ACTA NEUROBIOL. EXP. 1989. 49: 23-37
DIFFERENTIAL PROJECTION FROM THE MOTOR AND LIMBIC CORTICAL REGIONS TO THE MEDIODORSAL THALAMIC NUCLEUS IN THE DOG
Iwona STEPNIEWSKA and Anna KOSMAL Department of Neurophysiology, Nencki Institute of Experimental Biology 3 Pasteur Str., 02-093 Warsaw, Poland
Key words: mediodorsal thalamic nucleus, motor and limbic cortices, horseradish peroxidase Abstract. The cortical afferents to the mediodorsal thalamic nucleus in the dog were studied by using horseradish peroxidase. Small injec- tions allowed to establish two specific projection zones connected sepa- rately with the lateral and medial segments of the nucleus. The lateral segment received the major projection from the dorsal half of the hemi- sphere. It included premotor and part of the motor cortices in the ante- rior sigmoid gyrus and precruciate areas as well as the presylvian cor- tex. The medial segment of the nucleus was innervated by the limbic areas of the ventral half of the hemisphere. These areas included the medloventrally located genual, subcallosal and plriform cortices, as well as the cortex of the ventral bank of the anterior rhinal sulcus and the caudal part of the orbital gyrus. The cortical fields situated between these two main cortical zones, both on the lateral and medial surfaces (rhinal and sylvian sulci and anterior cingular gyrus, respectively) sent projec- tions to both medial and lateral segments of the nucleus. These results indicate that in the mediodorsal thalamic nucleus may take place the integration of information from two functionally defined systems, the motor and limbic ones.
INTRODUCTIOPJ The numerous studies of the cortical afferents of the mediodorsal thalamic nucleus (MD) showed, that although the prefrontal cortex (PFC) gives rise to the heaviest projection to MD, it is not the only cortical region projecting to thls nucleus. Degeneration methods, and more re- cently neuroanatomical techniques based on axonal transport, have in- dicated that the cortical sources of MD afferents are considerably richer. The first papers which considered this problem established an affe- rent projection to MD, mainly to its medial segment, originating in the cortex of temporal lobe, both in monkey (67) and cat (17, 53). The same segment was shown to receive axonal terminals from the olfactory cor- tex of the piriform lobe in the rat (16, 30, 43) and tree shrew (55). Sub- sequently, such connections were demonstrated also in other species wjth electrophysiological (39, 57) as well as horseradish peroxidase (HRP) and autoradiographic methods (8, 13, 52, 63). After injections of HRP to MD in the tree shrew (46), rat (47, 52), cat (9, 36, 42, 53) and rabbit (5), retrogradely labeled neurons were found in the part of the cortex covering the claustrum, known as the insular cortex. In addition, these connections have been described to be topographically organized in the rat (47). The lateral segment of MD, by contrast, has been shown to be con- nected with the cortex of the anterior cingulate gyrus (10, 17, 46, 52, 54) and the motor cortex (3-5, 17, 27, 28, 63). In the monkey, where the motor connections of MD are best known, their topography has also been established. Thus, the most lateral, paralamellar, segment of MD received projections from the primary motor cortex (area 4), whereas the more centrally located - parvocellular segment was connected with area 6 of the premotor cortex (4). Recently, connections arising from the ectosylvian and posterior syl- vian gyri (somatosensory, gustatory and auditory areas), suprasylvia~l gyrus (parietal association cortex), and, most surprisingly, from visually responsive areas in the occipital lobe, were described in the cat (17, 18, 34). Until now, these projections have not been confirmed in other species. Information concerning the cortical afferents of MD originating outside PFC in the dog's brain is very spwce. In addition to the topo- graphy of the PFC-MD projection (2, 21-23, 40, 58), only the relation- ships between the moto~r cortex and the lateral segment of MD have been selectively examined (24). In this paper we tried to systematize medial and lateral MD afferents regarding their relations to particular functional systems.
MATERIAL AND METHODS Eleven young (about one year old) dogs of either sex, weighing 8-13 kg were used. The animals received stereotaxic injections in h4D of 0.15-0.3 p1 30°/o HRP (Sigma, type VI or Boehringer) solution. Coordina- tes of all injection points were established on the basis of a stereotaxic atlas of the dog's brain (31). All injections were divided into three groups, comprising the medial (group I), lateral (group 11) and central (group 111) part of MD nucleus, respectively (7-8 cases in each group). The in- jections were made, first unilaterally and then bilaterally, due to~the statement only ipsilateral projections. The microsyringe needle was in- serted vertically into the thalamus. All animals survived 48h, then they were deeply anaesthetized and perfused through the heart with physio- lcgical saline followed by a mixture of 1°/0 psraformaldehyde and 2,5O/n glutaraldehyde or 4O/u formaline in phosphate buffer (pH = 7.4). After removal the brains were placed in 3O0/0 sucrose for 48h and then cut into 40 pm coronal frozen sections. To reveal the location of active HRP Mesulam procedure was used (38). The sections were mounted on glass slides and counterstained with cresyl violet or neutral red. Sections we- re examined in the light microscope and HRP-polsitive neurons were localized in the various cortical fields according to the Kreiner division (25). In 5 animals out of 11, the enzyme injection,^ were preceded by le- sons of the medial or lateral PFC surface. This procedure was use'd to analyze whether the elimination of the projections from PFC to MD might increase the intensity of HRP uptake by the axonal terminals of the other projection systems, as suggested by some investigators (52). In order to exclude incorrect interpretation, two type,s of control ex- per~mentswere made. First, the enzyme was injected into structures surrounding MD, because in some experiments the area of HRP diffu- sion spread beyond MD nucleus. The other control experiment was made in order to exclude HRP uptaking by damaged axons passing through MD region. It consisted in implanting a cannula in MD through which 7 days later a needle filled with HRP was inserted and an injection itlade (63). The results of all control experiments were taken into ac- count in the final analysis of labeled cells localization.
RESULTS
The tlistribution of labelecl, cells following medial ME injections (group I) The r~sultsreceived In th~sgroup of injections are illustratzd on the exxnple of dog A45 (F~gs.1 and 2). The prolectlons to this MU region or~glnatedfrom the cortical llrnblc areas, both lateral snd medial surfa- ces of the hem~sphere(Fig. 2B). On the lateral surface the majority of HRP-pos~t~iveneurons was concentrated 1n the region surrounding the anterior rhlnal sulcus (sRha), along a considerable part of its length (Fig. 2Bc-f). It corresponded largely to the insular cortex on the depth of which lies the claustrum. This zone of the intensive labeling of cells spread on to cortical areas located dorsally and to a lesser degree ven- trally (Fig. 2Bc-g). In adjacent zones labeled neurons became more and more scattered. Dorsally and rostrally to the anterior rhinal cortex labeled cells were observed in the posterior region of the orbital gyrus (ORB, Fig. 2Bc and 3). In all cases of injections in this group, labeled cells lying in the depth of the anterior rhinal sulcus and in the posterior zone of the orbital cortex formed a clear cellular band. This band did nlot extend to the anterior zone of the orbital cortex. On the other hand, dorsally and caudally to the anterior rhinal cortex this band of cells seemed to continue into the region of posterior insular cortex, where the number of labeled neurons was quite considerable (c.i., Fig. 2 Be-g). Sporadically labeled cells were seen in the cortex of sylvian and ectosylvian gyri (S, ES, Fig. 2Be-g). The ventral continuation of intensive labeling zone located in the depth of anterior rhinal sulcus was composed of nume- rous cells, which were found in the deep layers of the piriform cortex (c.p., Fig. 2Be-f). Such cells were observed in the anterior (prepiriform area), central (periamygdaloid area) as well as posterior (enthorhinal area) parts of this cortex. The second zone with numerous HRP-positive cells has been obser- ved on the medial surface of the hemisphere. It comprised the cortex of the anterior part of the subcallosal gyrus lying below corpus callosum (SC, Figs. 2Bc and 4) and also the genual area located beneath the genu- a1 sulcus (G, Fig. 2 Ba, b). Single HRP-positive cells were observed also in the anterior part of the cingular cortex (CN, Fig. 2Bd). The distribution of labeled cells following lateral MD injections (group 11) The distribution of labeled cells after lateral HRP injections is illu- strated on the example of dog L4 (Fig. 5). The projection to this part of nucleus originated mainly from the dorsal region of the frontal cortex. Following these injections the numerous labeled neurons were observed in the depth and the both walls - (lateral and medial) of the presylvian fissure (fPs, Figs. 5Ba-d; and 6). Whilst in the internal composite area of the lateral wall (CJ, Fig. 5Bb-d) more closely connected with the mo- tor cortex (24) they were extremely numerous and distributed quite eve- nly, in the paraorbital area of the medial wall they were much less nu- merous and concentrated mainly in its dorsal region (PORd, Fig. 5Bb-d). The cortex lying on the medial surface in the precruciate area (XC, XF, Fig. 5Bc, d) was rich in labeled cells, too. Furthermore, numerous cells Fig. 1. An example of the injection site limited to the medial segment of MD. Frontal section through the thalamus counterstained with cresyl violet.
Fig. 3. Microphotograph of the posterior orbital cortex (see insert in the upper right corner) showing HRP labeled pyramidal neurons located in layer V and VI after injection to the medial MD. In some of neurons apical dendrites are visible. Fig. 4. Microphotograph of subcallosal cortex (see insert in the upper right cor- ner) showing HRP labeled neurons after injection to the medial MD. port.
Fig 5 The :fistr:oullon of iabelec! neurons alter injchet~trn of IZRP tc: the latera! segment of MD (dog L4i L'lerotatroi~sas in Fig 2. Fig. 6. Microphotograph of the cortex in the depth and both walls of presylvi fissure (see insert in the upper left corner) showing HRP labeled cells injection the lateral MD. were labeled in the sigmoid area (CX, Fig. 5;Bb, c). In the case of the injection involving the extremely lateral MD region, the labeled cells were numerous in the anterior sigmoid area and in to a lesser extent in the cortical regions of the presylvian fissure and medial precruciate area. In this group fewer labeled neurons were found in the limbic cortex of the anterior cingulate gyrus, the posterior orbital cortex as well as in the insular cortex, sylvian and ectosylvian gyri. Contrasting with group I, labeled cells in the limbic cortex of the medial surface, genual and subcallosal areas were not observed.
The distribution of labeled cells following central MD injections (group 111) In group I11 the injections involved the central MD region overlap ping partly with the medial as well as lateral segment of this nucleus (Fig. 7A). The distribution of labeled cells in the dogs of this group is shown on the example of dog C8 (Fig. 7B). G 8
A .mi. post.
Fig. 7. The distribution of labeled neurons after injection of HRP to the central part of MD (dog C8). Denotations as in Fig. 2. After such injections the numerous labeled cells appeared in the cortical fields which were the source of projections into the medial and lhteral segments of MD. Such neurons lay in the limbic cartex of the medial surface of hemisphere - genual area and anterior cingulate gy- rus, whereas on the lateral one, around the rhinal sulcus as well as the posterior part of the orbital gyrus. Sporadically they were observed in the cortex of sylvian gyrus. However, in this group the labeled cells were not observed in the subcallosal area and piriform cortex (Fig. 7B). In the dorsal cortical regions, HRP-positive cells were localized in the precruciate area (XC, XP, Fig. 7Bb-d) and on the lateral surface in the depth and both walls of the presylvian fissure (PORd, CJ, Fig. 7Ba-d). In contrast with group 11, the majority of such cells in group I11 were found in the medial wall of this fissure, whereas in the lateral wall they were considerably less numerous. The anterior sigmoid area was free of labeling. Comparison of the distribution of labeled neurons in this group with two previous groups (I and 11) indicates that the neurons of certain lim- bic regions (subcallosal area and piriform cortex) as well as anterior sigmoid gyrus send axons to the extreme MD regions, not involved in the group I11 injections. Control experiments Control injections were made to thalamic structures surrounding MD, e.g. the central lateral and parataenial nucleus as well as anterior nu- clei. Following injection to the central lateral nucleus the region of la- beling was localized more posteriorly than in the case of MD injection. It comprised the large region of the precentral gyrus and the dorsal wall of the coronal sulcus (CS), whereas projection to MD originated from the small region of the anterior sigmold area (CX, Fig. 5). These areas are included In primary motor cortex (11, 12). It should be empha- sized however, that injection site never comprised the region of ventral lateral nucleus, which is the main target of projection from the primary motor cortex. Injection to anter~or nuclei caused the significant labeling in the cmgular gyrus, whereas injection to the parataenial nucleus - in genu- a1 area. Our results showed, that these cortical regions are connected aiso with MD. However, in cingular and genual areas the labeling was more intensive after injection to above mentioned nuclei than to MD. In the analysis of the d~stributionof HRP-positive neurons in these cortical regions we paid a special attention to the limitation of injection site to, the territory of MD. Taking into account the possibility of diffuse HRP uptaking by da- maged axo'ns passing through MD (but ending in the other thalamic nu- clei) in each of experimental groups we made injection with the needle of microsyringe inserted through cannula implanted earlier in the thala- mus at the level of MD. The distribution of labeled cells after such in- jections was cormparable with the distribution of cells after injections made directly with a needle of microsyringe. Thus, we think that the needle does not injure significantly the fiber,s passing through MD, which could uptake HRP and label neurons in cortical areas not directly rela- ted to this nucleus. The other experiment with injection of HRP after PFC lesion was performed in order to eliminate the prefrontal cortex as the region the
Fig. 8. Schematic representation of topography of afferent MD projection origina- ting in the dog's brain cortex. A, shows lateral; B, medial surface of the hemi- sphere. Empty circles and filled circles show labeled neurons after injections to the medial and lateral MD, respectively. Note transitional zone in which empty circIes and filled circels are mixed. strongest connected to MD. Such lesi'ons in our material did not cause an increase in the amount of labeled cells in the other structures sending direct connections to this nucleus, as it has been suggested by some authors (52, 62). The number of labeled cells in the cortex which lay ipsilaterally as well as contralaterally to the destruction side was similar in dogs with intact and destroyed PFC.
Topography of projection which originates from the cortical regions located beyond the PFC
The analysis of the neurons localization in all groups of injections showed, that there are three characteristic cortical regions which give rise to the afferents to MD (Fig. 8). The first zone is strongly connected with the lateral segment of MD and involves cortical regions located on the mediodorsal, dorsal and lateral surface of the hemisphere. It begins in the posterior precruciate area on the mediodorsal surface, and is continued in the precruciate and slgmoid area on the dorsal one (oomprises central precruciate and sig- moid areas), whereas, on the lateral surface it sprous into the cortex of the depth of the presylvian fissure. The second projection zone is connected with the medial MD seg- ment. This zone is situated on the medioventral surface of the hemisphe- re and involves mainly the cortex of genual and subcallosal areas. The same zone involves also the piriform cortex of the ventral surface of hemisphere, reaching the cortex surrounding the rhinal sulcus and the posterior orbital gyrus on the lateral surface. The obtained results showed, that between two mentioned zones (dorsolateral and medioventral) the transitional cortical regions exist, which innervate both segments of MD nucleus. They comprise anterior cingulate cortex on the medial surface and the cortex of rhinal and sylvian sulci on the lateral surface.
DISCUSSION
Although the connections of the mediodorsal thalamic nucleus (MD) with the prefrontal cortex (PFC) in the dog have been studied previou- sly by different methods, its relation to the other cortical regions is poorly known. In the present studies injections limited to discrete parts of MD nucleus shsowed differentiation of the cortical MD afferents. The topography of these afferents suggests a division of the MD nucleus into two main segments, which are specifically related to functionally dif- ferent cortical regions. The lateral MD segment receives a specific pro- jection from the dorsally localized part of the motor and premotor cor- tex, whereas the medial segment is innervated by the ventral cortical areas regarded as limbic cortex. The cortical fields lying between these two specific zones innervate the large central region of the nucleus, except its extreme lateral and medial parts. It is very interesting that injections to the lateral MD segment reve- aled numerous labeled cells in the anterior sigmoid area as well as in the dorsal and medial precruciate areas. Localization of cells in the ante- rior sigmoid area is close to the anterior bank of the cruciate sulcus, overlapping partly with area of giant pyramidal neurons in layer V, which is defined in dog as primary motor cortex (12, 59). According to electrophysiological results this region is involved in the area of fore- limbs representation (11). The lab^eled neurons found more frontally and medially in the pre- cruciate areas as well as in the lateral presylvian wall, are localized in the cortex with smaller and more scattered pyramidal cells in layer V. From cytoarchitectonic point of view it could be regarded as premo- tor cortex (12). Functionally this region was established as secondary motor cortex which is responsible for bilateral movements of the trunk and head (11). Unfortunately, there exists no electrophysiological data about localization of the "frontal eye field" in the dog. However, it may be localized as in the cat (14, 15, 48) in the depth of the presylvian fis- sure, where in dog we also found numerous labeled cells. Such distribu- tion of labeled neurons overlaps with the previously described transitio- nal field between the prefrontal and motor cortex (24). The problem of projectilon from motor and premotor cortices to the paralamellar MD segment was investigated also in monkey (3, 4, 27, 28). The topography of this projection in dog and monkey is generally simi- lar. The neurons of primary motor cortex send their axons to the most lateral part of MD, whereas, the zone of terminals of neurons of secondary motor cortex is localized a little more centrally. The referen- ces to a weak projection from the premotor cortex to the lateral segment of the nucleus concern also cat's (17, 18) and rabbit's (5) brains. The afferent MD projection originates not only from the association, but also from primary cortical areas. Apart from motor afferents descri- bed above, a projection from the primary visual cortex (area 17) wais described too (17, 18, 34). All the data reffered to above show, that the definition of R'ose and Woolsey (who described the prefrontal co~rtexas the MD projection area) in its original form is not accurate and requires expanding, as it was suggested earlier (37). The limbic cortex which is related to the medial MD segment is 19- cated in the ventral half of the hemisphere. The genual and subcallosal areas of the medioventral surface as well as the piriform cortex seem to be specifically related to the medial MD segment. The labeled cells appeared there only following the most me- dially localized injections. However, in the literature there are no data concerning projections of genual and subcallosal areas to MD, whe- reas there are data which suggest their relationship with anterior tha- lamic nuclei (68). This fact confirms the relationship of the medial MD within the limbic system. The projection running from the piriform cortex is well known in various smpemcies(7, 16, 29, 39, 43, 55, 57). According to these data, the area of axonal terminals is always contained in the medial part of nucleus, although its extent was varied in the different species. On the other hand, the site of origin of this projection is also m'ore or less limi- ted, and includes the piriform, periamygdaloid and perhapi entorhinal cortices. Only in opossum did Benjamin and Jackson (1982), who stu- died the olfactory sources of the MD afferents, showed that the narrow band of the piriform cortex adjacent to the olfactory tubercle alone sent -connections to the medial segment of this nucleus. Taking into account the present results we suggest that in dog as in other species the piri- form cortex (mainly the prepiriform and periamygdaloid areas) is the source of afferents to the medial MD. . The area of medial MD afferents is continued on the lateral surface in; the ventral bank of the anterior rhinal sulcus. This region partly overlaps with the cortex receiving the strong connections from amygda- la (20, 26). The anterior continuation of this projection is the cortex of posterior orbital gyrus. The labeling of cells in this part of the orbital gyrus is usually independent of labeling in its anterior part whi'ch is included in the PFC. So, it seems reassonable to separate these mentio- ned parts of the orbital gyrus and include its posterior region in the lim- bic cortex. The jutification of this view could be supported by cytoar- chitectonic and my-eloarchitectonic results (25). According to our results between two cortical projection zones descri- bed above, a transitional zone could be identified. It includes the ante- rior part of cingulate gyrus on the memdial surface and quite a large cortical region of the lateral surface involving the dorsal bank of th,e anterior rhinal sulcus and the area o'f the sylvian gyrus. In our results the area of axonal terminals of this projection involved the large cen- tral part of MD nucleus comprising its medial and lateral segments. The projection originating in the cingulate cortex has been described in rat and cat as terminating exclusively in the lateral MD segment (10, 19, 52, 54). However, information concerning connections between the sylvian cortex and the MD nucleus in other species is sparse (17, 53). In spite of existence of three projection zones it seems reasonable to distinguish only two MD segments. It could be correlated with the func- tional damage following lesions in this structure. This damage, on one hand, leads to changes in emotional behavior (6, 32, 33, 41, 44, 49, 51, 60, 66), which can be explained on the basis of its relation to the limbic system. On the other hand, damage of the MD leads to movement impair- ments (44, 49, 50, 61, 65), which could be the consequence of a rela- tionship between the lateral MD and motor structures described in the present paper.
This investigation was supported by Project CPBP 0401 of the Polish Academy of Sciences.
ABBREVIATIONS
CA anterior composite area c.i. insular cortex CJ internal composite area CL central lateral nucleus CN cingular gyrus c.p. piriform cortex CS composite sigmoid area CX anterior sigmoid area ES ectosylvian gyrus f Ps presylvian fissure FPs bottom of the presylvian fissure G genual area HRP horseradish peroxidase MD mediodorsal thalamic nucleus ORB orbital gyrus PFC pref rontal cortex PORd dorsal paraorbital area S sylvian gyrus SC subcallosal area sCor coronal sulcus sCr cruciate sulcus sEs ectosylvian sulcus sG genual sulcus sL lateral sulcus sPG pregenual sulcus sRha anterior rhinal sulcus ~Rhp posterior rhirlal sulcus ss sylvian sulcus ssp1 splenial sulcus sss suprasylvian sulcus XC central precruciate area XP posterior precruciate area
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Acccptcd 10 Auyust 1988