Afferents from the periaqueductal gray, medial hypothalamus and medial thalamus to the midbrain reticular core

Brain Research Builetin, Vol. 7, pp. 411-418, 1981. Printed in the U.S.A.

Afferents from the Periaqueductal Gray, Medial Hypothalamus and Medial Thalamus to the Midbrain Reticular Core’ A. PARENT Laboratoire *Laboratoire

AND M. STERIADE”

de Neurobiologie et Dkpartement d’Anatomie, and de Neurophysiologie et Ddpurtement de Physiologie

Faculth de Mhdecine,

Universite’ Laval, Q&bee, Received

PARENT, A, AND M. STERIADE.

GlK 7P4, Canada

15 May 1981

A~gre~tsfr~~ the peri~q~educt~igray,

medial hyp~t~~la~us

and medial

thala~u~

to

BRAIN RES. BULL.

7f4) 41 l-418, 1981.-On the basis of elect~physiolo~cal findings, a descending input from the midline diencephalic areas to the mesencephalic reticular formation has been envisaged to underlie a tonic, reinforcing control of the waking brain. In order to substantiate morphologically this hypothesis and to assess the exact sources of this descending input, unilateral injections (0.04 to 0.06 ~1) of horseradish peroxidase (HRP: 5f% solution in 2% DMSO) were made within the mesencephali~ reticular fo~ation (MRF) in 11 cats. The animals were allowed to survive from 24 to 48 hrs and the brain sections were treated according to the diamino-benzidine (DAB), the tetramethyl-benzidine (TM@, or the bezidine-dihydrochloride (BDHC) procedure. In most animals the injection site was rather small and confined to the nucleus cuneiformis and adjacent central tegmental field. Numerous positive cells, with HRP granules in the soma and proximal processes, were consistently found ipsilaterally at distances ranging from 0.2 to 1.5 mm from the wall of the aqueduct and the third ventricle. Thus, HRP-labelled neurons were seen (1) in the midbrain pe~aqueductal gray, mostly in its media-dorsal aspect, (2) in the caudal diencephalic ~~vent~cul~ gray, medial to the retroflex bundle, (3) in the periventricular and medial territories of the preoptico-hypothalamic complex, (4) in the centrum medianum-parafascicularis thalamic nuclei, and (5) less consistently, in the paracentralis thalamic nucleus. A few positive cells were also scattered within the central gray, contralateral to the injection site. At hypothalamic levels, HRP-labelled neurons predominated particularly within and around the ventromedial, arcuate, suprachiasmati~ and paraventricular nuclei, and in the medial preoptic re8ion. These results demonstrate that, in addition to the massive subthalamic input to the midbrain reticular formation described recently, a well-developed neuronal system extending from the mesencephalon to the anterior preoptico-hypothalamic region also provides a significant number of afferent fibers to the upper brainstem reticular core. the midbruin

r~ticfflar

core.

Midbrain reticular afferents Midbrain reticular core Horseradish peroxidase study Medial thalamus

THE reciprocal medial midbrain

relations between the hy~th~amus and the structures are thought to be involved in var-

ious, complex brain functions such as the sleep-waking cycle [22], defense and aggressive behaviour 17,301, reproduction [5], and the control of co~icosteroid secretion 1341. The efferent projections from different areas of the medial hypothalamus to the midbrain, traced by means of degeneration 1671 and autoradiographic [13,28] techniques, were found to arborize primarily within the ~~aqueductal gray. In keeping with such a view, lesions restricted to the central gray (CG) are effective in abolishing the rage reaction induced by hypothalamic stimulation [12,301. In other experiments, however, the extent of the midbrain lesions required to abolish the hypothalami~ally elicited rage outbursts largely exceeded the CC territory and included the adjacent mesencephalic reticular formation (MRF) and the ventral tegmental area [4]. Presented

Pe~aqueduct~

o 1981 ANKHO

Inte~ation~

Medial hy~thal~us

Thus, there is a need for further investigation because the same hypothalamic-midbrain circuitry is viewed as being responsible for waking as well as for fits of rage resulting in a mild tonic, or an extreme phasic activation 1221. Morphoiogical analyses in this domain should contribute to the elucidation of differential projections from various hypothalamic structures to the CG and MRF. Grofova et al. [lo] have recently investigated the diencephalic &erents to the CG by means of the horseradish peroxidase (HRP) retrograde labelling method. However, these authors did not specifically analyse the afferents to the MRF; the only case that involved the MRF in their study consisted of large HRP injections which also included the CG and the superior colliculus. Therefore, in view of the physiological importance of the diencephalo-mesencep~alic relationship, we thought it of interest to investigate in detail

in part at the 9th Annual Meeting of the Society for Neuroscience,

Copyright

gray

Atlanta, GA, 1979.

Inc .-0361-9~30/81/1~41~-08$0~.30/0

412

PARENT AND STERlADE LIST OF ABBREVIATIONS

AQ: CeM: CG: CM-k’f. D: FF: FTC: Fx: HL: Hm: IC: IP: LGd: LP: MD: MG: MTB: OCh: OT: PC: Pc: PIN: POA: PP: PUL: PV: RN: RTB: SC: SN: so: VB: VM: VPM: v3: ZI: 3: 3N: 4:

Aqueduct Nucleus centralis medialis thalami Central gray Nuclei centrum medianum-parafascicularis NucIeus of Darkschewitsch Fore1 field Central tegmental field Fornix Lateral hypothalamus Medial habenular nucleus Internal capsule Interpeduncular nucleus Lateral geniculate nucleus, dorsal part Nucleus lateralis posterior thalami Nucleus medialis dorsalis thaiami Medial geniculate nucleus Mammillo-thalamic bundle Optic chiasma Optic tract Posterior commissure Nucleus paracentralis thalami Pineal gland Preoptic area Pes ~duncuii Pulvinar Periventricular hypothalamic nucleus

thalami

Red nucleus Retroflex bundle Suprachiasmatic nucleus Substantia nigra Supraoptic nucleus Ventrobasal thalamic complex Ventrom~ial hy~~~~ic nucleus Ventral posteromedial thaiamic nucleus Third ventricle Zona incerta Oculomotor nucleus Oculomotor nerve Trochlear nucleus

the various sources of afferents to the rostra1 portion of the reticular core by means of the HRP method.

METHOD

A total of 13 adult cats of both sexes were used in this study. Under ketamine anesthesia (40 m&g, IM), HRP (Sigma, type VI) was injected unilaterally into the midbrain reticular core in 11 of them. The other two animals received HRP injection into the pons: one in the paramedian pontine reticular formation, the other in the dorsolateral pontine tegmentum. In all cases the HRP was delivered through a cannula consisting of a drawn glass capillary tube (tip diameter of about 80 pm) attached to a stereotaxically-driven Hamilton syringe. The enzyme (0.04 to 0.06 ~1 of 50% solution in 2% DMSO) was injected over a period of 10 min and the cannula was left in place for an additional 5 min. Follow-

ing a survival period ranging from 24 to 48 hrs, the animals were perfused under deep pentobarbital anesthesia with 400 CLIOf saline followed by 400-1000 ~1 of a freshly prepared fixative (2% Parafo~aIdehyde-1% glutaraldehyde in 0.1 M phosphate buffer, pH=7.4). The brains were removed, placed in the same fixative for 4 hrs, stored overnight in 0. I M phosphate buffer (cooled to 4”~) containing ~--IO% sucrose, and sectioned on a freezing microtome at 40 pm in the frontal plane. In three cases the serially-collected sections were processed according to the diamino-benzidine tetrahydrochloride (DAB) method ]14]. In the other cases, the tetramethyl benzidine (TMB) [20] or the benzidine dihydrochloride (BDHC) [ 191 procedures were used, the latter with counterstaining by means of neutral red. The extent of the injection sites and the location of HRP-labelled neurons were mapped on projection drawings of histological sections selected at appropriate levels. The photomi~rography was performed under both light- and darkfield illumination. RESULTS

In eight of the eleven cats injected in the midbrain, the HRP was confined to the territory of the MRF which comprises the nucleus cuneiformis [33] and its ventrorostral extension, the central tegmental field 133. In those cases the injection sites were rather elongated, with diameters of about 2.3 to 2.8 mmdorsoventrally, and of 1.1 to 1.6 mm mediolaterally (Figs. 1, 3). One animal had a double HRP injection resulting in a larger deposit (3.5 mm in diameter) which invaded the ventrolateral part of the central gray at posterior levels. The remaining two animals were discarded since they had large injection loci encroaching upon the superior colliculus and the CC, or upon the medial geniculate body. The injection of HRP into the MRF labels a multitude of neurons belonging to the zona incerta (ZI), ipsilaterally. Thus, this structure stands out as one of the major diencephalic sources of afferents to the rostra1 reticular core. The neuroanatomical and electrophysiological characteristics of the ZI-MRF connection have been fully reported elsewhere (1321, see also Fig. 4). Besides the Zl, numerous HRP-positive cells also occur ipsilaterally in the CG after MRF injection. They abound in the dorsomedial quadrant of the periaqueductal gray, and within the diencephalic pe~ventri~ular gray where they are mostly confined to periventricular and medial territories of the preopticohypothalamic complex, rostrally (Fig. 4A, D). Labelled fibers are also visualized between the injection site in the MRF and the CG (Fig. IB), and within the ventralmost aspect of the posterior commissure (Fig. 1C). Some of the HRP containing fibers linking the MRF and the CG could be seen to merge within heavily-labelled CC neurons indicating that these axons are part of a CG-MRF projection system. However, other positive fibers appeared to arborize into the CG, supporting the idea of a reciprocal connection between the MRF and CG (see [ 161). In regard to the HRP-filled fibers in the posterior commissure they could be part of the so-called parabigemino-collicular system, although this system appears mostly unilateral [2]; alternately, they could betong to a contralateral projection system from CG to MRF since some HRP-labelled neurons have been seen in the CG contralateral to the injection site (Fig. 4D). It is also worth noting that no HRP-labelled fibers were visualized in the posterior commissure in cases where HRP was injected into the pons. it is therefore unlikely that the fiber-labelling observed following injection into the MRF is the result of HRP

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GRAY AFFERENTS

TO RETICULAR

CORE

FIG. 1. Illustration of a typical case of HRP injection within the MRF: animal no. 387; 0.04 ~1 HRP; 36 hr survival period; BDHC method). The figure shows: A-the injection site at the level of its maximum extent, B-some HRP-labelled fibers coursing between the MRF and the periaqueductal gray, C-HRP-positive fibers within the posterior commisure, just above the periaqueductal gray (darkfield illumination), and D-HRP-labelled neurons in the dorsomedial quadrant of the periaqueductal gray. Calibration in mm (A) and in pm (ED).

leaking into damaged axons that are coursing downward to lower segments of brain stem. The HRP-positive neuronal somata disclosed in CG after MRF injection varied in shape from small bipolar (Fig. 2A) to large and multipolar (Fig. 2B). However, most neurons, which were lying in the dorsomedial quadrant of the CG, displayed a spindle shape (Fig. 1D). They appear to correspond to the fusiform type Ia and Ib neurons disclosed in the dorsal part of CG utilizing the Golgi method [ 161. The labelled cells in the diencephalic periventricular gray were particularly abundant along the ependymal wall beneath the habenula, caudally (Fig. 2C; and Fig. 4D), whereas more rostrally they were scattered within and around various hypothalamic structures such as the ventromedial, arcuate, suprachiasmatic and paraventricular nuclei (Fig. 4), and the medial preoptic region. The retrograde labelling of neurons in the ventromedial hypothalamic nucleus was particularly obvious in cases where the injection site slightly encroached upon the CG (see Fig. 4D). Some hypothalamic labelled cells

were lying very close to the ependymal wall of the third ventricle (Fig. 2D). Other neurons were found to be retrogradely labelled within the intralaminar nuclei, particularly the centre median-parafascicular complex and the nucleus paracentralis (Figs. 3 and 4). However, the HRP labelling was inconsistent in those areas, especially in nucleus paracentralis. In some MRF-injected animals no positive cells were disclosed in intralaminar nuclei and in most cases where labelled neurons occurred, the intensity of the labelling was often weak. This may indicate that the projections from intralaminar nuclei to the MRF are part of a highly collateralized system. For instance, a single intralaminar neuron could send axonal projections to both the neostriatum and midbrain tegmentum. Finally, it is worth mentioning that labelled cells were visualized in the contralateral tegmentum, as well as in the ipsilateral substantia nigra, pars reticulata, and superior colliculus (Fig. 4). The presence of HRP-positive cells in the

PARENT

AND STERIADE

FIG. 2. Illustration of other labelling features taken from the same animal as the one shown in Fig. 1. It depicts: A-two small HRP-positive cells intermingled among labelled processes along the midline, within the periaqueductal gray, B-a large, multipolar, HRP-labelled neuron in the dorsal aspect of the periaqueductal gray, C-a few HRP-positive cells disclosed in the caudal periventricular gray of the diencephalon, near the medial border of the fasciculus retroflexus, and D-one HRP-filled cell lying along the ependymal wall of the hypothalamus, medial to the ventromedial hypothalamic nucleus. Calibration in Wm.

substantia nigra and superior colliculus may be attributed, as well as the existence of MRF afferents from these two structures, to HRP uptake by nigro-collicular fibers (see [lo]) and colliculo-parabigeminal pathways [2,9] that may have been injured by the injection procedure. DISCUSSION

The complex,

reciprocal

relations

between

the medial-

periventricular hypothalamic nuclei and midbrain periaqueductal gray are well established, especially following extensive investigations in recent years with anterograde and retrograde tracing methods. Within the hypothalamus, the ventromedial nucleus is a site of converging inputs from the medial preoptic area 1281, suprachiasmatic nucleus [17] and dorsomedial hypothalamic area [17], while its efferent projections can be traced both forward through the periven-

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CORE

415

FIG. 3. Illustration of a case of HRP injection within the MRF (C-416; Ct.03pl HRP; 24 hr surviva1 period; BDHC method) which resulted in retrograde cell labelling in CM-Pf thalamic nuclei. It shows: A-the injection site, B-HRP-labelled neurons in the causal portion of the centrum med~anum nucleus (dark~eld iuum~nation~, C and HARP-~sitive cells visualized in the par~asc~cular nucleus, along the medial border of the fascicuius retroflexus. Calibration in mm (A) and in ym (B-D). Calibration in 3 is also valid for 4.

tricular territory to the preoptic region, and caudalward to the posterior hypothalamus [28]. One of the major target structures of medial hy~thalami~ structures such as the ventromedial, paraventricular, and suprach~smatic nuclei is the CG [10,133. In fact, the CG appears to be the main recipient structure of the entire hypothalamic outflow, which includes fiber systems from the lateral hypothalamic area and adjacent zona incerta as well [lo]. In turn, the CG itself gives rise to: (1) descending projections reaching the medial part of the lower brain stem [S] as well as the spinal cord [351, and (2) ascending projections representing reciprocal connections with the medial-pe~vent~cular hypothalamic system 1111. Also worth noting is the presence within the CG of a prominent system of monoamine-containing neurons which follows closely the trajectory of the so-called dorsal longitudinal fascicuius of Shiitz [23]. Both serotonin [23] and catecholamine [15] containing neurons have been shown to be part of this “periventricular system” which contributes significantly to the innervation of the hypothalamus [23]. The findings of the present study suggest, among other things, that the MRF is located on a parallel branch of the hypothalamic perivent~cular-midbrain CG circuitry.

First, certain hypothalamic neurons, particularly those in the ventromedial nucleus, were labelled especially when HRP injections invaded the lateral parts of the CG (compare A to D in Fig. 4). This is in keeping with the significant retrograde cell Iabelling observed in this nucleus after HRP injections restricted to the CG (see case 11985 in Fig. 2 of Grofova et al. [IO]). On the other hand, neuronal labelling in the remaining dorsal and ventral parts of the periventricular and medial hypothalamus occurred after injections restricted to the MRF territory (Fig. 4A). The medial hypothalamic projection to the MRF is conjunctional with that arising from the dorsolateral hypothalamic area and the adjacent medial part of the zona incerta [321. The existence of medial and lateral hypothalamic projections to the rostral reticular core, as demonstrated by HRP method, is further supported by the results of electrophysiological studies in which antidromic invasion of medial hy~thalamic neurons 1241 and zona incerta [32] neurons was obtained following midbrain reticular stimulation. The main difference between the medial and the lateral hypothalamic-subthalamic projections to the midbrain reticular core consists of a preference dist~bution from the medial hy~thaIamus to the CG and much slower conduction

416

PARENT AND STERIADE

FIG. 4. Schematic illustration of the distribution of the retrogradely labelled neurons (dots) in four different cases of midbrain HRP injection (A to D). The solid black at the level of the injection sites indicates the location of the tip of the cannula, while the heavy and lighter stippled areas represent the main diffusion zone of HRP and the halo, respectively. A-a typical case of HRP injection confined to the MRF. B and C-two examples where retrograde cell labelling was observed in CM-Pf thalamic nuclei after MRF injection. D-an example of MRF injection encroaching upon the central gray with the resulting massive cell labelling in medial hypothalamus.

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GRAY AFFERENTS

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CORE

velocities of medial hypothalamic fibers [24] compared to lateral hypothalamic-zona incerta axons [32]. In regard to the nature of the effects induced by these descending projections from medial diencephalic structures, the few reports on distant influences arising in the medial part of the anterior hypothalamus and acting upon single MRF units consistently showed an initial excitatory response [ 18, 27, 3 11. This fits in with prevailing initial excitation evoked by stimulation of preoptico-hypothalamic areas in other parts of the medial hypothalamic system [26]. Second, labelled neurons were consistently found in the periaqueductal gray and in the immediately rostra1 periventricular diencephalic gray following HRP injections into the MRF. The CG-midbrain reticular projection was already described in Golgi studies by Ramon y Cajal [25] who mentioned that the axons of cell bodies in both medial and lateral parts of the mesencephalic CG terminate within the adjacent reticular formation (see Fig. 164 in [25]). Thus, the entire system of reciprocal connections between the medial hypothalamic structures and the CG has access to the MRF and,

therefore, its functions involving defense-aggression instinctive behavior and complex endocrine processes (see introductory section) may affect different types of MRF neurons provided with ascending and descending axons. Finally, a third source of input to the MRF from medial diencephalic structures was found in the CM-Pf thalamic nuclei and, less consistently, in the intralaminar centralis lateralis nucleus. The absence of retrogradely labelled neurons in the CM-Pf thalamic complex after large, bilateral HRP injections in the CG and the dorsal part of the MRF reported by Grofova et al. [see Fig. 1 in [lo]) is most likely attributable to the less sensitive DAB method used by these authors. Indeed, our HRP findings obtained with either the TMB or the BDHC method suggest the existence of at least some axonal projections from the medial thalamic nuclei to the rostra1 portion of the brainstem tegmentum [29]. ACKNOWLEDGEMENTS

This research was supported by grants MT-5781 (to A. P.) and MT-3689 (to M. S.) of the Medical Research Council of Canada.

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