccentricities.…”