Morphological and physiological identification of excitatory pontine reticular neurons projecting to the cat abducens nucleus and spinal cord

doi:10.1016/0006-8993(80)90359-5

Brain Research

Volume 198, Issue 1, 29 September 1980, Pages 221-228

https://doi.org/10.1016/0006-8993(80)90359-5 Get rights and content

Abstract

The current study provides strong morphological and physiological evidence for identifying reticular neurons which project to the ipsilateral abducens nucleus. In conjunction with recent work in the alert cat, these neurons are believed to be excitatory and are implicated to play a role in the generation of saccadic and/or vestibular fast phase eye movements.

References (22)

J.A. Büttner-Ennever et al.
An autoradiographic study of the pathways from the pontine reticular formation involved in horizontal eye movements
Brain Research
(1976)
S. Cullheim et al.
Combined light and electron microscopic tracing of neurons, including axons and synaptic terminals, after intracellular injection of horseradish peroxidase
Neurosci. Lett.
(1976)
A.A. Grantyn et al.
Synaptic actions of tectofugal pathways on abducens motoneurons in the cat
Brain Research
(1976)
S.M. Highstein et al.
Synaptic input from the pontine reticular nuclei to abducens motoneurons and internuclear neurons in the cat
Brain Research
(1976)
Y. Igusa et al.
Excitotory premotor burst neurons in the cat pontine reticular formation related to the quick phase of vestibular nystagmus
Brain Research
(1980)
R.J. Maciewicz et al.
Vestibular and medullary brain stem afferents to the abducens nucleus in the cat
Brain Research
(1977)
H.-J. Steiger et al.
Relationship between motoneurons and internuclear neurons in the abducens nucleus: a double retrograde tracer study in the cat
Brain Research
(1978)
V. Büttner et al.
Neurons in the rostral mesencephalic and paramedian pontine reticular formation generating fast eye movements
C. Evinger et al.
Omnipauser cells in the cat

A. Grantyn et al.

Neuronal organization of the tecto-oculomotor pathways

Cited by (40)

The local loop of the saccadic system closes downstream of the superior colliculus
2006, Neuroscience
Citation Excerpt :
These authors provided a substantial list of fibers and neurons likely to mediate them. Briefly, they include collicular efferents deploying terminal fields in the abducens nucleus (Grantyn and Grantyn, 1982; Grantyn and Berthoz, 1985; Olivier et al., 1993), reticulospinal neurons which receive input from the SC and project to the abducens nucleus (Grantyn et al., 1980, 1987), neurons of the PH which also receive input from the SC and project to the abducens nucleus (Grantyn and Grantyn, 1982; Grantyn and Berthoz, 1985; Olivier et al., 1993) and tectorecipient reticulospinal neurons which discharge during orienting eye–neck synergies and give substantial collateral projections to both the PH and the medial vestibular nucleus (Grantyn et al., 1980, 1987, 1992). Since, most of the tectal efferents participating in these projections pass through the PDB, their stimulation and the generation of slow drifts were unavoidable in a majority of our stimulation sites.
Models of the saccadic system differ in several respects including the signals fed back to their comparators, as well as the location and identity of the units that could serve as comparators. Some models place the comparator in the superior colliculus while others assign this role to the reticular formation. To test the plausibility of reticular models we stimulated electrically efferent fibers of the superior colliculus (SC) of alert cats along their course through the pons, in the predorsal bundle (PDB). Our data demonstrate that electrical stimulation of the PDB evokes saccades, even with stimuli of relatively low frequency (100 Hz), which are often accompanied by slow drifts. The velocity and latency of saccades are influenced by the intensity and frequency of stimulation while their amplitude depends on the intensity of stimulation and the initial position of the eyes. The dynamics of evoked saccades are comparable to those of natural, self-generated saccades of the cat and to those evoked in response to the electrical stimulation of the SC. We also show that PDB-evoked saccades are not abolished by lesions of the SC and that therefore antidromic activation of the SC is not needed for their generation. Our data clearly demonstrate that the burst generator of the horizontal saccadic system is located downstream of the SC. If it is configured as a local loop controller, as assumed by most models of the saccadic system, our data also demonstrate that its comparator is located beyond the decussation of SC efferent fibers, in the pons.
The microscopic anatomy and physiology of the mammalian saccadic system
1996, Progress in Neurobiology
A central goal of the Neurosciences is to provide an account of how the brain works in terms of cell groups organised into pattern generating networks. This review focuses on the neural network that generates the rapid movements of the eyes that are called saccades. A brief description of the metrical and dynamical properties of saccades is provided first. Data obtained from lesion and electrical stimulation experiments are then described; these indicate that the relevant neural machinery spreads over at least 10 distinct cortical and subcortical regions of the brain. Each one of these regions harbors several distinct classes of saccade related cells (i.e. cells whose discharge encodes the metrical and often dynamical properties of saccades). The morphological and physiological properties of about 30 saccade related cell classes are described. To generate the signals they carry, and therefore saccades, distinct classes of cells influence each other in a non-random manner. Anatomical evidence is provided that indicates the existence of about 100 distinct connections established between saccade related neurons. The overall picture of the saccadic system that emerges from these studies is one of intricate complexity. In part this is due to the presence of at least 3, multiply interconnected negative feedback loops. Several computational models of the saccadic system have been proposed in an attempt to understand the functional significance of the simultaneous operation of these loops. An evaluation of these models demonstrates that besides providing a coherent summary of the data that concern it, successful models of the saccadic system generate realistic saccades (in precise quantitative psychophysical terms) when their elements are stimulated, produce abnormal saccades, reminiscent of those encountered in the clinic, when their elements are disabled, while their constituent units display realistic discharge patterns and are connected in a manner that respects anatomy.
Tonic activity during visuo-oculomotor behavior in the monkey superior colliculus
1996, Neuroscience Research
The purpose of this study was to examine whether the superior colliculus is involved in intermediary cognitive processes such as memory, movement preparation, and peripheral attention. To answer this question, we recorded single cell activities in the superior colliculus of monkeys trained to perform a series of visuo-oculomotor tasks: delayed saccade task (SACD), saccade task with overlap target (SACO), and attention task (ATT). We recorded 141 neurons showing tonic activities related to the tasks. Depending on the predominance of the activities among the three tasks, we classified the tonic neurons into four types: (1) visuomotor (greater activity in SACO), (2) mnemonic motor (SACD dominant), (3) attention (ATT), and (4) nonspecific. Among 108 neurons recorded in the intermediate layer, 13 were of a visuomotor type, 15 were of a mnemonic motor type, and 13 were of an attention type. The other 67 neurons were of a non-specific type. Of the 33 neurons in the superficial layer, many neurons were of the non-specific type. These results suggested that the tonic activities in the superior colliculus are related to memory of the target location, preparation of saccades and peripheral attention.
Glycine-mediated inhibitory postsynaptic potentials in the medial pontine reticular formation of the rat in vitro
1996, Neuroscience
Glycinergic neurotransmission was examined in rat medial pontine reticular formation neuronsin vitro. Intracellular recordings using glass microelectrodes were made in acutely prepared brainstem slices 400 it m thick. Spontaneous and electrically evoked synaptic activity was blocked by the glycine antagonist strychnine (1–5 μM) but not by the GABA antagonists bicuculline methiodide (40 μM) or picrotoxin (40 μM). Strychnine-sensitive spontaneous and evoked postsynaptic potentials persisted in the presence of the glutamate antagonist (kynurenate, 1 mM). Whole-cell voltage-clamp recordings were carried out in organotypic cultures of rat brainstem. The reversal potential of synaptic currents and responses to exogenously applied glycine were similar and were sensitive to manipulations of the chloride equilibrium potential. Synaptic activity but not responses to exogenous glycine were blocked by tetrodotoxin (0.3 μM).
These results indicate the presence of robust, chloride ion-mediated glycinergic inhibition of medial pontine reticular formation neurons, and suggest that glycinergic neurons play an important role in controlling pontine premotor circuitry.
Neuronal mechanisms of two-dimensional orienting movements in the cat. I. A quantitative study of saccades and slow drifts produced in response to the electrical stimulation of the superior colliculus
1996, Brain Research Bulletin
To evaluate the metrics of rapid eye movements caused by the activation of distinct collicular microzones, the superior colliculus (SC) was electrically stimulated in alert behaving cats while their heads were restrained. A quantitative study of electrically induced rapid eye movements demonstrated that their amplitude and direction depended on the intensity of stimulation, the electrode location, and the initial position of the eyes, while their duration depended on the intensity of stimulation. When detailed quantitative procedures are employed, properties of saccades produced in response to the electrical stimulation of the feline SC resemble those of saccades elicited in response to the electrical stimulation of a variety of primate brain areas. Besides saccades, electrical stimulation of the feline SC gave rise to slow drifts whose amplitude and direction was also influenced by the initial position of the eyes. Because their size depended on the frequency of stimulation and their time course reflected mechanical properties of theoculomotor plant, induced slow drifts could be due to a more or less direct projection of the SC onto extraocular motoneurons. A model that includes such a variety of connections between the SC and extraocular motoneurons is presented and is shown to produce realistic combinations of fast and slow eye movements when its input is a step function of time. The present findings support the notion that an orbital mechanical factor underlies the eye position sensitivity of slow drifts and saccades evoked in response to the electrical stimulation of the SC.
Innervation of multiple neck motor nuclei by single reticulospinal tract axons receiving tectal input in the upper cervical spinal cord
1994, Neuroscience Letters
Axons of reticulospinal neurons (RSNs) activated monosynaptically by stimulation of the contralateral superior colliculus (SC) were stained with intraaxonal injection of horseradish peroxidase in the cat upper cervical spinal cord. Stem axons of single RSNs gave rise to multiple axon collaterals to laminae IX, VIII and VII over a few cervical segments. Single RSNs made contacts with retrogradely labeled neck motoneurons of different neck muscles. Therefore, RSNs were regarded as mediating output of the SC to functionally different groups of neck muscles simultaneously. The result gave evidence of neural implementation of a functional synergy for a neck movement at a single neuron level.

View all citing articles on Scopus

^☆: Supported by United States Public Health Service Grants, EY-02007 from the National Eye Institute and NS-13742 from the National Institute of Neurological and Communicative Disorders and Stroke.

View full text

Short communicationMorphological and physiological identification of excitatory pontine reticular neurons projecting to the cat abducens nucleus and spinal cord☆

Abstract

Brain Research

Neurosci. Lett.

Brain Research

Brain Research

Brain Research

Brain Research

Brain Research

Neurons in the rostral mesencephalic and paramedian pontine reticular formation generating fast eye movements

Omnipauser cells in the cat

Neuronal organization of the tecto-oculomotor pathways

Short communication
Morphological and physiological identification of excitatory pontine reticular neurons projecting to the cat abducens nucleus and spinal cord☆