Fernando Reinoso-Suárez

Insular cortex and neighboring fields in the cat: A redefinition based on cortical microarchitecture and connections with the thalamus

The insular areas of the cerebral cortex in carnivores remain vaguely defined and fragmentarily characterized. We have examined the cortical microarchitecture and thalamic connections of the insular region in cats, as a part of a broader study aimed to clarify their subdivisions, functional affiliations, and eventual similarities with other mammals. We report that cortical areas, which resemble the insular fields of other mammals, are located in the cats orbital gyrus and anterior rhinal sulcus. Our data suggest four such areas: (a) a “ventral agranular insular area” in the lower bank of the anterior rhinal sulcus, architectonically transitional between iso‐ and allocortex and sparsely connected to the thalamus, mainly with midline nuclei; (b) a “dorsal agranular insular area” in the upper bank of the anterior rhinal sulcus, linked to the mediodorsal, ventromedial, parafascicular and midline nuclei; (c) a “dysgranular insular area” in the anteroventral half of the orbital gyrus, characterized by its connections with gustatory and viscerosensory portions of the ventroposterior complex and with the ventrolateral nucleus; and (d) a “granular insular area”, dorsocaudal in the orbital gyrus, which is chiefly bound to spinothalamic‐recipient thalamic nuclei such as the posterior medial and the ventroposterior inferior. Three further fields are situated caudally to the insular areas. The anterior sylvian gyrus and dorsal lip of the pseudosylvian sulcus, which we designate “anterior sylvian area”, is connected to the ventromedial, suprageniculate, and lateralis medialis nuclei. The fundus and ventral bank of the pseudosylvian sulcus, or “parainsular area”, is associated with caudal portions of the medial geniculate complex. The rostral part of the ventral bank of the anterior ectosylvian sulcus, referred to as “ventral anterior ectosylvian area”, is heavily interconnected with the lateral posterior‐pulvinar complex and the ventromedial nucleus. Present results reveal that these areas interact with a wide array of sensory, motor, and limbic thalamic nuclei. In addition, these data provide a consistent basis for comparisons with cortical fields in other mammals. J. Comp. Neurol. 384:456–482, 1997.

Topographical organization of the thalamic projections to the cortex of the anterior ectosylvian sulcus in the cat

SummaryThe thalamic afferents of the anterior ectosylvian sulcal region were studied in the cat using retrograde axonal transport of horseradish peroxidase. Following peroxidase injections in the cortex of both banks and fundus of the anterior ectosylvian sulcus, retrograde labeling was always very abundant in the ventromedial thalamic nucleus, whichever part of the sulcus was injected. Consistent numbers of labeled neurons were also identified in the lateral medial subdivision of the lateral posterior-pulvinar complex, suprageniculate nucleus, posterior thalamic nuclear group and magnocellular division of the medial geniculate nucleus. A smaller number of labeled neurons was found in the ventral part of the lateral posterior nucleus, and ventralis anterior, ventralis lateralis, medialis dorsalis and intralaminar nuclei. The quantity and topographical distribution of labeled neurons in these thalamic nuclei depended on the location of the injection in the banks and fundus of the sulcus.

Direct projections from hypothalamus to hippocampus in the rat demonstrated by retrograde transport of horseradish peroxidase

The hypothalamus and hippocampus have been correlated by both functional and morphological approachesS, 11. Direct hypothalamic projections to the hippocampus have been reported from studies with silver impregnation methods 2, but it now seems possible that some of these connecting fibers may be by-passing fibers from caudal regionsT, a. Recently, in cases of hippocampal injection of horseradish peroxidase (HRP), labeled neurons were found in the supramammillary region 9, an observation suggesting the existence of direct hypothalamo-hippocampal projections. In the present study the distribution of hypothalamic neurons labeled by HRP injections in the hippocampus was investigated in some more detail, and an attempt was made to establish topographical correlations between the two brain regions. Stereotaxic injections of 0.1-0.2 /zl of 50~ HRP solution (Sigma type VI) were made into the right or left hippocampus of 24 white rats (150-250 g) trying to avoid diffusion of HRP to neighboring regions. Sixteen rats were injected at various rostrocaudal points in the dorsal hippocampus. In 3 animals the injection was localized to the ventral hippocampus (the needle was introduced through the cortex in an oblique direction to avoid the dorsal hippocampus). In 5 control rats HRP was injected at different sites in the cortex overlying the hippocampus. After a 24-h survival time, the animals were perfused, and the brains sectioned on a freezing microtome in the frontal, horizontal or sagittal plane. The sections were processed according to the method of Llamas and Martinez-Moreno a. Labeled neurons were not found in any hypothalamic nuclei when HRP had been injected in any of the following places: the cortex above and lateral to the hippocampus, the anterior portion of the dorsal hippocampus, the subiculum of the dorsal posterior hippocampus (Fig. 1) and the anterior portion of the ventral hippocampus (not represented in the figure). Since HRP-filled neurons were observed in all these cases in other brain regions, it seems unlikely that this negative result is attributable to technical failure.

The topographic organization of hypothalamic and brain stem projections to the hippocampus.

Direct projections primarily ipsilateral to hippocampus from medial septal, diagonal band, supramammillary, submammillothalamic, locus coeruleus, and dorsal and medianus raphe nuclei were demonstrated. The locus coeruleus projects primarily through the cingulum and fornix superior to the dorsal posterior hippocampus, with its terminal fields in the stratum lacunosum moleculare of the subiculum and areas CA 1-CA 2 of the dorsal posterior hippocampus. LC projections to the granular layer of the dentate hilus were not found. Raphe nuclei project through the cingulum, fornix superior, and primarily the fimbria, to the dorsal and ventral posterior hippocampus, with their terminal fields in the stratum lacunosum moleculare of the dorsal posterior subicular region, stratum radiatum of CA 1-CA 3 in the dorsal hippocampus, and the stratum polymorph of the dentate gyrus, primarily in its superficial part. Raphe projections to the anterior hippocampal rudiment were found. However, no projection was found to the subiculum of the ventral posterior hippocampus, nor to stratum oriens. Hypothalamic nuclei project through the fornix superior and the fimbria, mainly to the dorsal posterior hippocampus with abundant terminal fibers in the depth of the dentate hilus. Smaller cells in these hypothalamic nuclei appear projecting to the ventral hippocampus. The number of neurons in the entorhinal area, the diagonal band, and the hypothalamic nuclei projecting to the hippocampus suggests these groups as the main sources of the extrinsic hippocampal afferents. In addition, they may also serve as relay stations for inputs from more caudal nuclei, and the topographic organization of their terminal fields as described herein may have important functional implications.

Sleep patterns after carbachol delivery in the ventral oral pontine tegmentum of the cat

This study examines dose-related effects on sleep produced by low-volume and low-dose carbachol microinjections in the ventral part of the cat nucleus reticularis pontis oralis. Carbachol microinjections (0.04, 0.08, 0.8 or 4 microg; volume 20 nl) in this location triggered paradoxical sleep with a very short dose-unrelated latency. The four carbachol doses effectively generated all the polygraphic and behavioral signs of paradoxical sleep when microinjected at any level within the ventral part of the nucleus reticularis pontis oralis (AP 0.5 to -3.5, L 0.5-3.5, V 3.5-5.0, on the Reinoso-Suárez atlas [Topographischer Hirnatlas der Katze (1961); Merck, Darmstadt]). The dose-related increase of total paradoxical sleep time was due to the increase in both the duration and number of paradoxical sleep episodes. This paradoxical sleep increase was associated with a dose-related decrease in the amount of time spent in both slow wave sleep and drowsiness, but not with any decrease in total wakefulness. The lengthening of the latency to slow wave sleep onset was dose related. These results show that the ventral oral pontine tegmentum is a very sensitive site for the induction and maintenance of paradoxical sleep.

Topographical organization of the cortical afferent connections to the cortex of the anterior ectosylvian sulcus in the cat

SummaryThe cortical afferents to the cortex of the anterior ectosylvian sulcus (SEsA) were studied in the cat, using the retrograde axonal transport of horseradish peroxidase technique. Following injections of the enzyme in the cortex of both banks, fundus and both ends (postero-dorsal and anteroventral) of the anterior ectosylvian sulcus, retrograde labeling was found in: the primary, secondary, and tertiary somatosensory areas (SI, SII and SIII); the motor and premotor cortices; the primary, secondary, anterior and suprasylvian fringe auditory areas; the lateral suprasylvian (LS) area, area 20 and posterior suprasylvian visual area; the insular cortex and cortex of posterior half of the sulcus sylvius; in area 36 of the perirhinal cortex; and in the medial bank of the presylvian sulcus in the prefrontal cortex. Moreover, these connections are topographically organized. Considering the topographical distribution of the cortical afferents, three sectors may be distinguished in the cortex of the SEsA. 1) The cortex of the rostral two-thirds of the dorsal bank. This sector receives cortical projections from areas SI, SII and SIII, and from the motor cortex. It also receives projections from the anterolateral subdivision of LS, and area 36. 2) The cortex of the posterior third of the dorsal bank and of the posterodorsal end. It receives cortical afferents principally from the primary, secondary and anterior auditory areas, from SI, SII and fourth somatosensory area, from the anterolateral subdivision of LS, vestibular cortex and area 36. 3) The cortex of the ventral bank and fundus. This sulcal sector receives abundant connections from visual areas (LS, 20, posterior suprasylvian, 21 and 19), principally from the lateral posterior and dorsal subdivisions of LS. It also receives abundant connections from the granular insular cortex, caudal part of the cortex of the sylvian sulcus and suprasylvian fringe. Less abundant cortical afferents were found to arise in area 36, second auditory area and prefrontal cortex. The abundant sensory input of different modalities which appears to converge in the cortex of the anterior ectosylvian sulcus, and the consistent projection from this cortex to the deep layers of the superior colliculus, make this cortical region well suited to play a role in the control of the orientation movements of the eyes and head toward different sensory stimuli.

Afferent connections of area 20 in the cat studied by means of the retrograde axonal transport of horseradish peroxidase

Following injections of horseradish peroxidase in area 20 of the cat neuronal labeling was observed in visual areas 19, 21 and lateral suprasylvian as well as in other sensory, association and limbic related neo- and allocortical regions, both ipsi- and contralaterally. Labeled neurons in the thalamus were identified in the LP-Pu complex, in the LIc, in the midline and intralaminar nuclei, and in the nuclei ventralis anterior, dorsalis medialis, lateralis anterior, lateralis medialis, ventralis posteroinferior, and in the medial subdivision of the posterior group. Projections from other subcortical prosencephalic and brain stem regions are also described.

Location and anatomical connections of a paradoxical sleep induction site in the cat ventral pontine tegmentum.

The brainstem mechanisms for the generation of paradoxical sleep are under considerable debate. Previous experiments in cats have demonstrated that injections of the cholinergic agonist carbachol into the oral pontine tegmentum elicit paradoxical sleep behaviour and its polygraphic correlates. The different results on the pontine structures that mediate this effect do not agree. We report here that limited microinjections of a carbachol solution into the ventral part of the oral pontine reticular nucleus in the cat induce, with a short latency, a dramatic, long‐lasting increase in paradoxical sleep. Moreover, neuronal tracing experiments show that this pontine site is connected with brain structures responsible for the different bioelectric events of paradoxical sleep. These two facts suggest that the ventral part of the oral pontine reticular nucleus is a nodal link in the neuronal network underlying paradoxical sleep mechanisms.

Allocortical afferent connections of the prefrontal cortex of the cat

Afferent connections of the prefrontal cortex of the cat arising in allocortical regions have been investigated using the horseradish peroxidase retrograde transport technique. Our results demonstrate the existence of projections from the olfactory peduncle, anterior and posterior prepiriform cortices, cortico-amygdaloid transition area, entorhinal cortex, ventral, caudal and dorsal subiculum and postsubiculum to the prefrontal cortex.

Stability of the neuronal population of the dorsal lateral geniculate nucleus (LGNd) of aged rats

The variations, with aging, of both neuronal and glial populations of the rat LGNd have been studied quantitatively. Our results show a stability of the total number of neurons of the rat LGNd with aging; this, plus the constant increase of the rat LGNd volume throughout rat life, causes the neuronal density to decrease slowly. Our data prove the necessity of determining the total number of neurons, not just neuronal density, in order to find out the actual evolution of the neuronal population with aging. Both glial cell number and density show an increase throughout rat life.