Influences of afferent neurons on efferent neurons. II. Some specific effects of deafferentation on central and efferent neurons.
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Efferent neurons in isolated pedal ganglia of the pteropodial mollusc Clione limacina were filled with Lucifer Yellow through the wing nerves. Then the ganglia were illuminated with intense blue light which resulted in the complete inactivation of these neurons. After inactivation of efferent neurons, interneurons of the pedal ganglia continued to generate the locomotor rhythm.
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This study provides a description of the organization of neurons efferent to different head areas in the cerebral ganglia of Helix pomatia, revealed by simultaneous Ni-lysine and Co-lysine back-filling of different pairs of cerebral nerves. The backfills show that labeled cerebral neurons that innervate the head areas are concentrated in seven representation foci distributed in different parts of the cerebral ganglia. Almost each head area is represented in each focus. At a gross level, the representation of the different head areas in the representation foci shows a topographic arrangement. Each focus is constituted by neurochemically different groups of neurons. All head areas are innervated by serotonin-containing fibers from a single focus (Focus 2) and by dopamine-containing fibers from Foci 1, 2, and 4. However, they are innervated by CARP and FMRFamide-containing fibers from all of the foci. The combination of retrograde labeling with 5, 6-dihydroxytriptamine induced pigment labeling of serotonin-containing neurons or with fluorescence tyrosinehydroxylase immunocytochemistry to detect dopamine-containing neurons showed that the different head areas are topographycally represented in the clusters of both the serotonin- and dopamine-containing cells. The combination of Ni-lysine backfillings from different cerebral nerves with fluorescence CARP and FMRFamide immunocytochemistry revealed that the head areas are represented also in both the CARP and FMRFamide immunoreactive groups of neurons in the different foci.
The distribution of vestibular efferent neurons projecting to the saccule and efferent neurons transmitting axons to the acoustic nerve (cochlear efferent neurons) has been studied in guinea pig by comparison using the method of retrograde axonal transport of horseradish peroxidase. The saccular efferent neurons are revealed bilaterally in the subendymal granular fundus of the fourth ventricle of the brain and more laterally of the facial nerve genu, ipsilaterally in the small-celled reticular nucleus as well as in nuclei of the supraolivary complex: nucleus of lateral oliva and lateral nucleus of the trapezoid body. The cochlear efferent neurons are localized ipsilaterally in the reticular caudal nucleus of the bridge in the anteroventral cochlear nucleus and in nuclei of lateral and medial olivae. In the medial nucleus of the trapezoid body such neurons are found contralaterally. Thus, the regions of the vestibular saccular efferent neurons are partially overlapped with such of the cochlear efferent units. Possible participation of the vestibular efferent neurons of the saccule in the mechanism of the acoustic perception is discussed.
Efferent neurones within the intraganglionic spiral bundle of the guinea pig cochlea were characterized in terms of their response properties, and their pattern of termination within the receptor organ revealed by intracellular labelling with horseradish peroxidase. All neurones subsequently identified as efferent neurones had clear features of their response properties which distinguished them from primary auditory afferents. They had long latency, low maximum discharge rate and low levels of spontaneous activity under Nembutal/Innovar anaesthesia. The pattern of discharge was extremely regular, revealed by symmetrical interspike interval histograms. 49.4% responded best to ipsilateral, 43.3% to contralateral sound and a third group of 7.3% responded equally well to either ipsilateral or contralateral sound. In cochleae in good physiological condition, these efferents were as sensitive and as sharply tuned as primary afferents with the same characteristic frequencies (CFs). All efferents fully traced in histological processing terminated on the outer hair cells. Several efferents showed extensive branching beneath the inner hair cells which might represent en passant synapses with other neuronal elements. There was clear evidence of tonotopic organization of the efferent projection. The site of termination on the outer hair cells in most instances was very close to the region of the cochlea predicted from the fibres' CF and the known place-frequency map for primary afferent neurones in the guinea pig.
Anterograde labeling techniques were used to examine peripheral innervation patterns of vestibular efferent neurons in the crista ampullares of the gerbil. Vestibular efferent neurons were labeled by extracellular injections of biocytin or biotinylated dextran amine into the contralateral or ipsilateral dorsal subgroup of efferent cell bodies (group e) located dorsolateral to the facial nerve genu. Anterogradely labeled efferent terminal field varicosities consist mainly of boutons en passant with fewer of the terminal type. The bouton swellings are located predominately in apposition to the basolateral borders of the afferent calyces and type II hair cells, but several boutons were identified close to the hair cell apical border on both types. Three-dimensional reconstruction and morphological analysis of the terminal fields from these cells located in the sensory neuroepithelium of the anterior, horizontal, and posterior cristae were performed. We show that efferent neurons densely innervate each end organ in widespread terminal fields. Subepithelial bifurcations of parent axons were minimal, with extensive collateralization occurring after the axons penetrated the basement membrane of the neuroepithelium. Axonal branching ranged between the 6th and 27th orders and terminal field collecting area far exceeds that of the peripheral terminals of primary afferent neurons. The terminal fields of the efferent neurons display three morphologically heterogeneous types: central, peripheral, and planum. All cell types possess terminal fields displaying a high degree of anisotropy with orientations typically parallel to or within +/-45 degrees of the longitudinal axis if the crista. Terminal fields of the central and planum zones predominately project medially toward the transverse axis from the more laterally located penetration of the basement membrane by the parent axon. Peripheral zone terminal fields extend predominately toward the planum semilunatum. The innervation areas of efferent terminal fields display a trend from smallest to largest for the central, peripheral, and planum types, respectively. Neurons that innervate the central zone of the crista do not extend into the peripheral or planum regions. Conversely, those neurons with terminal fields in the peripheral or planum regions do not innervate the central zone of the sensory neuroepithelium. The central zone of the crista is innervated preferentially by efferent neurons with cell bodies located in the ipsilateral group e. The peripheral and planum zones of the crista are innervated preferentially by efferent neurons with cell bodies located in the contralateral group e. A model incorporating our anatomic observations is presented describing an ipsilateral closed-loop feedback between ipsilateral efferent neurons and the periphery and an open-loop feed-forward innervation from contralateral efferent neurons. A possible role for the vestibular efferent neurons in the modulation of semicircular canal afferent response dynamics is proposed.
A bilateral projection from the vestibular efferent neurons, located dorsal to the genu of the facial nerve, to the cerebellar flocculus and ventral paraflocculus was demonstrated. Efferent neurons were double-labeled by the unilateral injections of separate retrograde tracers into the labyrinth and into the floccular and ventral parafloccular lobules. Efferent neurons were found with double retrograde tracer labeling both ipsilateral and contralateral to the sites of injection. No double labeling was found when using a fluorescent tracer with non-fluorescent tracers such as horseradish peroxidase (HRP) or biotinylated dextran amine (BDA), but large percentages of efferent neurons were found to be double labeled when using two fluorescent substances including: fluorogold, microruby dextran amine, or rhodamine labeled latex beads. These data suggest a potential role for vestibular efferent neurons in modulating the dynamics of the vestibulo-ocular reflex (VOR) during normal and adaptive conditions.
Collateral branching of efferent neurons' axons in the cat parietal associative cortex was studied with intracellular recording of antidromic activity. Specific features of the axon collaterals projecting onto the sensorimotor cortex, pontine nuclei proper and red nucleus, were revealed and described. Information arriving from the parietal cortex simultaneously at the above two motor structures suggests their interrelationship to be actualized through the axon collaterals of efferent neurons. This kind of functional interrelationship of the structures via axon branching of efferent neurons of the parietal cortex provides synchronous arrival of signals at the structures participating in motor integration.
Vagal efferent neurons innervating the digestive tract are mainly contained in the dorsal motor nucleus of the vagus. Previous studies have suggested that neurokinins and their neurokinin-1 and neurokinin-3 receptors are involved in the parasympathetic control of digestive functions. The purpose of the present study was to analyze the distribution of neurokinin-1 and neurokinin-3 receptors amongst vagal efferent neurons innervating the stomach, the duodenum, the ileum and the cecum. The immunocytochemical detection of neurokinin-1 and neurokinin-3 receptors was combined with the immunocytochemical detection of retrogradely transported cholera toxin-B subunit, previously injected in the gut wall. Neurokinin-1 and neurokinin-3 receptors were present in 19+/-7% and 8+/-3% of retrogradely labeled neurons innervating the stomach. Almost half of the labeled neurons innervating the duodenum (46+/-7%) expressed neurokinin-1 receptors but less than 0.5% contained neurokinin-3 receptors. None of the retrogradely labeled vagal efferent neurons innervating the ileum and the cecum were immunoreactive for neurokinin-1 and neurokinin-3 receptors. We conclude that neurokinin-1 and neurokinin-3 receptors are located on vagal efferent neurons which innervate the stomach and that neurokinin-1 receptors are common, whereas neurokinin-3 receptors are rare on neurons projecting to the duodenum. Additionally, the distal part of the rat small intestine is innervated by vagal efferent neurons that do not express neurokinins receptors on their membrane. This suggests that neurokinins may influence the parasympathetic control of different regions of the gastro-intestinal tract in specific ways.
We applied choline acetyltransferase, (ChAT) and calcitonin gene-related peptide (CGRP) immunocytochemistry to the efferent neurons that innervate the lateral line and the ear of the eel. Strong immunoreactivity to the ChAT antiserum was observed in neurons located within the octavolateralis efferent nucleus that could be distinguished, on the basis of their form, location and dendritic organization, from the ChAT-immunopositive motoneurons of the adjacent facial motor nucleus. Both facial motoneurons and efferent neurons were found to be immunopositive for CGRP, although the reaction was always stronger in the motoneurons. Double labelling experiments established the presence of both ChAT and CGRP in many efferent neurons. The results are evidence that cholinergic efferent neurons supplying end organs of different modalities may also produce calcitonin gene-related peptide.
The octavo-lateral efferent system of several anuran species was studied by means of retrograde transport of horseradish peroxidase. This system is organized similarly in all larval anurans and in all adult aglossids. All have two groups of efferent neurons in the nucleus reticularis medialis between the VIIIth and the IXth motor nucleus. The caudal group consists of efferent neurons that supply the posterior lateral-line nerve (NLLp) and a considerably smaller group of neurons supplying both the NLLp and the anterior lateral-line nerve (NLLa). The rostral group is composed of efferent neurons supplying the NLLa, neurons projecting to the inner ear and neurons supplying both the inner ear and the NLLa. Efferent neurons of the VIIIth cranial nerve exhibit a rostrocaudal cytoarchitectonic differentiation. Caudal perikarya, which are rounder in shape than those of the rostral part, have a dendritic projection to the superior olive. It is suggested that this differentiation reflects a functional differentiation of acoustic and vestibular efferent neurons. Labeled neurons were ipsilateral to the site of application of HRP. None were found in the vestibular nuclei or in the cerebellum. Efferent axons projecting to neuromasts of the NLLa leave the medulla with the VIIth nerve, axons projecting to neuromasts of the NLLp exit via the IXth nerve. Cell counts and the observation of axonal branching revealed that efferent units of both the lateral-line and the VIIIth-nerve system supply more than one receptor organ. In contrast to the lateral-line system, dendrites of efferent neurons of the VIIIth nerve project dorsally onto its nuclei, and afferents of the VIIIth nerve project onto efferent neurons. These structures most probably represent a feedback loop between the afferent and efferent systems of the VIIIth cranial nerve.
Efferent neurons of the deeper layers of the cat's superior colliculus were stained with horseradish peroxidase (HRP) to demonstrate patterns of somatodendritic morphology and axonal trajectory. A combination of somatodendritic and axonal features of the HRP-labeled cells revealed the existence of three major groups of tectal efferent neurons (X, T, and I). X neurons are mostly large and multipolar and participate in the crossed descending and ipsilateral ventral ascending projections of the superior colliculus. The X group includes multipolar radiating (X1), tufted (X2), large vertical (X3), medium-sized vertical (X4), and medium-sized horizontal (X5) neurons. T neurons participate in one or two of the major tectofugal bundles (medial descending ipsilateral, lateral descending ipsilateral, medial dorsal ascending, crossed descending) besides providing a commissural branch. They also issue recurrent collaterals distributed within a more or less restricted area of the deeper layers. The T group includes medium-sized, trapezoid, radiating (T1) and small or medium-sized, ovoid, vertical (T2) neurons. I neurons participate in the ipsilateral descending projection of the superior colliculus. They are small, triangular or ovoid, sparsely ramified cells that provide long, varicose collaterals irregularly distributed within the deeper layers. The majority of T neurons are located in the ventral stratum opticum or dorsal stratum griseum intermediale; X3 and X5 neurons are situated immediately below in the dorsal stratum griseum intermediale, while X1, X2, X4, and I neurons are indiscriminately distributed within the deeper layers. The polythetic classification presented here provides a conceptual framework for the description of tectal efferent neurons. It is open-ended and can thereby accommodate new cells types as indicated by the disclosure of a small horizontal (A) and a small radiating (unclassified) neuron. Moreover, it does not preclude the construction of alternate taxonomies. A dendro-architectonic classification into four groups [vertical (X3, X4, T2, I), horizontal (X5, A), radiating (X1, T1, I), and tufted (X2)] can be made and would relate to the mode of integration of various tectopetal inputs. A classification based on the dorsoventral location of tectal efferent neurons is also possible and would relate to the dorsoventral distribution of neurons with specific response properties.
1. The behavioral tractability of the rabbit was exploited and enabled, in the fully awake state, receptive-field analysis of antidromically identified efferent neurons within the vibrissa representation of primary somatosensory cortex (S-1). Efferent neurons studied included ipsilateral corticocortical neurons (C-IC neurons, n = 56) that project to or beyond the second somatosensory cortical area (S-2) and corticofugal neurons of layer 5 (CF-5 neurons, n = 75) and layer 6 (CF-6 neurons, n = 92) that project to and/or beyond the thalamus. 2. An additional class of neurons was studied that was not activated antidromically from any stimulus site, but which responded synaptically to electrical stimulation of the ventrobasal (VB) thalamus with a burst of three or more spikes at frequencies of 600 to greater than 900 Hz. Most of these neurons also responded synaptically to stimulation of S-2. The action potentials of these neurons were much shorter (mean = 0.43 ms), than those of efferent neurons (mean = 0.98 ms). Such properties have been associated with interneurons found throughout the central nervous system, and these neurons are thereby referred to as suspected interneurons (SINs). Although SINs were found at all cortical depths, a strong peak in the distribution occurred just superficial to the peak in the distribution of CF-5 neurons. Most SINs located within this peak responded to deflection of only a single vibrissa. In contrast, SINs located in layer 6 and in layer 2-3 responded to deflection of many vibrissae (median = 11.0 and 5.5 vibrissae, respectively). In addition, SINs of layer 6 and layer 2-3 had significantly longer synaptic latencies to stimulation of VB thalamus than did SINs located at intermediate cortical depths. 3. The properties of efferent neurons and SINs differed considerably. Efferent neurons never responded to stimulation of VB thalamus with the high-frequency burst of spikes characteristic of SINs. Although greater than 70% of CF-6, CF-5 and C-IC neurons had receptive fields that were directionally selective, only 20% of SINs showed any degree of directional selectivity. Furthermore, SINs showed both much lower angular thresholds to vibrissa deflection and a much greater ability to follow high-stimulus frequencies than was seen in efferent neurons. The spontaneous firing rates of SINs had a mean value of 16.5 spikes/s, which was the highest seen in any population within S-1. 4. CF-5 neurons had a number of properties which contrasted with those of both CF-6 and C-IC neurons.(ABSTRACT TRUNCATED AT 400 WORDS)
Vertebrate hair cell systems receive innervation from efferent neurons in the brain. Here we report the responses of octavolateral efferent neurons that innervate the inner ear and lateral lines in a teleost fish, Dormitator latifrons, to directional linear accelerations, and compare them with the afferent responses from the saccule, the main auditory organ in the inner ear of this species. Efferent neurons responded to acoustic stimuli, but had significantly different response properties than saccular afferents. The efferents produced uniform, omnidirectional responses with no phase-locking. Evoked spike rates increased monotonically with stimulus intensity. Efferents were more broadly tuned and responsive to lower frequencies than saccular afferents, and efferent modulation of the otolithic organs and lateral lines is likely more pronounced at lower frequencies. The efferents had wide dynamic ranges, shallow rate-level function slopes, and low maximum discharge rates. These findings support the role of the efferent innervation of the otolithic organs as part of a general arousal system that modulates overall sensitivity of the peripheral octavolateral organs. In addition, efferent feedback may help unmask biologically relevant directional stimuli, such as those emitted by a predator, prey, or conspecific, by reducing sensitivity of the auditory system to omnidirectional ambient noise.
1. Intracellular recordings were made, in vitro, fron neurones located within left renal ganglia and left coeliac ganglia of cat solar plexus. 2. Forty-three percent of the neurones of the renal ganglia tested were identified by antidromic activation as renal-efferent neurones. 3. Electrical stimulation of all nerve trunks emanating from renal ganglia, other than the renal nerves, did not antidromically activate renal ganglia neurones. Neurones not antidromically activated were designated as non-efferent neurones. 4. Neurones within the renal ganglia were also characterized as phasic or tonic neurones depending on their pattern of discharge. 5. Electrical stimulation of renal nerves produced excitatory synaptic potentials (e.p.s.p.s) in 18% of the renal-efferent neurones. 6. Compounded e.p.s.p.s were produced in 50% of the renal ganglia neurones tested by stimulation of the ipsilateral splanchnic nerves and in 84% of the neurones upon stimulation of the vertebral nerve. 7. Synaptic responses demonstrating characteristics typical of those induced by activation of multisynaptic neural pathways were produced upon stimulation of renal and coeliac nerves. 8. The results of this study indicate that the electrophysiological properties of renal-efferent neurones vary considerably from neurone to neurone and that these neurones receive synaptic inputs from a variety of preganglionic fibres and possibly from other neurones having their soma located within the solar plexus.
Responses of parietal association cortex efferent neurons to motor cortex and cerebellar nuclei stimulation were studied intracellularly in anaesthetized cats. Efferent neurons of the parietal cortex were identified according to their antidromic activation on stimulation of the motor cortex, pontine nuclei proper and red nucleus. Monosynaptic excitatory postsynaptic potentials of ipsilateral anterior suprasylvian and lateral gyri neurons to motor cortex stimulation have been established. Oligo- and polysynaptic excitatory responses of parietal cortex efferent neurons to cerebellar nuclei stimulation have been recorded. Correlation between the latencies of cerebellar-induced excitatory postsynaptic potentials and antidromic invasion of neurons on stimulation of different parietal cortex efferent projections (corticocortical, corticopontine, corticorubral) has been obtained. A similar correlation has been found between the latencies of excitatory postsynaptic potentials evoked on stimulation of one of the cerebellar nuclei and latencies of antidromic invasion induced on stimulation of all studied parietal cortex efferent systems. Feedforward and feedback mechanisms in the input-output organization of parietal association cortex have been discussed.
The laminar and size distribution of commissural efferent neurons were studied in the cat visual cortex including area 17, 18, 19 and the lateral suprasylvian cortex (the lateral wall of the middle suprasylvian gyrus) by means of retrograde transport of horseradish peroxidase. Single or multiple injections of the enzyme were made unilaterally along the medial part of the lateral gyrus (the adjoining parts of area 17 and 18) or along the lateral wall of the middle suprasylvian gyrus. In the contralateral cerebral cortex (area 17, 18, 19 and lateral suprasylvian cortex) the majority of peroxidase labeled commissural efferent neurons was identified in layer III with a smaller population in other layers except layer I. The size distribution of labeled cells of layer III showed that all sizes of neurons contribute to interhemispheric connections, ranging from small cells which are comparable to those predominating in layer III of the acommissural medial area 17 to the characteristic large pyramides of layer III at the area 17/18 boundary. There was a certain difference in the pattern of size distribution of commissural efferent neurons of layer III between area 17, 18, 19 and the lateral suprasylvian cortex. Labeled neurons in area 17, 18, 19 showed a dominant peak in the histograms of cell size, while in the lateral suprasylvian cortex they were more evenly distributed in a wide size range.