The fine organization of nigro-collicular channels with additional observations of their relationships with acetylcholinesterase in the rat

doi:10.1016/S0306-4522(01)00283-4

Neuroscience

Volume 106, Issue 2, 6 September 2001, Pages 357-374

https://doi.org/10.1016/S0306-4522(01)00283-4 Get rights and content

Abstract

The nigro-collicular pathway that links the basal ganglia to the sensorimotor layers of superior colliculus plays a crucial role in promoting orienting behaviors. This connection originating in the pars reticulata and lateralis of the substantia nigra has been shown in rat and cat to be topographically organized. In rat, a functional compartmentalization of the substantia nigra has also been shown reflecting that of the striatum. In light of this, we reinvestigated the topographical arrangement of the nigro-collicular pathway by examining the innervation of each nigral functional zone. We performed small injections of either biocytin or wheatgerm agglutinin conjugated with horseradish peroxidase restricted to identified somatic, visual and auditory nigral zones.

Frontally cut sections showed that innervations provided by the three main nigral zones form a mosaic of complementary domains stratified from the stratum opticum to the ventral part of the intermediate collicular layers, with the somatic afferents sandwiched between the visual and the auditory ones. When reconstructed from semi-horizontal sections, nigral innervations organized in the form of a honeycomb-like array composed of 100 cylindrical modules covering three-quarters of the collicular surface.

Such a modular architecture is reminiscent of the acetylcholinesterase lattice we previously described in rat intermediate collicular layers. In the enzyme lattice, the surroundings of the cylindrical modules are composed of a mosaic of dense and diffuse enzyme subdomains. Thus, we compared the distribution of the overall nigral projection and of its constituent channels with the acetylcholinesterase lattice. The procedure combined axonal labelling with histochemistry on single sections for acetylcholinesterase activity.

The results demonstrate that the overall nigral projection overlaps the acetylcholinesterase lattice and its constituent channels converge with either the dense or the diffuse enzyme subdomains. The stereometric arrangement of the nigro-collicular pathway is suggestive of an architecture promoting the selection of collicular motor programs for different classes of orienting behavior.

Section snippets

Tracer applications

Experiments were carried out in a total number of 29 male Sprague–Dawley rats (Charles River, France). Prior to the surgery, animals were anaesthetized with i.p. injections of sodium pentobarbital (40 mg/kg, Sanofi) and regularly supplemented by intramuscular administration of ketamine (100 mg/kg, Imalgène, Rhône Merieux), in order to maintain a stable level of anesthesia. Iontophoretic injections of either WGA–HRP (Sigma, 2.5% in 0.9% saline) or biocytin (Sigma, 3% in 0.9% saline) were

Frontal plane

This investigation was carried out in three rats. Five applications of WGA–HRP along the anteroposterior and mediolateral axis of the SN (at lateral 2 and 3 mm, and 8 and 7 mm ventral to the cortex surface respectively) were necessary to satisfactorily fill the SNR and SNL (Fig. 1A). Since the SN is encompassed by fibrous systems namely the medial lemniscus, the cerebral peduncles and the optic tract, such applications resulted in tracer diffusion well restricted to the nigral boundaries (with

Discussion

By the use of either WGA–HRP or biocytin as anterograde axonal tracers, the present study provides information about the stereometric arrangement of the nigro-collicular pathway in rat and a detailed description of its major constituent functional channels. Moreover, WGA–HRP injected in SN also allowed identification of the striato–nigro–collicular channels. Finally, by employing a histochemical procedure combining axonal labelling with staining for AChE activity we determined the relationships

Acknowledgements

The authors warmly thank Dr. S. Wiener for providing helpful comments on this manuscript. This work was supported by Grants from CNRS and Université Pierre et Marie Curie, France.

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The fine organization of nigro-collicular channels with additional observations of their relationships with acetylcholinesterase in the rat

Abstract

Section snippets

Tracer applications

Frontal plane

Discussion

Acknowledgements

Parallel organization of functionally segregated circuits linking basal ganglia and cortex

Annu. Rev. Neurosci.

Axonal branching and location of nigrothalamic and nigrocollicular neurons in the cat

J. Neurophysiol.

Ventral temporal cortex in the rat. Connections of secondary auditory areas Te2 and Te3

J. Comp. Neurol.

A comparison of the intranigral distribution of nigrotectal neurons labeled with horseradish peroxidase in the monkey, cat, and rat

J. Neurosci.

The nigrotectal projection in the cat: an electron microscope autoradiographic study

Neuroscience

A cholinergic projection to the rat superior colliculus demonstrated by retrograde transport of horseradish peroxidase and choline acetyltransferase immunohistochemistry

J. Comp. Neurol.

The organization of the efferent projections of the substantia nigra in the rat. A retrograde fluorescent double labeling study

Brain Res.

Collateral projections of predorsal bundle cells of the superior colliculus in the rat

J. Comp. Neurol.

The nigral projection to predorsal bundle cells in the superior colliculus of the rat

J. Comp. Neurol.

Neural substrate of defensive behavior in the midbrain tectum

Neurosci. Biobehav. Rev.

The tectopontine projection in the rat with comments on visual pathway to the basilar pons

J. Comp. Neurol.

Afferent projections to the superior colliculus in the rat, with special attention to the deep layers

J. Hirnforsch.

Bilateral tectal projection of single nigrostriatal dopamine cells in the rat

Neuroscience

Responses of visual, somatosensory and auditory neurons in the Golden hamster’s superior colliculus

J. Physiol.

Inhibitory nigral influence on tectospinal neurons, a possible implication of basal ganglia in orienting behavior

Exp. Brain Res.

Spatio-temporal organization of a branched tecto-spinal/tecto-diencephalic neuronal system

Neuroscience

Disinhibition as a basic process in the expression of striatal functions. I. The striatonigral influence on tecto-spinal/tecto-diencephalic neurons

Brain Res.

Disinhibition as a basic process in the expression of striatal functions

Trends Neurosci.

Evidence that biocytin is taken up by axons

Neurosci. Lett.

Honeycomb-like structure of the intermediate layers of the rat superior colliculus, with additional observations in several other mammals: AChE patterning

J. Comp. Neurol.

GABAergic nigro-collicular pathways modulate the defensive behaviour elicited by midbrain tectum stimulation

Behav. Brain Res.

Event or emergency? Two response systems in the mammalian superior colliculus

Trends Neurosci.

Bilateral projection of nigrocollicular neurons: an electrophysiological analysis in the rat

Neurosci. Lett.

The lamellar organization of the rat substantia nigra pars reticulata: distribution of projection neurons

Neuroscience

The lamellar organization of the rat substantia nigra pars reticulata: segregated patterns of striatal afferents and relationship to the topography of corticostriatal projections

Neuroscience

Topography of visual and somatosensory projections to mouse superior colliculus

J. Neurophysiol.

Topographical organization of the projections from physiologically identified areas of the motor cortex to the striatum in the rat

Neurosci. Res.

A functional analysis of the collicular output pathways: a dissociation of deficits following lesions of the dorsal tegmental decussation and the ipsilateral collicular efferent bundle in the Mongolian gerbil

Exp. Brain Res.

The cells of origin of nigrotectal, nigrothalamic and nigrostriatal projections in the rat

Neuroscience

The visual cortico-striato-nigral pathway in the rat

Neuroscience

Topography of visual and somatosensory projections to the superior colliculus of the golden hamster

Brain Res.

Localization of nigrostriatal, nigrothalamic and nigrotectal neurons in ventricular coordinates in macaques

Neuroscience

Distribution of acetylcholinesterase in the hippocampal region of the guinea pig. I. Entorhinal area, para subiculum and presubiculum

Z. Zellforsch. Mikrosc. Anat.

Crossed connections of the substantia nigra in the rat

J. Comp. Neurol.

An autoradiagraphic study of the efferent connections of the superior colliculus in the rat

J. Comp. Neurol.

A stereometric pattern of distribution of acetylcholinesterase in deep layers of the superior colliculus

Nature

Organization of the nigrotectal connection: an experimental tracer study in the cat