Intercollicular Area Research Articles

Perineuronal nets and subtypes of GABAergic cells differentiate auditory and multisensory nuclei in the intercollicular area of the midbrain.

The intercollicular region, which lies between the inferior and superior colliculi in the midbrain, contains neurons that respond to auditory, visual, and somatosensory stimuli. Golgi studies have been used to parse this region into three distinct nuclei: the intercollicular tegmentum (ICt), the rostral pole of the inferior colliculus (ICrp), and the nucleus of the brachium of the IC (NBIC). Few reports have focused on these nuclei, especially the ICt and the ICrp, possibly due to lack of a marker that distinguishes these areas and is compatible with modern methods. Here, we found that staining for GABAergic cells and perineuronal nets differentiates these intercollicular nuclei in guinea pigs. Further, we found that the proportions of four subtypes of GABAergic cells differentiate intercollicular nuclei from each other and from adjacent inferior collicular subdivisions. Our results support earlier studies that suggest distinct morphology and functions for intercollicular nuclei, and provide staining methods that differentiate intercollicular nuclei and are compatible with most modern techniques. We hope that this will help future studies to further characterize the intercollicular region.

Regional distribution of the anticonvulsant and behavioural effects of bicuculline injected into the pontine reticular formation of rats.

Previous experimental work has established that activation of sites in the dorsal midbrain can suppress tonic hindlimb extension in the electroshock model of epilepsy. The most sensitive region for this effect is centred on the intercollicular area and is referred to as the dorsal midbrain anticonvulsant zone (DMAZ). Subsequent experiments have shown that the ipsilateral descending projection from this region to the ventrolateral pons is critically involved in mediating its tonic seizure-suppressing properties. The purpose of the present investigation was to test whether direct anticonvulsant effects in the electroshock model could be obtained from selective manipulation of DMAZ target regions in the ventrolateral pons. Animals were prepared with chronically implanted guide cannulae through which microinjections could be made directly into the lateral pontine reticular formation. Animals received injections of saline or bicuculline (25-100 pmol) administered either bilaterally or unilaterally. The effects of these injections on the animals' behaviour were determined in an open arena, after which maximal electroshock (1 s, 40 mA, 50 Hz AC) was administered via ear-clip electrodes and the duration of tonic hindlimb extension was recorded. Bilateral injections of bicuculline (100 pmol) suppressed tonic seizures at a significantly higher proportion of sites centred on DMAZ target regions of the ventrolateral pons than surrounding areas. For injections centred on this region the suppressive effects of bicuculline were dose-related in the range 25-100 pmol. Unilateral injections of bicuculline into the ventrolateral pons also effectively suppressed tonic seizures in the electroshock model. Within the ventral pons there was a significant association between the behavioural and anticonvulsant effects of bicuculline; injections suppressing tonic seizures were associated with the induction of fast continuous locomotor activity. These data confirm that the DMAZ recipient region of the ventrolateral pontine reticular formation is part of a circuit which can suppress the manifestation of tonic hindlimb extension in the electroshock model. Whether this property is related to the participation of this region in normal locomotion and posture remains to be determined.

The dorsal midbrain anticonvulsant zone—II. Efferent connections revealed by the anterograde transport of wheatgerm agglutinin-horseradish peroxidase from injections centred on the intercollicular area in the rat

Activation of the dorsal midbrain has a powerful anticonvulsant effect in the maximal electroshock model of epilepsy. The suppression of tonic seizures can be obtained most reliably from an area centred on the intercollicular nucleus overlapping into the deep layers of the superior colliculus and adjacent mesencephalic reticular formation. As part of a series of investigations to identify neural mechanisms responsible for mediating the anticonvulsant properties of the dorsal midbrain, the present study provides an anatomical description of the efferent projections of this region. Small amounts of wheatgerm agglutinin-horseradish peroxidase (10-30 nl of a 1% solution) were injected into the intercollicular nucleus and surrounding tissue. The resulting anterograde transport of the tracer was plotted on a set of standard atlas sections. Four major output pathways were identified: (i) an ipsilateral descending projection which had terminations in the microcellular tegmental nucleus, lateral and ventral pontine reticular nucleus pars oralis, ventrolateral tegmental nucleus, ventral and caudal pontine reticular nucleus pars caudalis, raphe magnus nucleus and the gigantocellular nucleus; (ii) a contralateral descending projection which for the most part targeted the same brainstem structures but with weaker terminal labelling; (iii) a projection to the contralateral dorsal midbrain with comparatively weak terminal label in the contralateral superior colliculus, intercollicular nucleus, periaqueductal gray, mesencephalic reticular formation and cuneiform area; (iv) ipsilateral ascending pathway with terminations in the red nucleus, zona incerta, peripeduncular area, parafascicular nucleus, lateral hypothalamus, parts of the pretectum and caudal thalamus. At a general level the dorsal midbrain anticonvulsant zone shares its major output projections and efferent targets with at least one of its near neighbours, including the superior colliculus, periaqueductal gray, the cuneiform nucleus and pedunculopontine nucleus. The possibility that anticonvulsant properties of the intercollicular area can simply be attributed to a unique set of efferent projections is therefore not supported by the anatomy.

New subdivision schema for the avian torus semicircularis: Neurochemical maps in the chick

Chemoarchitectonic subdivisions in the chicken torus semicircularis were mapped by means of acetylcholinesterase histochemistry and immunocytochemical labeling of leucine-enkephalin, choline acetyltransferase, neuropeptide Y, and calbindin/calretinin in adjacent sections. The torus semicircularis was found to consist of three main divisions: intercollicular area, toral nucleus, and preisthmic superficial area. All three appear variously subdivided. The intercollicular area is a mid-mesencephalic ventral periventricular region and appears subdivided into core and shell intercollicular regions. The toral nucleus is formed by a large caudal periventricular cytoarchitectonic complex, consisting of a periventricular lamina subdivided into core and shell regions, a pericentral, diffuse external nucleus, a central nucleus subdivided into core and shell regions, a caudomedial shell nucleus, a paracentral nucleus, and a posterior hiliar nucleus, apart from other minor parcellations. The preisthmic superficial area extends superficially at the caudomedial end of the toral nucleus, reaching the paramedian dorsal brain surface just rostral to the isthmo-optic nucleus. It is subdivided into core and shell regions. This previously unnoticed area is distinguished here from the intercollicular area and from the caudomedial shell and paracentral nuclei, all of which are frequently mixed in the literature under the concept "intercollicular nucleus." The revised terminology and subdivision for the avian torus clarifies many chemoarchitectonic and hodological mappings reported in the literature. It also suggests new research subjects and eliminates some causes of confusion.

Immunohistochemical localization of neuropeptides in the vocal control regions of two songbird species

Immunohistochemistry was used to map the distribution of four neuropeptides in song control regions of two songbird species, the European starling (Sturnus vulgaris) and the song sparrow (Melospiza melodia). We searched for positively stained cell bodies or apparent terminals containing vasoactive intestinal peptide (VIP), methionine-enkephalin (MET), cholecystokinin (CCK), and substance P (SUB P). Intraventricular colchicine pretreatment was administered to enhance the visualization of peptide-containing cell bodies. Four areas implicated in the central control of song were examined. Three of these areas are sexually dimorphic telencephalic nuclei characteristic of songbirds: the caudal nucleus of the ventral hyperstriatum (HVc), the robust nucleus of the archistriatum (RA), and the magnocellular nucleus of the anterior neostriatum (MAN). The fourth region is the mesencephalic nucleus intercollicullaris (ICo), common to all birds, which contains the dorsomedial nucleus (DM) that appears to be specifically involved in the motor control of song. The pattern of neuropeptide localization was similar between the two species. However, the neuropeptides were heterogeneously dispersed among the four areas. VIP and MET were the most widely distributed, whereas CCK and SUB P were seen only in DM. MAN and HVc revealed remarkably similar patterns of staining for both MET and VIP. Fine varicosities immunolabeled for both these peptides appear to encircle nonreactive somata. In both these nuclei positively stained somata were observed for MET but not for VIP. In RA there was a dense accumulation of MET-positive multipolar cell bodies. VIP-containing neurons were seen in the surrounding archistriatum and caudal neostriatum but not in RA itself. Cell bodies and fibers for all four peptides were observed in DM; in no case were they limited to this subregion, but rather seemed to encompass the surrounding intercollicular area as well. The widespread distribution of VIP and MET strongly suggests a role for these peptides in the acquisition or production of passerine song.

Somatosensory systems and the milk-ejection reflex in the rat. I. Lesions of the mesencephalic lateral tegmentum disrupt the reflex and damage mesencephalic somatosensory connections

Bilateral electrolytic lesions and unilateral tracer injections were performed in lactating rats in order to study the participation of the mesencephalic lateral tegmentum in the milk-ejection reflex. The release of oxytocin was detected as a rise in intramammary pressure during each milk ejection. In animals with lesions, the lateral part of the deep grey layers of the superior colliculus, the intercollicular area and the rostromedial portion of the external nucleus of the inferior colliculus were destroyed. The mesencephalic lateral tegmentum of animals in which the milk-ejection reflex was blocked sustained a larger damage than in rats where the frequency of the milk-ejection response was only slowed down. Solutions of True Blue, horseradish peroxidase or horseradish peroxidase coupled to wheat germ agglutinin were injected in the mesencephalic lateral tegmentum of rats with and without lesions. Retrogradely labelled cells were found in several nuclei of the somatosensory pathways: the principal sensory and spinal parts of the trigeminal complex, the cuneate and gracile nuclei, the lateral cervical nucleus and the nucleus proprius of the spinal cord. Labelled cells were also found in the ventral nucleus of the lateral lemniscus. the ventral parabrachial nucleus, the gigantocellular reticular nucleus, the lateral nucleus of the substantia nigra, the prerubral nucleus of the thalamus, the hypothalamic ventromedial nucleus, the zona incerta and in the anterior and lateral hypothalamic areas. Labelled fibres and “terminal-like” labelling were found in the anterior pretectal area, in the thalamic parafascicular nucleus, in the posterior nucleus and the ventroposterior complex, in the zona incerta and in the fields of Forel, but none were observed in the supraoptic or paraventricular nuclei. Injections made in the area of the lateral cervical nucleus and in the cuneate and gracile nuclei labelled fibres and “terminal-like” fields in the external nucleus of the inferior colliculus. the intercollicular area, the deep grey layers of the superior colliculus and in the mesencephalic lateral tegmentum. After injections in the posterior nucleus and ventroposterior complex of the thalamus, retrogradely labelled cells were found in the lateral tegmentum, the intercollicular area and the external nucleus of the inferior colliculus. These results indicate that bilateral lesioning of the mesencephalic lateral tegmentum, which disrupts the milk-ejection response, could damage somatosensory projections originating from the dorsal horn of the spinal cord, the lateral cervical nucleus, the dorsal column nuclei and the sensory and spinal trigeminal nuclei. The importance of the intercollicular area and of the external nucleus of the inferior colliculus in the processing of the somatosensory informations is further suggested by the projection of those two areas onto the ventroposterior complex of the thalamus.

Projection from dorsal column nuclei to dorsal mesencephalon.

This study investigated the projection from the dorsal column nuclei (DCN) to the dorsal mesencephalon. Single-unit extracellular recordings were obtained from the DCN of alpha-chloralose anesthetized cats. Neurons were identified by standard antidromic stimulation criteria as projecting to the dorsal mesencephalon (M neurons), the diencephalon (D neurons), or to both regions (MD neurons). Fifty-two neurons could be antidromically activated from the dorsal mesencephalon. Of these, 31 could also be antidromically activated by stimulation in the diencephalon. An additional 34 neurons were studied that could be antidromically activated only from the diencephalon. Stimulation sites within the dorsal mesencephalon effective in antidromically activating M and MD neurons were in the caudal ventrolateral superior colliculus, the intercollicular area, and external nucleus of the inferior colliculus. Effective diencephalic stimulation sites were in the ventroposterolateral nucleus, the zona incerta, and the magnocellular division of the medial geniculate. The antidromic latencies to stimulation in the dorsal mesencephalon of M and MD neurons spanned a similar but wide range of values in contrast to the latencies to stimulation in the diencephalon of D neurons which were all short. Conduction velocities along the mesencephalic and diencephalic collaterals of MD neurons were similar. Many of the neurons projecting to the mesencephalon had receptive fields located proximally on the body. Most of the neurons had rapidly adapting responses to low-intensity mechanical stimulation of the skin. The major difference between the mesencephalic M and MD projection neurons and diencephalic projection D neurons was the larger percentage of neurons having proximal receptive fields in the former group. These findings are the first electrophysiological demonstration of a direct somatosensory input to the dorsal mesencephalon arising in the DCN. This input is probably responsible for providing some of the somatosensory input to the deeper layers of the superior colliculus, the external nucleus of the inferior colliculus, and the intercollicular area, regions known to have neurons responding to somatosensory stimuli.

Distribution of methionine-enkephalin immunoreactivity in the chick brain: an immunohistochemical study.

The distribution of Met-enkephalin-like immunoreactivity in the brains of 2-week-old domestic chicks was studied with immunohistofluorescence and the unlabeled antibody peroxidase-antiperoxidase technique, using antibodies to Met-enkephalin generated in rabbits. Immunoreactive cell bodies were found in the telencephalon, diencephalon, and mesencephalon in areas as yet uncharacterized as discrete nuclei in birds (E-1, E-2, E-3, E-4, E-5); further cells were located in the diencephalic nucleus spiriformis lateralis, the midbrain medial intercollicular nucleus (E-6), the nucleus mesencephalicus lateralis, pars dorsalis, the Edinger-Westphal nucleus and dorsal occulomotor nucleus; and in the nucleus of cranial nerve X and an uncharacterized area in the dorsolateral medulla (E-7). Immunoreactive fibers and/or terminals were located around the immunoreactive cell bodies and, in addition in the lateral septal area of the telencephalon; in the preoptic and hypothalamic areas of the diencephalon; in the anterior intercollicular area, periaqueductal central gray, area C, and the midventral tegmentum of the mesencephalon; in the nucleus solitarius, nucleus IX-X, nucleus intercalatus, nucleus intermedius, and ventrolateral areas of the rhombencephalon. The pattern of distribution of met-enkephalin in the chick is compared with that in the rat. A possible functional role for Met-enkephalin in neural mechanisms mediating some behaviors of the chick is suggested.

The representation of the auditory and somatosensory systems in the external nucleus of the cat inferior colliculus.

Parallel single unit and retrograde tracing experiments were carried out in the anesthetized cat to elucidate the representation of the auditory and somatosensory systems in the external nucleus of the inferior colliculus (ICX). Units responding to tonal stimuli were more commonly encountered in ICX and the adjacent intercollicular area (ICA) than were units with identified tactile receptive fields. Concomitantly, a larger number of retrogradely labeled cells were identified in midbrain auditory structures, following injections of horseradish peroxidase (HRP) into CRX, than were found in the combined dorsal column nuclei. Microelectrode recording revealed that the entire accessible body surface was represented in ICX, and receptive fields of individual units were usually large and mostly located on the contralateral side. HRP-labeled cells were scattered throughout the contralateral cuneate, gracile, and spinal trigeminal nuclei. tations of tone pips. Responses to complex sound were commonly observed. Binaural stimuli influenced the firing of the majority of auditory units. Labeled auditory neurons following ICX injections were found mainly in the inferior colliculus of both sides. Spread of tracer into the central and pericentral nuclei was associated with labeling of many neurons in hind brain auditory structures. Only vague suggestions of somatotopy or tonotopy were observed in the electrophysiological experiments; similarly, no topographical relationship between HRP injection site and locus of retrograde label in a given projecting nucleus could be discerned. Speculations were made, in the light of the dual convergent sensory representation in ICX, about the role of this structure in acoustico-motor mechanisms.

The intercollicular area of the inferior colliculus.

To study the somatosensory input to the inferior colliculus, lesions were made in the dorsal column nuclei of the hedgehog, tree shrew, slow loris, marmoset and African green monkey, and spinal cord of the hedgehog, tree shrew and slow loris. The degenerating fibers stained with silver impregnation methods. The dorsal column system projects primarily to an area lateral to the central nucleus of the inferior colliculus, whereas the spinotectal projection is primarily to the medial region in the hedgehog and medial and dorsal regions in the tree shrew and slow loris. Both fiber systems are quantitatively quite constant in the various species. It is apparent from published data on a variety of mammals that the central nucleus is primarily part of the auditory system in which the intercollicular area is involved only indirectly via projections from the central nucleus and auditory cortex. In nonmammalian vertebrates, the data available suggest that there is a comparable area in the mesencephalon that is involved with somatosensory as well as auditory sensation. Since low frequency stimulation, generally characterized as vibration, stimulates both modalities, the intercollicular area may be the input side of a mechanism for alterting the animal to vibratory stimuli.

Changes in visual responsiveness following intercollicular lesions and their effects on avoidance and attack.

In the normal chick, conspicuous visual stimuli induce targetting and pecking together, with vocalization. All three are abolished by lesion of the intercollicular area (ICo) or of connections passing through its medial margin. After such lesions, chicks also cease to treat significant visual stimuli as if they were startling and exciting, and may delay response as a result. However, they are still able to recognise, orient accurately to, and respond appropriately to, a variety of complex visual stimuli (e.g. food grains, copulation object). In addition, they are little affected by strange surroundings. Lesion evidence suggests the mammalian subcollicular area to have similar functions to the ICo and to be homologous with it. A route (present in bird), which is well-known in mammals for its association with threat, defense and escape evoked by strange and frightening objects (amygdala-diencephalic periventricular system-central mesencephalic grey, A-DPS-CMG) is stimuli via the 2 ICo (subcollicular area). Two different mechanisms may be involved caudal to the ICo. One consists of tectal afferents which might modulate the evocation of targetting, pecking and other responses via the tectum. The other is the predorsal system of tectal efferents which may mediate such responses. Classical syndromes of tameness and unresponsiveness produced by various interruptions of the A-DPS-CMG route may depend on interruption of connections to these midbrain mechanisms. Attack is depressed by ICo lesions as one aspect of reduced responsiveness to conspicuous and startling visual stimuli. Avoidance, which is apparently mediated by a separate system, much as in Anura, is facilitated.

Midbrain structures controlling vocalization in the domestic chick.

Bilateral lesions confined to the anterior intercollicular area (ICo) produce muting in domestic chicks. Calling is lost both in open field test, and to novel stimuli which evoke pecking. Lesions of the medial edge of the ICo also mute, perhaps by cutting connections with the central mesencephatic grey. Partial destruction of the ICo allows full intensity calling but with greatly increased latency. If an area ventral to the ICo is also destroyed, one type of calling reappears: it is still not readily evoked by particular stimuli which are effective in normal chicks but it often occurs during locomotion. Crowing survives ICo lesions and presumably depends on a different route to lower centres. Totally deaf birds show quite normal calling, so that hearing deficits are probably not involved in the muting. Finally, mammalian homologues of the ICo and its connections are identified.