Rom J Leg Med [26] 1-11 [2018]DOI: 10.4323/rjlm.2018.1© 2018 Romanian Society of Legal Medicine

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FUNDAMENTAL RESEARCH

Human gyrus cinguli as an anatomic marker in the neuronal system processing behavioural and cognitive act. Implications in forensic psychopathology

Ileana Marinescu1, Petru Răzvan Melinte2, Ileana Dincă2, Elena Pătrascu2, Mihaela Iustina Botoran Meșină2, Gheorghe S.Drăgoi3,4,*

_________________________________________________________________________________________ Abstract: The diversification of the analysis and evaluation methods of neuronal limbic system structures and of the gyrus cinguli in particular has led to the abandonment of classical methods of macro-neuro-anatomic dissection. We aim at working out a methodology for the macro-anatomic study of the form, relations and gyrus cinguli connexions in order to unveil the morphological features of gyrus cinguli that, in turn, might reveal the anatomo-functional correlations in psycho-neuro-pathology. The study was carried out on 81 human encephala of which 18 were taken from adults and 63 from feti. The topography of connective infoldings of the gyrus cinguli with limbic and paralimbic structures draws attention on the integrative potential of gyrus cinguli in the neuronal system coordinating behavioural and cognitive act. The anatomic and functional evaluation of this system enables the evaluation of location, connexions and lesions pertaining Brodman’s areas found on the cortical territories of gyrus cinguli, i.e. anterior cingulate cortex (ACC) for areas 25, 24 și 32; posterior cingulate cortex (PCC) for area 31 and retro splenial cortex (RSC) for area 30. We open a new perspective in approaching the macroanatomic, morphoscopic and morphometric aspects of gyrus cinguli and their connexions, correlated with the pathology of the deceased and the legal implications in forensic phychopathology. Key Words: Gyrus cinguli, Great limbic system, Connection infoldings, Brodman’s area, Processing system of behavioural and cognitive act.

1) University of Medicine and Pharmacy of Craiova, 5th Departament, Romania2) University of Medicine and Pharmacy of Craiova, Department of Anatomy, Romania3) Romanian Academy of Medical Science, Bucharest 4) University of Medicine and Pharmacy of Craiova, Doctoral School, Romania* Corresponding author: E-mail: dragoigs@gmail.com

INTRODUCTION

The interest for gyrus cinguli in the neuronal system of processing behavioural and cognitive act has increased along with the diversification of neuroanatomy studies (Burdach 1819 [1]; Gerdy 1838 [2]; Broca 1878 [3]), of neuro-microanatomy studies (Hammarberg 1895 [4]; Cajal 1901[5]; Johnston 1923 [6]), of functional neuro-anatomy study (Papez 1937 [7]; MacLean 1952, 1992 [8, 9]; Nauta 1973, 1979 [10, 11]; Nieuwenhuys et al. 1988, 2008 [12, 13]), of neuro-cyto-architecture study (Brodmann 1909 [14]; C.Vogt 1919 [15]; von Economo 1929 [16]; B.A.Vogt, 1993 [17]; Swanson and Petrovich

1998 [18]); of MRI neuro- imagery study ( Kremer et al. 2003 [19]; Ballmaier et al. 2004 [20]; McCormick et al.2006 [21]) and of PET neuro-imagery study (Lacerda et al. 2003 [22]; Narendran et al. 2011 [23]). In 1838 the French anatomist Pierre Nicolas Gerdy [2] described a “Ring-shaped convolution” (“Circonvolution annulaire”) on the medial face of the cerebral hemispheres, around the corpus callosum. The ring-shaped convolution was later equaled to “Circumvolution du corps calleux” (syn.“Lobe du corpe calleux”) in French Nomina Anatomica (Testut, 1929) [24] and re-named gyrus cinguli in Basel Nomina Anatomica (BNA, 1895) [25]. Pierre Paul Broca (1887) [3], neuro-surgeon and neuro-anatomist and

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Marinescu I. et al. Human gyrus cinguli as an anatomic marker in the neuronal system processing behavioural and cognitive act

Gerdy follower made the first anatomic integration of gyrus cinguli in a neuronal system. He associated gyrus parahippocampalis to gyrus cinguli and created a new entity which he called “Le grande lobe limbique”, found in French Nomina Anatomica (Testut 1929) [24] under the name the “Great Limbic Convolution” and later, as gyrus fornicatus in Basel Nomina Anatomica (BNA, 1895)[25]. James Wenceslaus Papez (1937) [7], American neuroanatomist, tried a first functional integration of the limbic lobe and the hypothalamus in a neuronal circuit (that was named after him) involved, in his opinion, in emotional control. Paul D.MacLean (1949 1952) [8, 9], American neurophysiologist and psychiatrist attemped a new anatomic and functional integration of the limbic lobe, hippocampus, corpus amygdaloideum and septum pellucidum in an entity that he called “Limbic system”. Walle J.H.Nauta (1973, 1979)[10, 11], Dutch neuroanatomist originating in Indonesia, expanded the concept of limbic system by including the preoptic area of the hypothalamus and medial mesencephalic structures - Mesencephalic central grey and Dorsal raphe nucleus - in an anatomo-functional system which he called “Limbic System Midbrain Circuit”, presumably involved in the endocrine and visceral mechanisms, on the one hand and the regulation of emotion and behaviour, on the other. Robert Nieuwenhuys și coll. (1988) [12] suggested the fusion of the “MacLean limbic system” and the “Limbic System Midbrain Circuit Nauta” into a new entity called the “Greater Limbic System”. In 1819 Karl Friedrich Burdach [1], German neuroanatomist and neurophysiologist discovered and termed the first paralimbic structure amygdala cerebri, before gyrus cinguli was identified, and later integrated it in the paralimbic neuronal system. The first detailed description of the amygdala cerebri was achieved in 1923 by J.B.Johnston [6] who called it amygdala complex. Its connexions were later on made clear by Swanson and Petrovich (1998) [18]. Today the macro-neuro-anatomic approach to necroptic gyrus cinguli has beed abandoned both in orthology and in psychopatology. In the present work, we attempt a new methodology for the macrocroanatomic analysis and evaluation of form, relations and connexions of gyrus cinguli which should enable transdisciplinary correlations in functional anatomy in general and in forensic psycho-neuro-pathology.

MATERIALS, METHODS AND TERMINOLOGY

Materials. The study on gyrus cinguli was carried out on human biological material obtained postmortem – complying with the norms of ethics and deontology - in the dissection labs from the Faculty of General Medicine of Craiova and in the morgue from the Filantropia Municipal Clinical Hospital of Craiova. The macroanatomic evaluation of gyrus cinguli form and connexion variability was carried out on 18 encephala

drawn from adults and were placed in 6 groups as follows: group 1- two cases; group 2 – 2 cases; group 3 – 3 cases; group 4 – 4 cases; group 5 – 2 cases; group 6 – 4 cases. The macroanatomic analysis of morphogenessis border grooves and connexion infoldings of gyrus cinguli was performed on 63 encephala drawn from feti of the following gestational age: 21 weeks – 12 cases; 24 weeks – 10 cases; 26 weeks – 8 cases; 27 weeks – 6 cases; 28 weeks - 5 cases; 30 weeks – 7 cases; 36 weeks – 6 cases; 34 weeks – 4 cases; and 40 weeks – 5 cases. Methods and terminology Once drawn from the crania, the encephala were washed in continual jet for 60 minutes. Fixation for 48 hours was done in formalin 10% buffered saline solution having the following composition: formaldehide 36-40% - 10 mL; Calcium carbonate 1g; Natrium cloride 0.9g and water ad. 90mL. Long-term fixation, for at least 30 days, was done through a new fixation in the same formalin 10% buffered saline solution. After cutting the encephalon medio-sagitally, gyrus cinguli were visualized on the medial face of the cerebral hemispheres. The analysis of the relief and connexions of gyrus cinguli was done on the areas and sectors limited by plane Cartesian ordinates and the origin center at the level of Monro interventricular orifice (Fig. 1). In order to term the areas and the sectors on the medial face of the cerebral hemisphere we resorted to the International Anatomical Terminology (I.T.A., 1998) [26] specific to the neuronal system, i.e. dorsal (syn. superior, cranial) and ventral (syn. inferior, caudal, basal) on the axis X-0-X’; anterior (syn. frontal) and posterior (syn. occipital) on the axis Y-0-Y’. Based on these two criteria, the we limited two regions (ventral and dorsal) and three sectors (I, II, III). Sectors were numbered clockwise, with Roman numbers and termed ventral-anterior (sector I); dorsal-anterior (sector II) and dorsal-posterior (sector III). Sector I corresponds to the location of ventral Anterior Cingulate Cortex (vACC). Sector II corresponds to the location of dorsal Anterior Cingulate Cortex (dACC). Sector III corresponds to the location of Posterior Cingulate Cortex (PCC). Corpus callosum was used as reference mark in order to limit the subsectors in sector I. We draw a perpendicular on axis X - 0 –X’, tangent to the anterior curve of genu corporis callosi, dividing sector I into two subsectors: pregenual (vACCpg) and subgenual ( vACCsg). The macroanatomic image was taken by Prof.univ.dr. Gheorghe S.Drăgoi, with a digital camera Canon Eos 1Ds MarkII and Macro Ultrasonic Lens EF 100 mm,F/2.8.

RESULTS

The macroanatomic study of cerebral hemispheres in adult and fetus human encephala aimed at the stereotopographic and morphogenesis investigation of gyrus cinguli, its infoldings and of the sulcus cinguli.

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A. Macroanatomic analysis of cerebral hemispheres in six groups of adult human encephala The configurations of gyrus cinguli, its connective infoldings and of the sulcus cinguli in each encephalon group were correlatively examined. Group no. 1 Gyrus cinguli is curved around the corpus callosum. From is origin, in the space situated under the rostrum corporis callosi, it envelops genu corporis callosi from the posterior to the anterior and becomes horizontal to the truncus corporis callosi and continues to the splenium corporis callosi where, through the isthmus gyri cinguli becomes connected to the gyrus parahyppocampalis. The upper ridge of gyrus cinguli is bordered and convoluted through the presence of vascular incisures. We also identified six connective infoldings:

cingulo-paraolfactor, ventral cingulo-frontal via cingulo-rostral infolding, dorsal cingulo-frontal , anterior cingulo-parietal, posterior cingulo-parietal and cingulo-temporal (Figs 1, 2, 3A and 3B). Sulcus cinguli appeares as a deep depression, discontinued through the connective infoldings intersecting it, i.e. the dorsal cingulo-frontal infolding and the anterior cingulo-parietal one. In its sinusoidal trajectory, sulcus cinguli succesively crosses Cartesian sectors I and II of the medial faces of cerebral hemispheres (Fig. 1) Sulcus cinguli originates in sector I, from under genu corporis callosi, at the interference of gyrus cinguli, paraolfactoria area and the rostral gyrus (Figs 1 and 2). At this level there are two connective infoldings: the connective infolding between gyrus cinguli and the paraolfactoria area and the connecting infolding between gyrus cinguli and the rostral gyrus

Figure 1. Adult human encephalon in group 1. Regions and Cartesian sectors of the medial aspect of the right hand side cerebral hemisphere. Brodman’s areas location estimation. Regions: a) Ventral and Dorsal on the cartesian orthogonal axis X-0-X’ ; b) Anterior and posterior on the cartesian ortogonal axis Y-0-Y’. Sectors: Sector I: vACC = ventral Anterior Cingulate Cortex ; vACCpg = ventral Anterior Cingulate Cortex pregenual; vACCsg = ventral Anterior Cingulate Cortex subgenual; Sector II : dACC = dorsal Anterior Cingulate Cortex ; Sector III : PCC = Posterior Cingulate Cortex. Structures: 1.Area paraolfactoria. 2.Rostrum corporis callosi. 3.Genu corporis callosi. 4.Truncus corporis callosi. 5.Gyrus cinguli. 6. Gyrus frontalis superior. 7.Lobulus paracentralis. 7a.Gyrus paracentralis anterior. 7b.Gyrus paracentralis posterior. 8.Precuneus. 8a. Anterior cingulo-parietal connective infolding: 8b). Posterior cingulo-parietal connective infolding. 9.Cuneus. 10 Gyrus lingualis. 11. Isthmus gyri cinguli. 12.Splenium corporis callosi. 13. Foramen interventriculare (Monro). Grooves: S1. Supraorbital sulcus (Broca). S2. Sulcus cinguli. S3. Sulcus paracentralis. S4. Sulcus precentralis. S5. Sulcus centralis. S6 .Ramus marginalis sulcus cinguli (sin. Sulcus marginalis). S7. Sulcus subparietalis. S8 Sulcus parietooccipitalis. S9. Sulcus calcarinus. Connective infolding: C1. Connective infolding between gyrus cinguli and rostral gyrus. C2. Connective infolding between gyrus cinguli and area paraolfactoria. C3. Dorsal cingulo-frontal connective infolding. C4. Connective infolding between gyrus frontalis superior and gyrus paracentralis anterior. C5. Anterior cingulo-parietal connective infolding. C6. Cingulo-temporal connective infolding.

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Marinescu I. et al. Human gyrus cinguli as an anatomic marker in the neuronal system processing behavioural and cognitive act

(Figs 1 and 2). The latter continues with the upper frontal gyrus, integrating itself into a complex structure, i.e. the ventral cingulo-frontal infolding via the rostral gyrus. The trajectory of the sulcus cinguli is broken in sector II by the dorsal cingulo- frontal infolding. It becomes separated from its supragenual portion, crosses sulcus cinguli and then connects to gyrus frontalis superior and, after a spiral trajectory, becomes connected to gyrus paracentralis anterior to finally reach gyrus precentralis (Figs 1, 3A and 3B). From behind this obstacle, from sulcus cinguli an incisure emerges towards the upper border of the cerebral hemisphere, making up the groove termed by Broca „incisures préovalaire” and sulcus paracentralis in the International Anatomical Terminology (1988).This groove separates gyrus paracentralis anterior, as the frontal part of the lobulus paracentralis from the medial

part of the gyrus frontalis superior. In sector III, after a horizontal trajectory parallel to truncus corporis callosi, sulcus cinguli is discontinued again by the anterior cingulo-parietal connective infloding. At this level we noticed a change of trajectory of the cingulate sulcus towards the upper part of the cerebral hemisphere. This part of the trajectory of the sulcus cinguli is termed sulcus marginalis (syn. Ramus marginalis sulcus cinguli). It becomes the borderline between gyrus paracentralis posterior and the anterior cingulo-parietal connective infolding from precuneus. In the suprasplenial part of the sulcus cinguli and posterior to the anterior cingulo-parietal connective infolding there is sulcus subparietalis, from which two separating incisures of the precuneus area appear. The anterior compartment is occupied by the anterior cingulo-parietal

Figure 2. Adult human encephalon in group 1. Detail. Macroanatomic distribution of the structures in the crossroads space (Carrefour Broca) from under rostrum corporis callosi in the right hand side cerebral hemisphere. Sectors: Sector I; Sector II; Sector III. Structures: 1.Rostrum corporis callosi. 2.Genu corporis callosi. 3.Septum pellucidum. 4.Truncus corporis callosi. 5.Fornis (Pars libera columnae fornicis). 6.Foramen interventriculare (Monro). 7.Fornix (Pars tecta columnae fornicis). 8.Commissura anterior. 9.Lamina terminalis. 10.Gyrus paraterminalis (sin. Subcallosal gyrus; Peduncle of the corpus callosum). 11.Chiasma opticum. 12.Nervus opticus. 13. Area paraolfactoria. 14.Gyrus olfactorius medialis. 15. Gyrus rectus. 16.Rostral gyrus. 17. Gyrus cinguli - pars subgenua. 18. Gyrus cinguli –pars pregenua. 19.Gyrus frontalis superior. Grooves: S1. The groove of the anterior cerebral artery. S2. Posterior paraolfactory sulcus. S3. Anterior paraolfactory sulcus. S4. Supraorbital sulcus (Broca). S5. Sulcus olfactorius (syn.Internal orbital groove). S6. Sulcus cinguli. S7. Sulcus corporis callosi. Connective infoldings: C1. Connective infolding between gyrus cinguli and area paraolfactoria. C2. Connective infolding between gyrus cinguli ant rostral gyrus. C3. Connective infolding between area paraolfactoria and rostral gyrus. C4. Connective infolding between area paraolfactoria and gyrus rectus. C5. Connective infolding between area paraolfactoria și gyrus olfactorius medialis. C6. Connective infolding betweeen rostral gyrus and gyrus frontalis superior (syn: Ventral cingulo-frontal infolding via rostral gyrus). C7. Connective infolding between gyrus cinguli and gyrus frontalis superior.

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connective infolding while the posterior compartment by the posterior cingulo-parietal connective infolding, the two merging together with the retrosplenial part of the gyrus cinguli and to form isthmus gyri cinguli which is a connective infolding with the gyrus parahippocampalis (Fig. 1). Group no. 2 Gyrus cinguli is threadlike in the origin, in the space from under rostrum corporis callosi. At this level three connective infoldings have been identified: the infolding between gyrus cinguli and area paraolfactoria, the one between area paraolfactoria and the rostral gyrus and the one between rostral gyrus and the medial olfactory gyrus. In sector II gyrus cinguli progressively increases its volume and the upper ridge is smooth, continuous and without convolutions (Fig. 3C). In sector III, the upper ridge is bordered and generates the anterior cingulo-parietal connective infolding. In the supra- and retro-spenial areas gyrus cinguli has two fissures. It is continuous, along with the retrospenial posterior cingulo-parietal connective infolding, with girus parahippocampsalis through isthmus gyri cinguli (Fig. 3C). Sulcus cinguli crosses sectors I and II uninterrupted because the dorsal cingulo-frontal gyrus is absent at this level. It defines the border between gyrus cinguli and girus frontalis superior. In the part above the sulcus cinguli trunk vascular incisures of gyrus cinguli can be seen, on the one hand and, on the other hand, the sulcus paracentralis that originates in sulcus cinguli and goes towards the upper ridge of the cerebral hemisphere. It makes up the borderline between gyrus frontalis superior and gyrus paracentralis anterior. In sector III the trajectory of the sulcus cinguli is interrupted by the presence of the anterior cingulo-parietal connective infolding. Before this connective infolding the trajectory of the sulcus cinguli is deviated obliquely, postero-laterally towards the upper border of the cerebral hemisphere and forms sulcus marginalis. Posteriorly, the anterior cingulo-parietal connective infolding is limited by sulcus subparietalis. In the precuneus area we have identified a connective system of gyrus cinguli and gyrus postcentralis through the anterior cingulo-parietal connective infolding, on the one hand and with gyrus parahippocampalis through isthmus gyri cinguli, via the posterior parieto-cingulate connective infolding, on the other hand, (Fig. 3 C). Group no. 3 Gyrus cinguli originates in sector I, under the rostrum corporis callosi and is part of the Carrfour Broca through two connective infoldings: the connective infolding between gyrus cinguli and area paraolfactoria and the infolding between gyrus cinguli and the rostral gyrus that continues with the gyrus frontalis superior. In sector II gyrus cinguli increases in volume and generates a dorsal cingulo-frontal connective infolding that has a vertical incisure. Posteriorly to this infolding we have identified a deep, vertical, sinusoid groove. It separates

the anterior cingulo-parietal connective infolding from the posterior cingulo-parietal infolding that also has a vertical incisure. In the retrosplenial space, the posterior part of gyrus cinguli comes together with the posterior cingulo-parietal connective infolding and makes up the cingulo-temporal connective infolding (syn. Broca’s temporo-limbic infolding) introduced in Basel Nomina Anatomică (1895) [25] as isthmus gyri fornicati and in Nomina Anatomica Parisiensia (1955) [27] as Isthmus gyri cinguli (Fig. 3D). Sulcus cinguli crosses without interruption sector I. In sector II the trajectory of the sulcus cinguli is interrupted by the dorsl cingulo-frontal connective infolding. Posteriorly to this infolding, from sulcus cinguli, sulcus paracentralis originates which is the border between gyrus paracentralis anterior and the medial part of the superior frontal gyrus. In sector III the sulcus cinguli is discontinuous because of the anterior cingulo-parietal connective infolding. At this level there appears a change of the sulcus cinguli trajectory towards the upper margin of the cerebral hemisphere and the formation of sulcus marginalis. This groove is the border between gyrus paracentralis posterior and the anterior cingulo-parietal connective infolding. Sulcus cinguli re-appears in precuneus area as sulcus subparietalis. It is a deep, sinusoid groove obliquely ascending towards the anterior part and separates two cingulo-parietal connective infoldings, one anterior and one posterior. The anterior infolding is limited by sulcus marginalis on the anterior aspect and sulcus subparietalis on the posterior (Fig. 3D). The central part of the anterior infolding is marked by a straight incisure that subdivides it into two subinfoldings reunited in their ventral and dorsal extremities. The posterior infolding is limited by sulcus subparietalis on the anterior aspect and by sulcus parieto-occipitalis on the posterior part. It is subdivided by a secondary incisure under the form of recumbent capital letter H into two subinfoldings reunited in their ventral and dorsal extremities Fig. 3D). Group no. 4 Gyrus cinguli, in its origin, in sector I, under the rostrum corporis callosi, makes two connexions: one with the paraolfactoria area and one with the rostral gyrus through which it is connected to gyrus frontalis superior. We have identified a volumic increase of the gyrus cinguli in sectors II and III. The upper ridge of gyrus cinguli has a sinusoid trajectory and a convoluted aspect in sector III. The anterior cingulo-parietal connective infolding breaks away from the horizontal part of gyrus cinguli and is limited by sulcus marginalis on the anterior aspect and the sulcus subparietalis on the posterior part (Fig. 3E). The posterior cingulo-parietal connective infolding, under the form of a piramid, is limited on the interior by sulcus subparietalis, perpendicular on the upper ridge of the cerebral hemisphere, and by sulcus parieto-occipitalis on the posterior. It presents deep vascular grooves. The retrosplenial part of the gyrus cinguli is fused with the

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Marinescu I. et al. Human gyrus cinguli as an anatomic marker in the neuronal system processing behavioural and cognitive act

Figure 3. Adult human encephala. Architectural variability of gyrus cinguli in 6 groups of encephala. 1.Sulcus cinguli. 2.Dorsal cingulo-frontal connective infolding 3.Sulcus paracentralis. 4.Ramus marginalis sulcus cinguli 5.Sulcus subparietalis. 6.Sulcus parietooccipitalis. 7.Sulcus calcarinus. 8.Supraorbital sulcus (Broca). 9. Ventral cingulo-frontal connective infolding via rostral gyrus. 10.Gyrus paracentralis anterior. 11.Gyrus paracentralis posterior. 12.Gyrus precentralis. 13.Gyrus postcentralis. 14.Anterior cingulo-parietal connective infolding. 15. A.collosomarginalis.16.R.frontalis anteromedialis. 17.A.pericalosa. 18.Rr paracentrales.19.Rr. precuneales.20.Rr. parietooccipitales. Macrophotografies of the medial aspects of cerebral hemispheres (A,B-G) and at the border medial and superior lateral aspect (B, H).

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posterior cingulo-parietal connective infolding and forms isthmus gyri cinguli (Fig. 3E). Sulcus cinguli crosses sectors I and II uninterrupted. The first discontinuity of the sulcus cinguli trajectory was identified in sector III, generated by the anterior cingulo-parietal connective infolding. It is bordered by sulcus marginalis on the a anterior and by sulcus subparietalis on the posterior plus an emerging incisure that has an ascending trajectory towards the upper part of the cerebral hemisphere. Sulcus marginalis appears like an incisure derived from sulcus cinguli. Its trajectory is curvelike, with the posterior upward convexity to the upper margin of the cerebral hemisphere. This is the border between gyrus paracentralis posterior and the anterior cingulo-parietal connective infolding. Sulcus paracentralis appears like a deep groove separated from the sulcus cinguli. It has a straight, sinusoid trajectory up to the margin of the cerebral hemisphere where it forms the border between gyrus paracentralis anterior and gyrus frontalis superior (Fig. 3E). Sulcus subparietalis is situated in precuneus and makes the border between the anterior cingulo-parietal connective infolding and the posterior cingulo-parietal connective infolding. The latter is subdivided by a curved incisure, its posterior concavity having two subinfoldings, anterior and posterior, re-united dorsally and ventrally Fig. 3E). Group no. 5 The variability of gyrus cinguli, sulcus cinguli and of the connective infoldings of the gyrus cinguli depend on the stereodistribution of anterior and posterior cerebral arterial branches. Two of the postcommisure branches (Segmentum A2) of the anterior cerebral artery contribute to the morphogenesis of cingulate structures, i.e. arteria pericallosa și arteria callosomarginalis. Arteria pericallosa was easily identified in the sulcus corporis callosi. From its origin in the anterior cerebral artery, it is in connection with genu corporis callosi which it circumscribes following an anteriorly convex curve (Fig. 3F). At the level of the truncus corporis callosi three important branches emerge, i.e. rr. paracentrales, rr. Precuneales și rr. parieto-occipitales. They contribute to the morphogenesis of incisures that cross gyrus cinguli and the connective infoldings within the bordering areas of lobululus paracentralis și precuneus. Form, trajectory and depth of cingulate sulcus are dictated by the presence of arteria callosomarginalis. It branches out into five arms: rr.frontalis anteromedialis, rr.frontalis intermediomedialis, rr.frontalis posteromedialis, rr.cingularis and rr.paracentralis (Fig. 3F). Of the posterior cerebral artery branches our attention was drawn by the medial occipital branch (Segmentum P4) that contributes to the angioarchitecture of the medial face of the cerebral hemisphere with five arterial branches, i.e. r. corporis callosi dorsalis, r. parietalis, r. parietoocipitalis, r. calcarinus și r. occipitotemporalis. An important anastomosis exists between the anterior

and posterior cerebral arteries through the participation of artera pericallosa emerging from the anterior cerebral artery, i.e. r. corporis callosi dorsalis of the posterior cerebral artery. Group no. 6 Along its trajectory gyrus cinguli is of variable thickness. In sector I, under the rostrum corpori calllosi it is thick and presents connexions with the area paraolfactoria and gyrus rectus. In the horizontal part of gyrus cinguli two dorsal cingulo-frontal connective infoldings have been identified; they come together again and are continuous with the gyrus frontalis superior (Fig. 3G). In sector III, the anterior cingulo-parietal connective infolding is crossed by a vascular incisure. It is limited by the sulcus marginalis on the anterior part and the sulcus subparietalis on the posterior. The posterior cingulo-parietal connective infolding has 3 convergent grooves. Sulcus cinguli has a sinusoid, discontinuous trajectory because of two connective infoldings that cross it, i.e. dorsal cingulo-frontal și anterior cingulo-parietal (Fig. 3G). The dorsal cingulo-parietal connective infolding is easily identifiable in sector II. It is bordered on the posterior aspect by sulcus paracentralis, has antero-dorsal oblique trajectory and connects to gyrus precentralis through gyrus paracentralis anterior. In Cartesian sector III sulcus cinguli becomes again posterior to the dorsal cingulo-frontal connective infolding and continues with two grooves, i.e. an anterior one called sulcus paracentralis and a posterior one, sulcus marginalis. These grooves plus sulcus cinguli make up the border between, lobulus paracentralis, gyrus cinguli, and the anterior cingulo-parietal connective infolding. In sector III, in precuneus, we have identified the terminal part of sulcus cinguli under the form of sulcus subparietalis, that appears like a deep depression of postero-dorsal, ascending, oblique trajectory (Fig. 3G). It is the border between two cingulo-parietal connective infoldings, i.e. antero-dorsal and postero-ventral. The antero-dorsal cingulo-parietal connective infolding connects to gyrus postcentralis through gyrus paracentralis posterior. The postero-ventral cingulo-parietal connective infolding connects to gyrus parahippocampalis via isthmus gyri cinguli.

B. Morphogenesis macroanatomic analysis of the medial aspect of cerebral hemispheres in the nine groups of human fetus encephala The results of the macroanatomic analysis performed out on 63 human fetus encephala has led to the conclusion that the formation of gyrus cinguli, primary and secondary border grooves and of the connective infoldings on the medial part of the encephalon is a a slow process, developing in time and space (Figs 4 and 5). In week 21 the authors noticed the development of two primary grooves, i.e. Sulcus calcarinus and Sulcus parietooccipitalis (Fig. 5A). In week 24 a third primary groove appeares, i.e. Sulcus cinguli. At the level of the occipital lobe, sulcus calcarinus between cuneus and

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Marinescu I. et al. Human gyrus cinguli as an anatomic marker in the neuronal system processing behavioural and cognitive act

Figure 4. Fetal human encephalon. Morphological differentiation of gyrus cinguli connective infolding 1.Area paraolfactoria.2.Gyrus cinguli.3.Gyrus frontalis superior.4.Gyrus paracentralis anterior.5.Lobulus paracentralis.6.Gyrus paracentralis posterior.7.Precuneus.8.Cuneus.9.Gyrus lingualis.10.Isthmus gyri cinguli.11.Gyrus parahippocampalis. Grooves and incisures: S1.Sulcus cinguli. S2. Sulcus paracentralis. S3.Sulcus centralis.S4.Sulcus postcentralis. S5.Ramus marginalis sulcus cinguli.S6.Sulcus subparietalis.S7.Sulcus parietooccipitalis.S8.Sulcus calcarinus.S9.Incisura occipito-limbica. S10.Supraorbital sulcus (Broca). Connective infolding: C1.Cingulo-rostral connective infolding. C2. Connective infolding between gyrus cinguli and area paraolfactoria. C3.Dorsal cingulo-frontal connective infolding. C4. Anterior cinguloparietal connective infolding. C5. Posterior cingulo-parietal connective infolding. C6. Precuneo-limbic connective infolding. C7.Cingulo-temporal connective infolding (Isthmus gyri cinguli). C8. Parahipocampo-lingual connective infolding. (A,B-G) and at the border medial and superior lateral aspect (B, H).

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Figure 5. Fetal encephalon . Antepartum morphogenersis of the medial aspect of cerebral hemispheres. 1.Gyrus cinguli. 2.Sulcus parietooccipitalis. 3.Sulcus calcarinus. 4. Pia mater vascular network. 5. Sulcus cinguli. 6. Ramus marginalis sulcus cinguli. 7. Anterior cingulo-parietal connective infolding. 8. Sulcus subparietalis. 9. Posterior cingulo-parietal connective infolding. 10. Supraorbital sulcus (Broca). 11.Sulcus paracentralis. GFs –Gyrus frontalis superior. Lp – Lobulus paracentralis. Pc – Precuneus. C – Cuneus. Gl – Gyrus lingualis.

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Marinescu I. et al. Human gyrus cinguli as an anatomic marker in the neuronal system processing behavioural and cognitive act

gyrus lingualis becomes visible. Sulcus parieto-occipitalis is present between precuneus ans cuneus (Fig. 5B). These grooves are straight and perpendicular on each other. Starting with week 30 sulcus parieto-occipitalis becomes longer antero-ventrally up to the connective infolding of gyrus lingualis with isthmus gyri cinguli. Secondary grooves are present and differentiate in week 30, i.e. Sulcus paracentralis, Ramus marginalis sulcus cinguli, Sulcus sub-parietalis, frontale și cingulate incisures derived from sulcus cinguli (Fig. 5 F-I; Fig. 4 A and B). The connective infoldings with gyrus precentralis (ventral cingulofrontal, dorsal cingulofrontal, gyrus paracentralis anterior), with gyrus postcentralis (Gyrus paracentralis posterior, anterior cingulo-parietal connective infolding) and with the hippocampus (posterior cingulo-parietal infolding) are well-formed beginning with the week 34.

DISCUSSION

Anatomically speaking, gyrus cinguli is not an independent entity. It is an important component of the “Greater limbic system” and is part of a network of interconnexions, of the alocortex and isocortex (Drăgoi, 2008) [28] Our study yields clear data revealing the connexion of gyrus cinguli with limbic and paralimbic neuronal structures. These connexions are made by the connective infoldings seen in the sectors of the Cartesian ortogonal system drawn on the medial aspect of cerebral hemispheres. The variability of the gyrus cinguli form is dictated by the morphology of its upper margin. It is crenellated through the presence of several vascular incisures emerging from the sulcus cinguli in groups 1, 3, 5, 6 and their absence in groups 2 and 4. The trajectory of sulcus cinguli is interrupted by the connective foldings emerging from gyrus cinguli, i.e. the dorsal cingulo-frontal infolding in groups 1, 3, and 6 and the anterior cingulo-parietal infolding in groups 1 – 4. They break up the sulcus cinguli and facilitate the emergence of three new adjacent grooves, i.e. paracentralis, marginalis and subparietalis. We noticed a particular spatial distribution of the connective infoldings in sectors I – III. In sector I, in the space below rostrum corporis calosi they have identified infoldings of direct connextion of gyrus cinguli with area paraolfactoria and gyrus frontalis superior and an indirect connexion with gyrus rectus and with gyrus olfactorius medialis, via area paraolfactoria. In sector II we have identified the presence of the dorsal cingulo-frontal connective infolding emerging from the supragenual part of gyrus cinguli in groups 1, 3, 5, 6. It connects gyrus cinguli to gyrus precentralis via anterior paracentral gyrus. In groups 2 and 4 the dorsal cingulo-frontal connective infolding is absent but a new connective infolding has been identified, i.e. the ventral cingulo-frontal infolding. It makes the connexion with gyrus paracentralis via a host of intermediate connective infoldings, i.e. the infolding between gyrus cinguli and area paraolfactoria, the

infolding between area paraolfactoria and rostral gyrus and the infolding between gyrus frontalis superior and gyrus paracentralis anterior. In sector III, in the precuneus of the parietal lobe the authors have identified the anterior cingulo-parietal connective infolding that makes a double connexion, i.e. the first with gyrus postcentralis via gyrus paracentralis posterior and the second with the isthmus gyri cinguli via the the posterior cingulo-parietal gyrus. The estimation of Brodman’s areas at the level of gyrus cinguli cortex is particularly important for the anatomic and functional evaluation of the neuronal system processing behavioural and cognitive act. Three cortical territories are of special interest from this angle: the anterior cingulate cortex (ACC) for Brodman’s areas 25, 24, and 32, the posterior cingulate cortex (PCC) for Brodman’s areas 23 and 31 and the retrosplenial cortex (RSC) for Brodman’s areas 26, 29 and 30 (Fig. 1). The anterior cingulate cortex (ACC) is involved, through cingulo-frontal and cingulo-amyglaloid interactions in motivational and emotional functions. The lesions of the anterior cingulate cortex are associated with hypokinetic manifestations, apathy and emotional instability existing in patients with epileptic manifestations, schizophrenia and bipolar disorder, The posterior cingulate cortex (PCC) is involved, through temporo-cingulate and thalamo-cingulate interactions in cognitive functions, memory and attention focusing. The lesions of the posterior cingulate cortex are associated with depression, lack of attention, of memory and sensitive-sensory processing. Retrosplenial cortex (RSC) is involved in cognitive functions, episotic memory and in the pathology in ante-retrograde and retrograde amnesia, topographic disorientation and in the prodromal stage of Alzheimer’s disease.

CONCLUSION

1. Gyrus cinguli is an important anatomic marker in the neuronal system processing behavioural and cognitive act via its connexions with frontal, parietal and occipito-temporal lobes. 2. The accuracy of the macro-anatonic study of gyrus cinguli on postmortem human material requires the observation of a strict evaluation protocol and transdisciplinary evaluation. 3. Working on sectors in Cartesian co-ordinates of the medial aspects of cerebral hemispheres helps in marking the crossings of the teritories of gyrus cingulate connective infoldings involved in the neuronal system of processing behavioural and cognitive act. 4. The territory under rostrum corporis callosi represents a transit topographic zone of gyrus cinguli towards the paralimbic structures of the amygdala complex. 5. Lobulus paracentralis and precuneus appear as transit topographic zones of the gyrus cinguli connective infoldings with the prefrontal cortical areas and witht

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parieto-occipito-temporal ones. 6. Lobulus paracentralis must be considered as a transit topographic zone of the cingulo-frontal, ventral and dorsal connective infoldings with the gyrus precentralis a and somatomotor. 7. Precuneus is a crossroads of the connective

infoldings with the somato-sensitive postcentral gyrus, on the one hand and the paralimbic structures of the parietal lobe, on the other.

Conflict of interest. The authors declare that there is no conflict of interest.

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