072

Anatomical substrates of oculomotor control

Jean A Btittner-Ennever* and Anja KE Hornt

It is convenient to describe oculomotor neuroanatomy in In this review, we will first describe the basic neuro-
terms of five to six different eye movement types, each anatomical networks controlling each eye movement type,
with relatively independent neural circuitry: saccades, and then examine recent studies on the saccadic circuits
vestibulo-ocular reflex, optokinetic response, smooth pursuit, in the reticular formation. Nucleus reticularis tegmenti
vergence and, most recently added to the list, gaze-holding. pontis (nrtp) is taken as an example of a structure in which
Current research indicates that many structures participate in information from several eye movement types appears to
several eye movement types, such as the nucleus reticularis converge. Next, we review the neural connections of the
tegmenti pontis, frontal eye fields and pretectum. However, pretectum, in particular, the nucleus of the optic tract
the circuits appear to run in parallel rather than being (NOT), and discuss its association with several different
integrated. eye movement types, not only the optokinetic response or
smooth pursuit. Finally, we consider the advances in the
anatomical organization of the eye fields in the cerebral
Addresses cortex.
Institute of Anatomy, Ludwig-Maximilian University, Pettenkoferstrasse
11, D-80336 Munich, Germany
*e-mail: Buettner@anat.med.uni-muenchen.de Basic oculomotor circuits
‘e-mail: Anja.Bochtler@anat.med.uni-muenchende A simple description of the premotor circuits for saccadic
Current Opinion in Neurobiology 1997, 7:872-879
eye movements is that premotor burst neurons in the para-
median pontine reticular formation (PPRF) activate eye
http://biomednet.com/elecref/0959438800700872
muscle motoneurons during horizontal saccades, whereas
0 Current Biology Ltd ISSN 0959-4388 those in the rostra1 interstitial nucleus of the medial
longitudinal fasciculus (rihlLF) activate the eye muscle
Abbreviations
DTN dorsal terminal nucleus of the accessory optic tract motoneurons during vertical saccades. Between saccades
EBN excitatory burst neuron the premotor neurons in PPRF and rihILF are inhibited
FEF frontal eye field by omnipause neurons (OPNs) in the nucleus raphe
GABA y-aminobutyric acid
interpositus (rip). Burst neurons and omnipause neurons
IBN inhibitory burst neuron
receive afferent control from the superior colliculus (SC),
iC interstitial nucleus of Cajal
LGNd dorsal lateral geniculate nucleus whereas the frontal eye fields (FEFs) of the cerebral cortex
MRI magnetic resonance imaging appear only to contact the OPNs [S”].
NOT nucleus of the optic tract
nrpc nucleus reticularis pontis caudalis
The vestibule-ocular reflex is generated by sensory signals
nr@ nucleus reticularis tegmenti pontis
OKN optokinetic response from the labyrinthine canals and otoliths, relayed through
OPN omnipause neuron the vestibular nuclei to the extraocular motoneurons in
PET positron emission tomography cranial nerve nuclei III, IV and VI.
PMT cell groups of the paramedian tract
PPRF paramedian pontine reticular formation
nucleus prepositus hypoglossi The optokinetic responses (OKNs) are elicited by the
PPH
riMLF rostra1 interstitial nucleus of the medial longitudinal fasciculus movement of large visual fields across the retina, which
SC superior colliculus generate responses in the retino-recipient accessory optic
terminal nuclei of the mesencephalon: the dorsal, medial
lateral and interstitial terminal nuclei (DTN, hITI%, LTN,
Introduction and ITN). These nuclei, along with NOT in the pretec-
Up to now it has been convenient to divide eye turn, feed the information into the vestibular-oculomotor
movements into different types (i.e. saccades, vestibulo- circuits through which the OKN is generated.
ocular reflex, optokinetic response, smooth pursuit and
vergence), and to consider the neuroanatomical circuits Smooth pursuit pathways receive retinal information
generating each type as relatively separate [l,Z]. But through two parallel afferent pathways: a motion-sensitive
as a clearer understanding of the circuits emerges, and or ‘magnocellular’ pathway, and a form- and colour- sensi-
with the development of new research techniques ((3.1; tive ‘parvocellular’ pathway. Each pathway projects in par-
N Gerrits, \V Graf, N Yatim, G Ugolini, Sot Neulosci Abstt- allel through the dorsal lateral geniculate nucleus (LGNd)
1996, 22:665), there is a tendency in many of the recent to the primary visual cortex, and supplies posterior parietal
publications to move away from the oversimplification cortical areas with information concerning object motion
of separate anatomical pathways and to tackle the more in space (known as the dorsal stream), in contrast to
complex problems of how and where different eye the inferotemporal region, which is more involved in the
movement types interact with each other or with other analysis of form (i.e. the ventral stream). Descending
internal neural networks [4*]. projections from the posterior parietal cortex terminate in
 Anatomical substrates of oculomotor control BOttner-Ennever and Horn 073

the dorsolateral pontine nuclei, from which information Fiaure 1

is relayed co the dorsal and ventral paraflocculus and the
caudal vermis of the cerebellum. Cerebellar efferents,
(a) Parasagittal view
through intermediate relays to the oculomotor nuclei, then
generate smooch pursuit.

Vergence premotor neurons have been found in the

mesencephalic reticular formation dorsal to the oculomotor
nucleus, as well as in the pretectum [1,6], and provide the
vergence command to the oculomotor nuclei.

In addition to these eye movement types, gaze-holding

should be included in the list. Gaze-holding circuits
are involved in overcoming the elastic properties of the
eyeball in the orbit, and serve to hold the eye in a
new position after a quick movement. Like other eye
movement types, gaze-holding is also subtended by a
relatively separate group of neural circuits involving the
velocity-to-position integrator: the interstitial nucleus of
Cajal (iC) and nucleus prepositus hypoglossi (ppH), with (b) Lateral view
their reciprocal vestibular and cerebellar connections.

The brainstem reticular formation

Saccadic premotor cell groups
In the PPRF, it has now proved possible co anatomically
identify some of the functional subgroups essential for the
generation of saccades. Premotor excitatory burst neurons
(EBNs) for horizontal saccades form a compact group
of medium-sized neurons within the dorsomedial part of
rhe nucleus reticularis pontis caudalis (nrpc) that can be
identified on ordinary Nissl stained sections; inhibitory
burst neurons (IBNs) lie more caudally in the nucleus
paragigantocellularis dorsalis [7] (Figure 1).

In the rihlLF of monkey, premotor neurons for up-

ward and downward saccades appear to be intermingled
Current Op~mn I” Neurobiology
[5”,8”], whereas in cat. upward neurons were found more
caudally than downward neurons [9’]. The same authors A (a) parasagittal and (b) lateral view of the macaque monkey brain,
describe a possible correlate for vertical IBi%s in the showing the anatomical location of some of the cortical fields and
rihILF using GABA as a transmitter, lvhereas excitation bralnstem structures participating in the control of eye movements,
is mediated by glutamate/aspartate to oculomotor neurons and referred to in the text. al, lateral arcuate sulcus; as, superior
arcuate sulcus; cga, anterior cingulate gyrus; cgp, posterior clngulate
[lO”*,ll**]. Inhibitory OPNs in PPRF use glycine as
gyrus; cgs, cingulate gyrus; cs, central sulcus; FST, fundus of the
a transmitter [12); their destruction with ibotenic acid superior temporal area; io, Inferior olive; ip, lntraparietal sulcus;
results in a prolonged duration and slowing of saccades L, large saccade region of FEF; LIP, lateral lntraparietal area;
[13”]. In clinical cases of progressive supranuclear palsy Ml, pnmary motor cortex; MST, medial superior temporal sulcus;
MT, medial temporal area; nrpo, nucleus retlcularls pontis oralis;
with saccadic disturbances, OPNs were associated with
pgd, nucleus paragigantocellularis dorsalis; ps, prtncipal sulcus;
neurofibrillary tangles [ 14”). All saccadic premotor neu- PSR, principal sulcus region; pt, pretectum; s, small saccade region
rons and the OPNs contain the calcium-binding protein of FEF; Sl, primary sensory cortex; SEF, supplementary eye field;
parvalbumin. a fact utilized to locate the homologue SMA, supplementary motor area; SP, smooth pursuit region of FEF;
STP, superior temporal polysensory area; Vl, primary visual cortex;
cell groups in humans [S*‘,lS**]. Pontine long-lead burst
V3A, parietal visual area V3A; VIP, ventral lntraparietal area; 5, area 5;
neurons have been found within the projection areas of 7, area 7; 19, area 19; Ill, oculomotor nucleus; VI, abducens nucleus.
the SC: the dorsomedial part of the nrtp, the nucleus
reticularis pontis oralis (nrpo) and its border with the
nrpc (Figure 1) [16**]. Finally, the central mesencephalic
reticular formation, lateral to the oculomotor nucleus, is an could provide the feedback signals essential for some
area of the reticular formation that is receiving renewed models of the saccadic burst generator ([ 17.1; for a review,
interest on account of its projections to the SC, which see [S”]).
a74 Motor systems

Saccadic premotor connectivity afferents from all oculomotor structures [32]. In cat, ppH
There have been several studies on the connectivity of the neurons project to the SC transmitting eye position and
functional saccadic cell groups described above. Pontine velocity signals [38’,39**], suggesting that it serves as
long-lead bursters innervate the EBK and OPN areas, a feedback control of saccades. It is pointed out by
and at least some of them may provide the long-sought Kokkoroyannis et nl. [33”] that iC (the vertical equivalent
inhibition of the OPNs during a saccade [16**,18’]. Recent of ppH) does not project to SC, which would make SC’s
anatomical and physiological studies in cat and monkey role as a feedback of saccades seem less likely. However,
revealed differential projections from the SC to the lesions of the ppH neurons do not affect saccades, but
saccadic premotor network in the reticular formation, impair gaze-holding [40**].
supporting the concept of a saccade pathway and a fixation
pathway [19’]. The caudal third of the SC projects directly A function in gaze-holding is also attributed to a collection
to the EBN area, but not to the OPn’s, lvhereas the rostra1 of cell groups within the paramedian tract (PhlT) neurons
third of the SC sends direct projections to the OPNs, but of the pontine and medullary reticular formation. The
more sparsely to the premotor burst neurons ((ZO’,Zl’*]; PhIT cell groups receive a copy of all premotor signals,
JA Biittner-Ennever, AKE Horn, Y Henn, Sor ~Vewosci and they project to the cerebellar flocculus and ventral
Abstr 1997, 23:1297). The identification of accommodation paraflocculus [41*].
neurons in rostra1 SC adds some indirect support for its
participation in fixation [W]. A recent model suggests the Pretectum
interaction of the saccadic and vergence system at the level The oculomotor functions associated with the pretectum
of the OPNs [6]. An additional role of the SC in slow are the generation of OKN, the pupillary light reflex and
drifts is being studied by several groups [23’,24,25’]. Slow a more recently recognised role in smooth pursuit eye
drifts is a term used for a distinct oculomotor pattern in movements. The pretectal olivary nucleus is essential for
cats that is intermediate between saccades and pursuit, and the pupillary light reflex [42”,43”], and in the primate,
serves to correct motor error after a saccade is terminated. it lies engulfed within the KOT, a structure crucial for
The anatomical pathways proposed for the drifts are direct ocular following ([44*]; S Yakushin, 11 Gizzi, H Reisine,
connections between the SC and the abducens nucleus B Cohen, Sor h’ett?-osci Absfr 1994, 20:772.) There is
that are provided by the tectoreticulospinal neurons. An a mounting interest in the interactions between NOT
alternative hypothesis suggests that the slow drifts may be and the highly structured and complex pretectal olivary
generated by the saccade feedback circuitry [26’]. nucleus [45”,46”]. The reciprocal connections of NOT to
all ipsilateral accessory optic nuclei, and of pretectal olivary
The nrtp is a good example of the increasing recognition nucleus to all contralateral accessory optic nuclei imply
of the complexity within oculomotor circuits. It is a a functional interplay between the NOT and pretectal
precerebellar nucleus composed of several subdivisions; olivary nucleus, possibly associated with the perceived
it lies dorsal to the pontine nuclei and is separated from motion (parallax) between a fixated visual object and its
it by ascending and descending fibre tracts. The ventral visual background [47,48**].
border of nrtp merges with the pontine nuclei, perhaps
even functionally [27-l. Until recently, nrtp was associated Recent anatomical studies on the efferents of the pre-
with saccades on account of its connections with the SC tectum have concentrated on the optokinetic-related
and FEFs, although distinctly separate OKN regions in pathways to ppH, the accessory optic nuclei, the inferior
nrtp have been recorded by Keller and Crandall (see [l]). olive, the pontine nuclei and nrtp [49’]. However, a
Newer data reveals the additional involvement of nrtp summary of NOT connections shown in Figure 2 makes it
in vergence [Z&29], smooth-pursuit-like slow drifts [30”], clear that NOT projects to all known visuomotor systems,
and even in the stabilization of Listing’s plane [31”]. and, in addition, interacts with other neural circuits, such
as visual attention [48’*]. It is not yet clear how these
Gaze-holding premotor circuits connections are used to coordinate the generation of eye
The iC lies adjacent to riMLF, and contains several movements.
eye-movement related neuronal groups [32]. Presumably,
burst-tonic and tonic neurons, which contribute to the TWO new and interesting projections from NOT have been
vertical and torsional integrator function, project directly reported recently: one is to the magnocellular layers of
to vertical ocular motoneurons [8**]. Other projection LGNd, fitting with the role of NOT in visual motion
targets of iC are the rihlLF, the vestibular nuclei and the [48”]; the second projection involves a select group
spinal cord [33”]. The function of saccade-related burst of extraocular motoneurons outside the main subgroups
neurons in iC is still unclear [34’]. Different torsional of the oculomotor nucleus, previously suggested to
deficits are present after unilateral riMLF versus iC lesions participate in convergence [46*-l. As pretectal efferents
[35”,36”]. from the pretectal olivary nucleus are known to control
pupillary constriction [43”], a role for the pretectal olivary
The ppH, like the iC, is involved in integrator function nucleus/NOT complex in the near-response (pupillary
[37*], but for horizontal eye movements, and receives constriction, accommodation and convergence) has been
 Anatomical substrates of oculomotor control Biittner-Ennever and Horn 875

Figure 2

Cerebral
cortex Retina

Saccade generatlon
Gaze flxatlon

SC

/ 3

Ocular followlng Visual thalamtc relay

VOR adaptation modulation

VOR adaptation

r7-j

A simplified diagram of NOT efferents to wuomotor structures, proposlng functIonal roles for the pathways. The pattern of connectiwty lmplles
that NOT participates In the control of all the different eye movement types. AON, accessory optic nuclei; dlpn, dorsolateral pontlne nuclei;
EW, Edinger-Westphal complex; io, lnferlor olive; Ic, locus coeruleus; Ign, lateral genlculate nucleus; nlll, oculomotor nucleus; pgn, pregenlculate
nucleus; ppd, nucleus peripeduncularis; ppt, pedunculopontine tegmental nucleus; rt, thalamlc reticular nucleus.

proposed [46**]: howc\,er, recordings from the pretectal The pretcctum also projects to the zona incerta. \lay Pt
olivary nucleus of the alert monkey have cscludcd ii N/. [.5.3**] present 3 careful study of the connectivity of
role for at least the pretect21 Iuminancc neurons in the zone incerta to SC and the pretcctum. lvith the salutar)
near-response [42”]. demonstration that its pretcctal affercnts arise from the
anterior pretectal nucleus rather than NO’I’. AS some
The majority of recent papers make no distinction studicb assumed [-KY*]. A contemporary rcpol-t .sho\vs for
between DTN and NO’T. Iiowever, they are anatomicall) the first time that there are saccadc-rcl:lted p~tse neurons
completely separate structures: DTK receives retinal in the zona incerta [i-l’].
afferents from the accessory optic tract, and is an accessory
optic nucleus: whereas NOT receives retinal afferents Cortical eye fields
through a different pathway the brachium of the SC Initially the FEFs \vrre thought to play ;I role on11
[48”]. Retinal-slip neurons occur in both NOT and in saccades, but subsequent research has sho\vn that
DTN; however. unlike DTN, NOT contains several FEFs control gaze-fixation [55]. Now. it is further
additional classes of neurons: jerk-neurons, LGKd-pro- subdivided into a FEF-pursuit and a l:EF-svccade area
jetting neurons (recently confirmed as GAB&positive but (Figure 1). Different retrograde tracers were injected into
calbindin- and P”r~“lbumin-negative [SO*]), 2nd two nen the FEF-pursuit and FEF-saccadc arcas. and labelling
NOT cell types (LGNd-projecting-saccade neurons [51*], was found in many cortical eye fields (including SEF,
and omnidirectional pausers [SP]). In the pretectum, the LIP, .\lST, PSR; see Figure 1) [56,57**]. Double-labelling
retinal-slip and saccade-related circuitries appear to run in experiments demonstrated that each of the above eye
parallel with each other rather than becoming integrated. fields had two separate nodes of labelling: one cluster
The repeated misconception that X0-1’ is an accessory labelled from the pursuit area, and the other from the
optic nucleus has certainly contributed to maintaining the FEF saccade region. implying that the saccadic and the
mystery regarding its function. cortical pursuit networks are relatively independent [57**].
076 Motor systems

The interconnected cortical eye fields appeared to be References and recommended reading
about the same hierarchical level, based on the criteria Papers of particular interest, published within the annual period of review,
have been highlighted as:
that cortico-cortical connections, between complex and
less-complex visual processing areas, are evident from . of special interest
the bilaminar pattern of terminals (in laminae I and l * of outstanding interest

V/VI), whereas a columnar input, to all layers, indicates a

1. Bijttner U, Bijttner-Ennever JA: Present concepts of oculomotor
connection between cortical areas on the same hierarchical
organization. In Neuroanatomy of the Ocu/omotor System. Edited
level [56,57**]. Some of these studies were carried out in by Biittner-Ennever JA. Amsterdam: Elsevier; 1966332.
the capuchin (Cebus) monkey, which has been shown to
2. Biittner-Ennever JA, Jenkins C, Armin-Parsa H, Horn AKE,
have similar cortical eye fields to those of the macaque Elston JS: A neuroanatomical analysis of lid-eye coordination
[57**,58*]. In humans, independent saccadic-FEFs and in cases of ptosis and downgaze paralysis. C/in Neuropathol
1996, 15:313-316.
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RIRI imaging: they appear to be localized to Brodmann’s 3. Kaufman GD, Mustari MJ, Miselis RR, Perachio AA: Transneuronal
. pathways to the vestibulocerebellum. I Comp Neural 1996,
area 6, rather than area 8, as in the monkey [59*]. 370:501-523.
A powerful technique (see N Gerrits, W Graf, N Yatim, G Ugolinl, Sot Neuro-
sciAbstr 1996, 22:665) that can effectively reveal crosslinks between neural
circuits in the oculomotor system, in which basic pathways are reasonably
The posterior cingulate cortex (cgp) (Figure l), is usually
well understood.
considered as a limbic area, but experiments in the alert
4. Vermersch Al, Muri RM, Rivaud S, Vidailhet M, Gaymard B, Agid Y,
monkey found that single-cell responses are associated . Pierrot Deseilligny C: Saccade disturbances after bilateral
with the monitoring of eye movements [60’]. Colleagues lentiform nucleus lesions in humans. I Neural Neurosurg
from the same group simultaneously published results Psychiatry 1996, 60:179-l 64.
Indicates a role of the putamen and globus pallidus in the cortical control
that indeed act as a warning to the interpretation of of saccades when the experimental paradigm requires the use of an Internal
cortical responses in alert monkey. They demonstrated, by representation of the target, such as in memory-guided or predictive sac-
cades.
a variety of ingeniously devised tasks, that attention and
anticipation played a major role in unit responses recorded 5. Moschovakis AK, Scudder CA, Highstein SM: The microscopic
.. anatomy and physiology of the mammalian saccadic system.
from area LIP in the parietal eye fields (Figure 1) [61”]. Prog Neurobiol 1996, 50:133-254.
A monumental review of the physlological and anatomical properties of all
known functional cell groups associated with saccades. Most of the data
Functional imaging techniques such as PET scans, are based on the reconstruction of physiologically identified, intracellularly
injected neurons in the primate. The authors evaluate several models for
functional hlRI, or transcranial magnetic stimulation have saccade generation.
enabled the cortical eye fields found in monkey to
6. Mays LE, Gamlin PD: Neuronal circuitry controlling the near
be anatomically visualized for the first time in humans response. Curr Opin Neurobiol 1995, 5:763-766.
[62]. Unfortunately, interpreting the functional images is
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often extremely difficult, and is completely impossible identification of premotor neurons for horizontal saccades
in xeroxed articles! However, there have now been in monkey and man by parvalbumin immunostaining. J Comp
Neural 1995, 359:350-363.
several demonstrations of saccade-paradigms enhancing
activity in the FEF, the supplementary eye fields, 6. Horn AKE, BOttner-Ennever JA: Premotor neurons for vertical
.. eye-movements in the rostra1 mesencephalon of monkey
dorsolareral prefrontal cortex, parietal eye fields. posterior and man: the histological identification by parvalbumin
parietal cortex and, in some cases, the cingulatr gyrus immunostaining. I Comp Neural 1997, in press.
Identified vertical premotor neurons in the riMLF and IC of monkey, which are
[63*,64*]. whereas smooth pursuit enhances the lateral medium-sized and parvalbumin-lmmunoreactive. These properties are used
occipitotemporal cortex [65**]. to accurately outline the riMLF and iC homologue in humans.

9. Wang SF, Spencer RF: Spatial organization of premotor

. neurons related to vertical upward and downward saccadic
eye movements in the rostra1 interstitial nucleus of the medial
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366:163-l 60.
Conclusions Small biocytin injections into different regions of the riMLF In cat suggest a
In conclusion, recent investigations of the anatomical tendency of premotor upward-neurons to lie more caudally and downward-
substrates of oculomotor control reveal that in several neurons to lie more rostrally.

structures, such as the FEFs of the cortex, the pretectum 10. Wang SF, Spencer RF: Morphology and soma-dendritic
.. distribution of synaptic endings from the rostra1 interstitial
and nrtp, more than one type of eye movement is
nucleus of the medial longitudinal fasciculus (riMLF) on
represented (e.g. saccades, smooth pursuit, vergence or motoneurons in the oculomotor and trochlear nuclei in the cat
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Using double-labelling methods in combination with electron microscopy, the
from each other at these levels, indicative of parallel authors studied the morphology and distribution of synaptic terminals from
processing. riMLF afferents at the vertical eye muscle motoneurons. They showed that
the same riMLF region contacts the motoneurons by excitatory and inhibitory
boutons mainly at the proximal and distal dendrites. The innervation pattern
from riMLF afferents is compared to the vestibular inputs to oculomotor neu-
rons and was found to be different in morphology, mode, and soma-dendritic
location.
Acknowledgements 11. Spencer RF, Wang SF: lmmunohistochemical localization of
This work was supported 1)~ the Deurxhc F[,rschung\gcmclnschafr .. neurotransmilters utilized by neurons in the rostra1 interstitial
(SFU 462; 03). nucleus of the medial longitudinal fasciculus (riMLF) that
 Anatomical substrates of oculomotor control BOttner-Ennever and Horn a77

project to the oculomotor and trochlear nuclei in the cat.
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Using double-labelling methods in combination with electron microscopy,
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However, the authors’ location of the nucleus raphe interpositus (rip) is in-
correct.

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Neurotransmitter profile of saccadic omnipause neurons in . mechanisms of two-dimensional orienting movements in
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.. neurons on saccadic eye movements in Rhesus macaques. A complementary study to (241, supporting the hypothesis that slow post-
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A chemical lesion study with careful histological controls demonstratmg a directly on abducens motoneurons and an indirect oligosynaptic pathway,
decrease in peak saccadic velocity and increase in saccade duration, but not involving the saccadic burst generator.
no impairment of fixation, after damage of the omnipause neurons.
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reduced in number and exhibit neurofibrillary tangle formation) than in cases Another study about slow eye movements atter stlmulatton of the supenor
without eye movement deficits. colliculus (see [23’]) examining the effects of stimulation parameters upon
movement velocity.
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A review of the identification of functional premotor cell groups of the sac-
This paper proposes an alternative hypothesis for the generation of slow eye
cadic system in humans.
movements after prolonged stimulatton of the superior colliculus.
16. Scudder CA, Moschovakis AK, Karabelas AB, Highstein SM:
.. 2 7. Schwarz C, Thler P: Comparison of projection neurons in the
Anatomy and physiology of saccadic long-lead burst neurons
. pontine nuclei and the nucleus reticularis tegmenti pontis of
recorded in the alert squirrel monkey. II. Pontine neurons.
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J Neurophysiol 1996, 76:353-370.
A useful double-labelling technique for studying the detailed morphology of
This is the first detailed description of the projection targets of physlologlcally
retrogradely identified neurons, and applied here to an area of high Interest.
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formation using intra-axonal HRP-injections in the pnmate. Three types of 28. Gamlln PDR, Clarke RJ: Single-unit activity in the primate
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.. movements evoked by microstimulation in macaque nucleus
1 7. Waitzman DM, Silakov VL, Cohen B: Central mesencephalic
. reticular formation (cMRF) neurons discharging before and reticularis tegmenti pontis. J Neurophysiol 1996, 76:3313-3324.
during eye movements. J Neurophysiol 1996, 75:1546-l 572. The exact reconstruction of stimulation sites reveal a topography in nrtp in
A physiological characterisation of neurons in the cMRF suggesttng an im- which a new smooth-pursuit-like area lies rostromedially and the saccade-like
portant role in saccades, providing the superior colliculus with tnformatlon neurons lie in caudal nrtp.
on the current eye displacement during a saccade. 31. Van Opstal Al, Hepp K, Suzuki Y, Henn V: Role of monkey
.. nucleus reticularis tegmenti pontis in stabilization of Listing’s
18. Kamogawa H, Ohki Y, Shimazu H, Suzuki I, Yamashita M:
. plane. J Neurosci 1997, 16:7284-7296.
Inhibitory input to pause neurons from pontine burst neuron
area in the cat. Neurosci Leff 1996, 203:163-l 66. This study provides evidence for neural circuits implementing Listing’s law,
A specific area of nucleus reticularis pontis caudalis within the excitatory rather than passive orbital forces -a controversial topic.
burst neuron area, purported to contain long-lead burst neurons, was found 32. Fukushima K, Kaneko CRS, Fuchs AF: The neuronal substrate
to be the most effective site from which omnipause neurons could be inhib- of integration in the oculomotor system. Prog Neurobiol 1992,
ited by electrical stimulation. 39:609-639.
19. Munoz DP, Waitzman DM, Wurtz RH: Activity of neurons in 33. Kokkoroyannis T, Scudder CA, Balaban CD, Highstem SM,
. monkey superior colliculus during interrupted saccades. .. Moschovakis AK: Anatomy and physiology of the primate
J Neurophysiol 1996, 75:2562-2580. interstitial nucleus of Cajal. 1. Efferent projections.
A stimulation and recording study in the superior colliculus (SC) of monkey J Neurophysiol 1996, 75:725-739.
suggesting that fixation cells in the rostra1 SC inhibit burst and build-up This is the first anatomical description of efferent pathways of the intersti-
neurons in the caudal SC. teal nucleus of Cajal in primate using small tracer injections with Phaseolus
lectin and biocytin. It disclosed three projection systems: a commissural, an
20. Chimoto S, lwamoto Y, Shimazu H, Yoshida K: Functional
ascending and a descending pathway.
. connectivity of the superior colliculus with saccade-related
brain stem neurons in the cat Prog Brain Res 1996, 112:157- 34. Helmchen C, Rambold H, Bijttner U: Saccade-related burst
165. . neurons with torsional and vertical on-directions in the
An electrophysiological study in the cat showtng that stimulation of the cau- interstitial nucleus of Cajal of the alert monkey. Exp Brain Res
dal superior colliculus (SC) activates premotor burst neurons at monosy- 1996, 112:63-78.
naptic latencies, which do not respond to stimulation of the rostra1 SC. Physiological study of non-premotor saccade-related neurons in the Inter&
Stimulation of the rostra1 SC activates ommpause neurons directly, which teal nucleus of Cajal usmg three-dimensional eye movement recordings. The
are inhibited after stimulation of the caudal SC. properties are compared to those of saccadic premotor burst neurons in the
riMLF.
21. Scudder CA, Moschovakis AK, Karabelas AB, HIghstein SM:
.. Anatomy and physiology of saccadic long-lead burst 35. Helmchen C, Glasauer S, Bartl K, Bi.ittner U: Contralesionally
neurons recorded in the alert squirrel monkey. I. Descending .. beating torsional nystagmus in a unilateral rostra1 midbrain
projections from the mesencephalon. J Neurophysiol 1996, lesion. Neurology 1996, 47:482-486.
76:332-352. A small unilateral lesion, thought to affect the nMLF, causes a torsIonal nys-
An excellent intracellular-HRP-injection study of physiologically Identified tagmus to the contralateral side of the lesion, which is the opposite directjon
mesencephalic long-lead burst neurons showing for the first time the pro- found after a unilateral lesion of the interstitial nucleus of Cajal. A slowing of
jection targets within the paramedian pontine reticular formation. ipsilaleral torsional fast phases was also seen (see [36”]).
878 Motor systems

36. Riordan-Eva P, Faldon M, Biittner-Ennever JA, Gass A, 47. Miles FA: The sensing of rotational and translational optic flow
.. Bronstein AM, Gresty MA: Abnormalities of torsional fast by the primate optokinetic system. In Visual Marion and Its
phase eye movements in unilateral rostra1 midbrain disease. Role in the Stabilization of Gaze. Edited by Miles FA, Wallman J.
Neurology 1996, 47:201-207. Amsterdam: Elsevier; 1993:393-403.
Small unilateral lesions thought to affect riMLF efferents caused only a
48. Biittner-Ennever JA, Cohen 8, Horn AKE, Reisine H: Efferent
slowing of ipsidirectional torsional fast phase eye movements. Compare
.. pathways of the nucleus of the optic tract in monkey and their
with [35”].
role in eye movements. I Comp Neurol 1996, 373:90-l 07.
37. Godaux E, Cheron G: The hypothesis of the uniqueness of the A functional analysis of the efferent pathways from NOT, demonstrating that
. oculomotor neural integrator: direct experimental evidence in it projects to structures involved in the control of six different types of eye
the cat. / Physiol Land 1996, 492:517-527. movements. It is suggested that, under the control of the cerebral cortex,
A recording study in the prepositus nucleus of the cat that favours the hy- NOT could function as a coordinator of the oculomotor circuits to generate
pothesis of a unique horizontal oculomotor integrator. the appropriate motor response. The paper emphasizes the importance of
considering NOT and DTN as functionally separate structures.
38. Hardy 0, Corvisier J: Firing properties of preposito-collicular
. neurones related to horizontal eye movements in the alert cat 49. Vargas CD, Volchan E, Nasi JP, Bernardes RF, Rochamiranda CE:
tip Brain Res 1996, 1 lo:41 3-424. . The nucleus of the optic tract (NOT) and the dorsal terminal
A recording study demonstrating that preposito-collicular neurons code eye nucleus (DTN) of opossums (Didelphis marsupialis aurita).
position and eye velocity just like eye muscle motoneurons, suggesting a role Brain Behav ho/ 1996, 48:1-l 5.
In feedback control of an ongoing saccade. A comparison of pretectal cell groups with commissural or Inferior olive
projectrons in the opossum. NOT and DTN differ, but are considered as a
39. Corvisier J, Hardy 0: Topographical characteristics of preposito- complex.
.. collicular projections in the cat as revealed by Phaseolus
vulgaris-leucoagglutinin technique. A possible organisation 50. Reimann S, Schmidt M: Histochemical characterisation of the
underlying temporal-to-spatial transformations. fwp Brain Res . pretecto-geniculate projection in kitten and adult cat Dev Bra/n
1997, 114:461-471. Res 1996, 91 :143-l 48.
An anatomical tracing study, which shows that the preposito-collicular (see Thrs study shows that 50% of the pretecto-geniculate projection neurons
[38’]) projection is organized in two axonal trajectories; in addition, the pro- are GABAergic, but no projection neurons are calbindin- or parvalbumin-
jectron is weighted along the rostrocaudal axis of the contralateral superior Immunoreactive.
colliculus.
51. Schmidt M: Neurons in the cat pretectum that project to
40. Kaneko CRS: Eye movement deficits following ibotenic acid . the dorsal lateral geniculate nucleus are activated during
.. lesions of the nucleus prepositus hypoglossi in monkey. saccades. J Neurophysiol 1996, 76:2907-2918.
I. Saccades and fixation. I Neurophysiol 1997, 78:1763-l 768. Description of a new group of cells in NOT and posterior pretectal nucleus
A chemical lesion study of the prepositus nucleus (ppH) with careful his- that fire with saccades in the light and darkness (in contrast, the jerk neurons
tological controls of the damage, demonstrating only minor deficits in gaze fire only with saccades in light). Unfortunately no differentiation between
holding, no changes of saccades, but impairment of the fixation ability. This NOT and DTN was made.
paper favours the existence of multiple neuronal Integrators rather than of a 52. Mustari MJ, Fuchs AF, Pong M: Response properties of pretectal
single multipurpose element (see [37’]), and it contradicts models that rely . omnidirectional pause neurons in the behaving primate.
on feedback control from the ppH (see [36’,39”1).
J Neurophysiol 1997, 77:116-l 25.
41. Biittner-Ennever JA. Horn AKE: Pathwavs from cell arouos of Description of the physiological properties of a new cell group type in the
. the paramedian tr&ts to the floccula; region. Ann-NYkcad SC; pretectum that pauses after all saccades.
1996, 761:532-540. 53. May PJ, Sun W, Hall WC: Reciprocal connections between the
This study demonstrated for the first time the route taken by the paramedian .. zona incerta and the pretectum and superior colliculus of the
tract (PMT) neurons efferents in the external arcuate fibres to the flocculus cat. Neuroscience 1997, 77:1091-l 114.
and ventral paraflocculus. The PMT cell groups receive inputs similar to the This paper IS a comprehensive study about the connectivity of the zona
extraocular motoneurons, and could provide the cerebellum with a motor lncerta (zi), with the superior colliculus and pretectum using tracer methods
error feedback signal. combined with electron microscopy. The study revealed projections from the
42. Zhang H, Clarke RJ, Gamlin PDR: Behavior of luminance intermediate layers In the superior colliculus to the zi, supporting Its involve-
.. neurons in the pretectal olivary nucleus during the pupillary ment in control of saccades (see [54-I). A stronger incertotectal pathway
near response. fxp Brain Res 1996, 112:156-l 62. was shown to originate primarily from the ventral subdivision of ZI. From the
Shows luminance neurons In the pretectal olive do not fire with the pupillary pretectum, mainly the anterior pretectal nucleus sends an excitatory projec-
constriction accompanying the near-response. This finding is a clear answer tion to the ventral zi.
to the hypothesis that this nucleus might be involved in the near-response 54. Ma TP: Saccade-related omnivectoral pause neurons in the
(see [46”1). It remains to be seen what neural elements in this region are . primate zona incerta. Neuroreporf 1997, 7:2713-2716.
associated with the small motoneurons of the oculomotor nucleus. This is the first detailed descnption of another saccade-related group of
pause-neurons in the zona incerta of monkey. These cells show a similar
43. Kourouyan HD, Horton JC: Transneuronal retinal input to the
.. firing pattern during saccades as the omnipause neurons in the nucleus
primate Edinger-Westphal nucleus. J Comp Neurol 1997,
raphe interpositus, but they have direct probably GABAergic projections to
381:68-80.
the superior colliculus (shown in [53”]).
A satisfying demonstration of the retinal input through the pretectal olive to
the Edinger-Westphal complex with [3H]proline, and a critical account of 55. Dias EC, Kiesau M, Segraves MA: Acute activation and
terminology of the area. inactivation of macaque frontal eye field with GABA-related
drugs. J Neurophysiol 1995, 74:2744-2748.
44. llg UJ, Hoffmann KP: Responses of neurons of the nucleus
. of the optic tract and the dorsal terminal nucleus of the 56. Stanton GB, Bruce CJ, Goldberg ME: Topography of projections
accessory optic tract in the awake monkey. fur J Neurosci to posterior cortical areas from the macaque frontal eye fields.
1996, 8:92-l 05. J Comp Neural 1995, 353:291-305.
Single-cell recording analyzing the role of NOTlDTN in optokinetlc and
smooth pursuit eye movements. Unfortunately, no differentiation between 57. Tian JR, Lynch JC: Corticocortical input to the smooth pursuit
NOT and DTN was made. .. and saccadic eye movement subregions of the frontal eye field
in Cebus monkeys. J Neurophysiol 1996, 76:2754-2771.
45. Klooster J, Vrensen GFJM: The ultrastructure of the The authors demonstrate that the smooth pursuit-frontal eye field (FEF) area
.. olivary pretectal nucleus in rats. A tracing and GABA and saccadlc-FEF area have separate afferent sites within the other cortical
immunohistochemical study. Exp Brain Res 1997, 114:51-62. eye fields. The results imply the parallel flow of smooth pursuit and saccadlc
A technically excellent study of the complex structure of the pretectal olive. information in the cortex rather than a convergence of information. The cebus
and macaque monkey have similar cortical eye fields.
46. Btittner-Ennever JA, Cohen B, Horn AKE, Reisine H: Pretectal
.. projections to the oculomotor complex of the monkey and 58. Leichnetz GR, Gonzalo-Ruiz A: Prearcuate cortex in the Cebus
their role in eye movements. J Comp Neural 1996, 366:346- . monkey has cortical and subcortical connections like the
359. macaque frontal eye field and projects to fastigial-recipient
Pretectal projections to a specific set of oculomotor motoneurons (c-group) oculomotor-related brainstem nuclei. Brain Res Bull 1996,
are verified with transsynaptic retrograde tracer, and suggest a role of the 41 :l -29.
pretectum in the near-response. This is the first attempt to correlate the A comprehensive documentation of cortical and subcortlcal connections of
function of two closely associated components of the pretectum: the NOT the prearcuate cortex (the putative homologue of the frontal eye field) using
and the pretectal olivary nucleus. horseradish peroxidase tracing.
 Anatomical substrates of oculomotor control Btittner-Ennever and Horn 879

59. Petit L, Clark VP, lngeholm J, Haxby JV: Dissociation of saccade-
. related and pursuit-related activation in human frontal eye
fields as revealed by fMRI. J Neurophysiol 1997, 773386-3390.
The study confirms the location of frontal eye fields (FEFs) I” humans and
provides evidence for subdivisions into a pursuit and saccade area.
60. Olson CR, Musil SY, Goldberg ME: Single neurons in posterior
. cingulate cortex of behaving macaque: eye movement signals.
J Neurophysiol 1996, 76:3285-X300.
Establishes saccade-related properties of a cortical area associated with
spatial analysis of visual images.
61. Colby CL, Duhamel JR, Goldberg ME: Visual, presaccadic,
.. and cognitive activation of single neurons in monkey lateral
intraparietal area. I Neurophysiol 1997, 76:2841-2852.
Provides a clever set of paradigms lo tease out the effects of attention and
anticipation on parietal eye field cell responses.
62. Carter N, Zee DS: The anatomical localization of saccades
using functional imaging studies and transcranial magnetic
stimulation. Curr Opln Neural 1997, 10:10-l 7.
63. Sweeney JA, Mintun MA, Kwee S, Wiseman MB, Brown DL,
. Rosenberg DR, Carl JR: Positron emission tomography study
of voluntary saccadic eye movements and spatial working
memory. J Neurophysiol 1996, 75:454-468.
Regions of the cerebral cortex in humans involved in different types of sac-
cadic eye movements are localized with respect to the hand-related motor
cortex (used here as a landmark). The results appear in agreement with
those found in monkey cortex, but the data are extremely difficult to assess
anatomically.
64. Petit L, Orssaud C, Tzourio N, Crivello F, Berthoz A, Mazoyer B:
. Functional anatomy of a prelearned sequence of horizontal
saccades in humans. J Neurosci 1996, 16:3714-3726.
Excltlng results indicating cortical eye fields, basal ganglia and vermis in
internally generated saccade-tasks, but difficult to assess anatomically.
65. Barton JJS, Simpson T, Kirikopoulos E, Stewart C, Crawley A,
.. Guthrie B, Wood M, Mikulis D: Functional MRI of lateral
occipitotemporal cortex during pursuit and motion perception.
Ann Neural 1996, 40:387-398.
A clear discussion on the comparison of human cortical oculomotor func-
tlon with exisrlng results In monkey. The findings show that an area in the
lateral occipitotemporal cortex is related to target motion during pursuit eye
movements, and could represent the human homologue of MT. However,
additional eye-movement-related inputs to this area suggest that MST may
also Ile I” the same region.