Projections from the amygdaloid complex to the piriform cortex: A PHA-L study in the rat
Step 6 At the caudal end of the amygdala Figs 3E4J—K and 5the gyrus ambiensincluding the medial intermediate subfield of the entorhinal cortex, is replaced by the amygdalo-hippocampal area and the uncus, which is composed of the subiculum and the CA1 subfield 64 Therefore, we concluded that the use of the perirhinal cortex to define the thickness of the piriform component of the PCA does not significantly affect the data evaluation.
References
The amygdalo-hippocampal area becomes apparent at the caudal part of the gyrus uncinatusrostral to the hippocampal fissure Fig 1D. It is the site of action for the proconvulsant action of chemoconvulsants. Therefore, it is advisable to employ identical section thickness to use the minimum number of MR partitions to estimate the volumes
LATEST VERSION OF CCLEANER FOR WINDOWS 7 Differences between the study groups were determined by using the Mann-Whitney test with the Bonferroni adjustment x 3 for multiple comparisons. From Wikipedia, the free encyclopedia.
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We hypothesized that the piriform and cortical amygdala is damaged in a subpopulation of patients and, further, it is most damaged in patients with lesions in other temporal lobe structures e. Comparative localization study of the brain according to the principles of cellular structures [in German].
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Step 5 Starting approximately 12 mm from the LI, the amygdala is at its largest and the temporal horn of the lateral ventricle appears ventrolateral to the amygdala Figs 3C4G and 5. Except for the hippocampus and amygdala, focal atrophies of the para-hippocampal cortices are virtually indiscernible with current cross-sectional high-resolution imaging. Repeated measurements were performed for 10 control subjects. Consequently, it is possible that atrophy of the perirhinal cortex can bias the estimation of the volume of the PCA.
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Patients and control individuals underwent imaging on a 1. This resulted in — contiguous T1-weighted images with a 1. Consequently, the reconstructed MR images and the histologic sections had an identical in-plane orientation and spacing, which facilitated the identification of the anatomic boundaries.
Using a different in-plane orientation on MR imaging would make the histologic boundaries difficult to reproduce and another MR imaging section thickness would impair the definition and contrast of the images if less than 2.
According to the histologically defined landmarks, the boundaries of the PCA were drawn manually by using a trackball-driven cursor. To minimize the effect of a possible bias, the cases were analyzed in random order without knowledge of the side of the epileptic focus.
The volumetric analysis of the hippocampus 55 , amygdala 7 and entorhinal cortex 54 , from these cases was previously reported see Table 1 for a brief description of the results. Normalized volumes and asymmetry ratios of the right and left hippocampus, amygdala complex and entorhinal cortex.
The histologic appearance and location of the PC area 51 of Brodmann [ 56 ] , the cortical amygdaloid nuclei including the anterior cortical nucleus, medial nucleus, and periamygdaloid cortex, as well as the amygdalo-hippocampal area are shown in Figure 1 for nomenclature of the human amygdala, see [ 57 ].
Together they form a ribbon located around the limen insulae and share a common trilaminated structure 58 — 61 that defines the paleocortex. Next, we describe the major anatomic landmarks used to identify each of these cortical regions in a rostral to caudal direction Fig 2.
Brightfield photomicrographs of thionin-stained sections on the coronal plane show cytoarchitectonic borders arrowheads of the different components of the piriform cortex-cortical amygdala PCA region as defined in the present study.
A is the most rostal at the level of the limen insulae and D is the most caudal hippocampal head. PC indicates piriform cortex; PRC, perirhinal cortex; es, endorhinal sulcus ; PAC, periamygdaloid cortex; L, amygdala lateral nucleus; EC, entorhinal cortex; AB, amygdala accessory basal nucleus; B, amygdala basal nucleus; ssa, sulcus semiannularis ; cs, colateral sulcus ; AHA, amygdalo-hippocampal area; CA1, hippocampal field 1; Sub, subiculum; hf, hippocampal fissure; asterisk, lateral ventricle.
Scale bar equals 2 mm. Schematic representation of the rostrocaudal location and extent of the major landmarks relative to the limen insula set at 0 used to define the PCA. The most rostral aspect of the PC is located in the caudolateral portion of the orbitofrontal cortex where it is situated lateral and ventral to the lateral olfactory tract.
From there, it extends to the dorsal medial temporal lobe where its major portion is located, and terminates in the periamygdaloid region where it fuses with the cortical amygdala. In Nissl preparations, the PC has a characteristic prominent S-shape, due to a cell-sparse layer I and densely packed layer II that is composed of large pyramidal cells.
Although the boundaries of the PC can be easily identified from the adjacent cortices in Nissl-stained histologic sections, there are no clues to outline its borders on correspondent MR images, particularly in the frontal lobe.
Therefore, to obtain a more reliable estimate of the PC volume, we focused on the temporal extension of the PC. There are also no landmarks for placing the border between the PC and the cortical amygdaloid nuclei the anterior cortical nucleus.
Therefore, the neighboring cortical amygdala and the amygdalo-hippocampal area were included in the analysis. Histologic analysis of 23 hemispheres demonstrated that the PC in the temporal lobe begins at the level of the limen insulae LI, or frontotemporal junction, formed at the junction between the frontal and temporal lobes in 21 of 23 cases Figs 3 and 4A.
In two cases, the rostral border of the PC was approximately 1 mm rostral to the LI. Therefore, the coronal MR imaging section containing the LI was demarcated as the section containing the most rostral portion of the PC Fig 5.
At this level, the dorsal border of the PC was drawn at the fundus of the endorhinal sulcus Figs 1A and 5. The most caudal section where the PC is present is located approximately 6 mm caudal to the LI Fig 5.
Here, the cortical amygdala occupies most of the dorsal surface of the medial temporal lobe. In histologic sections, the thickness of the PC reaches 1 mm throughout its full rostro-caudal extent. A is the most rostral and F is the most caudal.
A, Shows the limen insulae LI ; B, first section where the characteristic ovoid shape of the amygdala A can be recognized; C, full extent of the amygdala A with lateral ventricle appearing underneath asterisk ; D, appearance of the rostral hippocampus HC ; E, rostral hippocampus at the level of the hippocampal head and lateral ventricle asterisk ; and F, hippocampal fissure hf; arrow.
Scale bar equals 20 mm applies to all panels. Coronal 2-mm-thick MR images from a control subject demonstrate the outline of the PCA at different rostrocaudal levels. Line drawings of the same MR imaging sections demonstrating more anatomic details are shown in Figure 5 numbers in the lower left corner correspond to the levels of the line-drawings.
A is the most rostral and K is the most caudal. In panels A and B, the thickness of the perirhinal cortex, which serves as reference for the thickness of the PCA is indicated. Panel C marks the anterior-most limit of the entorhinal cortex.
In panels D, E and F, the characteristic ovoid shape of the amygdala can be recognized. Panel G shows the appearance of the subiculum. Panels H—K show the hippocampal head. EC indicates entorhinal cortex; cs, colateral sulcus arrow ; A, amygdala; es, endorhinal sulcus arrow ; HC, hippocampus; hf, hippocampal fissure arrow ; LI, limen insulae ; PRC, perirhinal cortex; ssa, s ulcus semiannularis arrow ; Sub, subiculum; and arrowheads, boundaries of the entorhinal and perirhinal cortices.
Scale bar equals 10 mm applies to all panels. Line-drawings corresponding to MR images in Figure 4 summarize the anatomic landmarks used to draw the outlines of the PCA. Only the images displaying critical landmarks are shown. In section 2 Fig 4C, the PCA extends down as far as the continuation of the limit of the white matter at its crossing with the pial surface alternatively, if it were absent, the limit is given by the visualization of the sulcus semiannularis.
Section 4 Fig 4D is at the level of the rostralmost portion of the amygdala. At this level, the PCA extends from the endorhinal sulcus down to the sulcus semiannularis ssa, or in its absence, as in the previous level.
Its thickness encompasses the entire cortical gray matter. In section 6 Fig 4F, the amygdala is larger. The PCA occupies the entire medial temporal cortex down from the endorhinal sulcus to the sulcus semiannularis.
In sections 7—9 Fig 4G—I, the rostral hippocampus appears. The PCA is defined as in level 6. In section 11, the opening of the hippocampal fissure hf marks the last image to be quantified. HC indicates hippocampus; cs, colateral sulcus ; Sub, subiculum.
Scale bar equals 10 mm all panels. The cortical amygdala is the most caudal segment of the olfactory allocortex, located on the medial surface of the human temporal lobe It is composed of several superficial amygdaloid nuclei with defined cytoarchitectonic, chemoarchitectonic, and connectional characteristics for nomenclature, see [ 57 ].
The present volumetric analysis included the cortical nuclei of the amygdala cortical amygdala, for short, composed of the anterior cortical nucleus, the medial nucleus, the nucleus of the lateral olfactory tract, olfactory amygdala [ 63 ] , the periamygdaloid cortex PAC 0 , PAC 1 , PAC 2 , PAC 3 , and PAC S subfields, and the posterior cortical nucleus Fig 1.
It extends down to the ventral bank of the sulcus semiannularis ssa where it borders the entorhinal cortex Fig 1B—C. At caudal levels it becomes continuous with the amygdalo-hippocampal transitional area Fig 1D.
Rostrally, the cortical amygdala including the PACo appears at the level of the beginning of the amygdala approximately 6 mm caudal to the LI 64 Figs 1B and 5. One section caudally, where the amygdaloid complex is larger Fig 5 and often the temporal horn of the lateral ventricle is present, the cortical amygdala including the anterior cortical nucleus, nucleus of the lateral olfactory tract, PAC3, and PACs extends as far as the border with the rostromedial portion of the entorhinal cortex at the fundus of the sulcus semiannularis In cases, where the sulcus semiannularis is not apparent, the border defined by the line extending medially from the white matter to the surface of the brain was used as the ventral border of the cortical amygdala Fig 5 At the beginning of the subiculum at the head of the hippocampus 64 , the cortical amygdala medial nucleus, posterior cortical nucleus, PACs becomes continuous with the amygdalo-hippocampal transitional area AHA Fig 1D.
This transitional area between the hippocampus and the amygdala 65 continues caudally the gyrus semilunaris, approximately at the level of the diverticulum unci The caudal end of the cortical amygdala comes into close contact with the amygdalo-hippocampal transitional area AHA, which establishes the link between the rostral extremity of the uncal hippocampal allocortex and the caudal end of the olfactory amygdala.
Due to the lack of any apparent landmarks to separate the AHA from the cortical amygdala, it was included in the volumetric measurement. The amygdalo-hippocampal area becomes apparent at the caudal part of the gyrus uncinatus, rostral to the hippocampal fissure Fig 1D.
The caudal limit of the AHA was coincident with the beginning of the hippocampal fissure in most of the cases. The PCA was outlined from the rostral to caudal direction, according to the MR imaging step-by-step protocol defined below.
Before PCA measurements in TLE patients, ten randomly assigned control subjects were selected for intra - and interobserver tests to assure the reproducibility of the protocol. Measurements of TLE subjects were performed by a single investigator P.
In cases where the cortical boundaries were not clear, a second opinion T. The localization of the PCA region in the medial temporal lobe is presented in coronal MR images in Figures 3 and 4 and schematically in corresponding line-drawings in Figure 5.
At this level, the PCA is composed of the PC, which was not identifiable in terms of different contrast. At this level, the entire cortex from the fundus of the endorhinal sulcus to the most medial point of the gyrus semilunaris on the medial temporal cortex was included into the PCA.
If the sulcus semiannularis was already present, the fundus of the sulcus was considered to be the ventral limit of the PCA. The entire thickness of the cortex was included in the PCA. On the next 2. Starting approximately 12 mm from the LI, the amygdala is at its largest and the temporal horn of the lateral ventricle appears ventrolateral to the amygdala Figs 3C, 4G and 5.
At this level, the sulcus semiannularis is near its end, and it may be either absent or show a shallow appearance on MR images. If the sulcus semiannularis is visible, the PCA extends from the fundus of the endorhinal sulcus to the fundus of the sulcus semiannularis.
In the cases were the sulcus semiannularis cannot be identified, the approximate ventral limit of PCA was determined by the intersection of the line extending from the white matter under the amygdala medial extension of the external capsule to the surface of the brain, as defined previously 50 for the entorhinal cortex.
The entire thickness of the cortex was included into the PCA. In more caudal sections where the rostral end of the hippocampus uncus appears Figs 3D, 4H—I, and 5 , the PCA is defined accordingly. At the caudal end of the amygdala Figs 3E, 4J—K and 5 , the gyrus ambiens, including the medial intermediate subfield of the entorhinal cortex, is replaced by the amygdalo-hippocampal area and the uncus, which is composed of the subiculum and the CA1 subfield 64 , At this level, the endorhinal sulcus becomes very narrow and locates in close proximity to the optic tract.
The last section, in which the PCA was present, was usually coincident with the opening of the hippocampal fissure Figs 3F, 4K and 5. The outlines of the PCA were drawn as in Step 5. Once the PCA cortices were outlined on each of the coronal images, the final volume was calculated by using a program developed in-house for a standard work console.
As it is generally accepted that interindividual variability in head size affects the volumes of brain regions, we corrected the PCA volume to the individual brain area obtained at the level of the anterior commissure, according to Cendes et al 67 with modifications Briefly, we used the formula: Ten randomly assigned control subjects were selected for intra - and interobserver tests, by using the method introduced by Bland and Altman Repeated measurements were performed for 10 control subjects.
The mean difference in volume was near zero and thus, not considered significant. Scatter plots show the intra - and inter-observer variability of repeated measurements in the assessment of the right and left volume of the PCA of 10 control subjects.
A, shows intra-observer measurement P. The limits of agreement between the first and second measurements are expressed as the mean difference in volume: Inserts in the lower left corner show the association between the first x-axis and second y-axis.
For statistical analysis, the patients were divided into two groups according to localization of the seizure focus: Because the initial statistical survey indicated that the parameters studied were not normally distributed and the number of subjects in each study group was small, nonparametric analyses were used.
Differences between the study groups were determined by using the Mann-Whitney test with the Bonferroni adjustment x 3 for multiple comparisons. To assess the degree of volume asymmetry, the PCA asymmetry ratio was calculated according to Bernasconi et al Subsequently, patients were divided accordingly to their measured hippocampal volumes HCvol in HS patients, if the volume was less than two SD from the control mean and without HS if HCvol was at least two SD from the control mean.
A P value of less than. Figure 7 is the plot of the volume estimation for the PCA areas in the seven hemispheres quantified. In addition, the contribution of the point counting to the overall coefficient of error was approximately half of the contribution of the variability between sections.
Values obtained were smaller compared with MR imaging determinations. Plot of the individual volume estimation of the PCA, obtained by the stereological assessment of seven brain hemispheres see Materials and Methods section for details.
Each square represents a case. The mean normalized volumes and the asymmetry ratios of the PCA volumes in control subjects are shown in Table 2. There was no significant right—left asymmetry in the mean volumes. There was no sex difference in the PCA volumes.
Also, there was no correlation between PCA volume and age. Normalized volumes and asymmetry ratio of the right and left piriform-cortical amygdala in control subjects and patients groups and subgroups.
The sex distribution and mean age did not differ between control subjects and patients with TLE. When control subjects and patients with right or left TLE were compared, there were differences in the mean PCA volumes between groups.
The mean contralateral PCA volume did not differ from that in control subjects Table 2. The mean right PCA did not differ from that in control subjects. We assessed whether the volume reduction within the PCA is associated with hippocampal, amygdaloid, or entorhinal atrophy Table 1.
Scatter plots show the correlation between the ipsilateral and contralateral volumes of the PCA and the volumes of the hippocampus A, amygdala B, and entorhinal cortex C in patients with TLE.
PCA volumes correlated with the atrophy in the hippocampus, amygdala, and entorhinal cortex. Closed circles refer to the ipsilateral values and open circles to the contralateral values. There were no patients with an entorhinal cortex volume reduction of less than two SDs from the mean of the control subjects The volume of the ipsilateral or contralateral PCA did not correlate with the lifetime seizure number.
In the present study, we developed a method to measure the volume of the PCA in coronal MR images of the human brain. This method allowed us to assess the occurrence and severity of PCA atrophy in patients with TLE and its co-occurrence with volume reduction in the hippocampus, amygdala, or entorhinal cortex.
Only patients with an unknown etiology for TLE were included in the study. After establishing the adequate methodological considerations, the study revealed four major findings. First, there was no hemispheric asymmetry of the PCA in control subjects.
Also, the volume did not vary depending on the sex or age of the subjects. Fourth, there was no association between the PCA volumes and lifetime seizure number. The purpose of this study was to investigate the occurrence of damage in the PC and the cortical amygdala in patients with TLE by means of quantitative MR imaging.
Based on histologic analysis, we have elaborated a protocol that can be used to measure the volume of the human PCA in 2. Our MR protocol was designed based on anatomic landmarks derived from the analysis of histologic sections from postmortem brains of healthy subjects.
Thus, we were able to locate the different segments of the PCA and extrapolate the findings to determine the boundaries on MR images. The major difficulty was in determining the thickness of the piriform cortex. This cortical area appears embedded in the endorhinal sulcus on the first three MR images, starting at the LI, and there are no clear reference points to delineate this region on MR images.
Therefore, we used the thickness of the neighboring perirhinal cortex as a reference. Consequently, it is possible that atrophy of the perirhinal cortex can bias the estimation of the volume of the PCA.
Also, volume reduction of the perirhinal cortex is relatively uncommon, even in patients with intractable epilepsy 8 , 10 , Therefore, we concluded that the use of the perirhinal cortex to define the thickness of the piriform component of the PCA does not significantly affect the data evaluation.
The thickness and orientation of the MR images was set according to identical thickness and orientation of the histologic sections, facilitating in this way the identification of the boundaries and minimizing partial volume effects.
Even so, partial voluming is an inherent property of the discretized image and would still persist if the contrast between tissues were maximal or if the thickness was sub-milimetric.
Therefore, it is advisable to employ identical section thickness to use the minimum number of MR partitions to estimate the volumes Except for the hippocampus and amygdala, focal atrophies of the para-hippocampal cortices are virtually indiscernible with current cross-sectional high-resolution imaging.
Similarly, PCA atrophies can only be detected quantitatively. It is possible, however, that MR imaging performed at higher fields than 1. Still, we were unable to confirm our data histologically.
Indeed, to date there exists no gold standard consisting of MR imaging and histologic analysis of the same TLE cases. Future post-surgical or autopsy-based studies are needed to substantiate our data and to definitively establish the role that the human PC and cortical amygdala have as critical areas in epileptogenesis.
The results indicate a high concordance between PCA atrophies on one hand, and the EEG findings and the hippocampal atrophies, on the other. These data suggest that a reduced PCA volume or abnormal asymmetry index can be a useful addition to the tools currently used to determine the side of the seizure focus.
Volumetric MR imaging measurements of the amygdala 7 , 67 , entorhinal 54 , 70 , perirhinal 10 and parahippocampal 71 cortices, thalamus, lenticular and caudate nuclei 78 , fornix, and mammillary bodies 79 , 80 support the concept that tissue damage in TLE is not limited to the hippocampus, but involves other associated limbic structures.
These data are consistent with previous data suggesting that structural atrophy secondary to cell loss often extends outside the hippocampus. Furthermore, in the absence of clearly identifiable HS in TLE, extra-hippocampal damage, including that in the PCA, can be part of the epileptogenic zone responsible for the symptomatic findings.
Whether the damage in these various brain areas occurs at the same time or develops in parallel or sequentially later during the epileptogenic process 6 remains to be studied, along with the relative sensitivity, specificity and predictive value of the various quantitative MR imaging protocols that we have at our disposal to characterize the overall brain damage induced by TLE.
Atrophy of the PCA occurs in a subgroup of patients with TLE and the severity of the volume reduction correlates with hippocampal atrophy. These data demonstrate that the PCA is one component of the damaged temporal lobe network in humans.
Furthermore, volumetric assessment of the PCA provides additional information to determine the lateralization of seizure focus. We thank Professor Fernando Lopes da Silva for his constructive comments on the final version of this article.
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This article has not yet been cited by articles in journals that are participating in Crossref Cited-by Linking. Skip to main content. American Journal of Neuroradiology February, 26 2 ;. The study includes the estimation of the contribution of the point counting to the precision of the Cavalieri estimate of volume of the PCA according to the following equation, Thus, the contribution to the overall CE due to the variation between section areas of the PCA can be predicted from the equation, where subscript s and t means section and total respectively.
View inline View popup. Definition of the PC and Cortical Amygdala Borders in Histologic Sections The histologic appearance and location of the PC area 51 of Brodmann [ 56 ] , the cortical amygdaloid nuclei including the anterior cortical nucleus, medial nucleus, and periamygdaloid cortex, as well as the amygdalo-hippocampal area are shown in Figure 1 for nomenclature of the human amygdala, see [ 57 ].
Step 4 On the next 2. Step 5 Starting approximately 12 mm from the LI, the amygdala is at its largest and the temporal horn of the lateral ventricle appears ventrolateral to the amygdala Figs 3C, 4G and 5.
Step 6 At the caudal end of the amygdala Figs 3E, 4J—K and 5 , the gyrus ambiens, including the medial intermediate subfield of the entorhinal cortex, is replaced by the amygdalo-hippocampal area and the uncus, which is composed of the subiculum and the CA1 subfield 64 , Control Subjects The mean normalized volumes and the asymmetry ratios of the PCA volumes in control subjects are shown in Table 2.
Discussion In the present study, we developed a method to measure the volume of the PCA in coronal MR images of the human brain. Methodological Considerations The purpose of this study was to investigate the occurrence of damage in the PC and the cortical amygdala in patients with TLE by means of quantitative MR imaging.
PCA Atrophy is One Component of Overall Damage in the Temporal Lobe Volumetric MR imaging measurements of the amygdala 7 , 67 , entorhinal 54 , 70 , perirhinal 10 and parahippocampal 71 cortices, thalamus, lenticular and caudate nuclei 78 , fornix, and mammillary bodies 79 , 80 support the concept that tissue damage in TLE is not limited to the hippocampus, but involves other associated limbic structures.
Acknowledgments We thank Professor Fernando Lopes da Silva for his constructive comments on the final version of this article. Proposal for revised clinical and electroencephalographic classification of epileptic seizures. Epilepsia ; Proposal for revised classification of epilepsies and epileptic syndromes.
The epidemiology of epilepsy in Rochester, Minnesota, through Clinical characteristics of partial seizures. Recognized as neopallium or neocortex, enlarged dorsal areas envelop the paleopallial piriform cortex in humans and Old World monkeys.
Among taxonomic groupings of mammals, the piriform cortex and the olfactory bulb become proportionally smaller in the brains of phylogenically younger species. The piriform cortex occupies a greater proportion of the overall brain and of the telencephalic brains of insectivores than in primates.
The piriform cortex continues to occupy a consistent albeit small and declining proportion of the increasingly large telencephalon in the most recent primate species while the volume of the olfactory bulb becomes less in proportion.
The piriform cortex contains a critical, functionally defined epileptogenic trigger zone, "Area Tempestas". It is the site of action for the proconvulsant action of chemoconvulsants. From Wikipedia, the free encyclopedia.
Clinical Neuroanatomy and Neuroscience: Odor quality coding and categorization in human posterior piriform cortex. Nature neuroscience, 12 7 , Atlas of the human brain, 3rd edition. Coronal Atlas — Plate 8 anterior view.
Cameron; Rommelfanger, Karen S. Epithelium glands mucosa Sustentacular cell Tufted cell. Anatomy of the cerebral cortex of the human brain. Superior frontal gyrus 4 6 8 Middle frontal gyrus 9 10 46 Inferior frontal gyrus: Precentral gyrus Precentral sulcus.
Paracentral lobule 4 Paracentral sulcus. Primary motor cortex 4 Premotor cortex 6 Supplementary motor area 6 Supplementary eye field 6 Frontal eye fields 8. Superior parietal lobule 5 7 Inferior parietal lobule 40 - Supramarginal gyrus 39 - Angular gyrus Parietal operculum 43 Intraparietal sulcus.
Paracentral lobule 1 2 3 5 Precuneus 7 Marginal sulcus. Occipital pole of cerebrum Lateral occipital gyrus 18 19 Lunate sulcus Transverse occipital sulcus. Visual cortex 17 Cuneus Lingual gyrus Calcarine sulcus.
Fusiform gyrus 37 Medial temporal lobe 27 28 34 35 36 Inferior temporal gyrus 20 Inferior temporal sulcus. Subgenual area 25 Anterior cingulate 24 32 33 Posterior cingulate 23 31 Isthmus of cingulate gyrus: Retrosplenial cortex 26 29
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17.05.2017 - Visual cortex 17 Cuneus Lingual gyrus Calcarine sulcus. The results indicate that only selective amygdaloid nuclei or their subdivisions project to the piriform cortex.
Ccleaner-pro-full-version-for-free-2016 Scale bar equals 10 mm all panels. This page was last edited on 12 Februaryat This cortical area appears embedded in the endorhinal sulcus on the first three MR images, starting at the LI, and there are no clear reference points to delineate this region on MR images.
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29.08.2017 - Systematic sampling in stereology. At this level, the endorhinal sulcus becomes very narrow and locates in close proximity to the optic tract.
Ccleaner-mac-os-x-10-4-11 Control Subjects The mean normalized volumes and the asymmetry ratios of the PCA volumes in control subjects are shown in Table 2. The definition of anatomic landmarks on MR images was based on histologic analysis of 23 autopsy control subjects.
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30.07.2017 - Due to the lack of any apparent landmarks to separate the AHA from the cortical amygdala, it was included in the volumetric measurement. The assessment of patients with temporal lobe epilepsy TLE traditionally focuses on the hippocampal formation.
Ccleaner-pc-04-perfect-combiner-upgrade-set We then investigated the occurrence of PCA damage by quantifying the degree of atrophy as well as its association with the volumes of hippocampus, amygdala, and entorhinal cortex in patients with chronic TLE. Data of the distribution of pathways underlying the information flow between these regions are, however, incomplete and controversial.
The PCA occupies the entire medial temporal cortex down from the endorhinal sulcus to the sulcus semiannularis. In sections 7—9 Fig 4G—I, the rostral hippocampus appears. The PCA is defined as in level 6.
In section 11, the opening of the hippocampal fissure hf marks the last image to be quantified. HC indicates hippocampus; cs, colateral sulcus ; Sub, subiculum. Scale bar equals 10 mm all panels.
The cortical amygdala is the most caudal segment of the olfactory allocortex, located on the medial surface of the human temporal lobe It is composed of several superficial amygdaloid nuclei with defined cytoarchitectonic, chemoarchitectonic, and connectional characteristics for nomenclature, see [ 57 ].
The present volumetric analysis included the cortical nuclei of the amygdala cortical amygdala, for short, composed of the anterior cortical nucleus, the medial nucleus, the nucleus of the lateral olfactory tract, olfactory amygdala [ 63 ] , the periamygdaloid cortex PAC 0 , PAC 1 , PAC 2 , PAC 3 , and PAC S subfields, and the posterior cortical nucleus Fig 1.
It extends down to the ventral bank of the sulcus semiannularis ssa where it borders the entorhinal cortex Fig 1B—C. At caudal levels it becomes continuous with the amygdalo-hippocampal transitional area Fig 1D. Rostrally, the cortical amygdala including the PACo appears at the level of the beginning of the amygdala approximately 6 mm caudal to the LI 64 Figs 1B and 5.
One section caudally, where the amygdaloid complex is larger Fig 5 and often the temporal horn of the lateral ventricle is present, the cortical amygdala including the anterior cortical nucleus, nucleus of the lateral olfactory tract, PAC3, and PACs extends as far as the border with the rostromedial portion of the entorhinal cortex at the fundus of the sulcus semiannularis In cases, where the sulcus semiannularis is not apparent, the border defined by the line extending medially from the white matter to the surface of the brain was used as the ventral border of the cortical amygdala Fig 5 At the beginning of the subiculum at the head of the hippocampus 64 , the cortical amygdala medial nucleus, posterior cortical nucleus, PACs becomes continuous with the amygdalo-hippocampal transitional area AHA Fig 1D.
This transitional area between the hippocampus and the amygdala 65 continues caudally the gyrus semilunaris, approximately at the level of the diverticulum unci The caudal end of the cortical amygdala comes into close contact with the amygdalo-hippocampal transitional area AHA, which establishes the link between the rostral extremity of the uncal hippocampal allocortex and the caudal end of the olfactory amygdala.
Due to the lack of any apparent landmarks to separate the AHA from the cortical amygdala, it was included in the volumetric measurement. The amygdalo-hippocampal area becomes apparent at the caudal part of the gyrus uncinatus, rostral to the hippocampal fissure Fig 1D.
The caudal limit of the AHA was coincident with the beginning of the hippocampal fissure in most of the cases. The PCA was outlined from the rostral to caudal direction, according to the MR imaging step-by-step protocol defined below.
Before PCA measurements in TLE patients, ten randomly assigned control subjects were selected for intra - and interobserver tests to assure the reproducibility of the protocol. Measurements of TLE subjects were performed by a single investigator P.
In cases where the cortical boundaries were not clear, a second opinion T. The localization of the PCA region in the medial temporal lobe is presented in coronal MR images in Figures 3 and 4 and schematically in corresponding line-drawings in Figure 5.
At this level, the PCA is composed of the PC, which was not identifiable in terms of different contrast. At this level, the entire cortex from the fundus of the endorhinal sulcus to the most medial point of the gyrus semilunaris on the medial temporal cortex was included into the PCA.
If the sulcus semiannularis was already present, the fundus of the sulcus was considered to be the ventral limit of the PCA. The entire thickness of the cortex was included in the PCA.
On the next 2. Starting approximately 12 mm from the LI, the amygdala is at its largest and the temporal horn of the lateral ventricle appears ventrolateral to the amygdala Figs 3C, 4G and 5. At this level, the sulcus semiannularis is near its end, and it may be either absent or show a shallow appearance on MR images.
If the sulcus semiannularis is visible, the PCA extends from the fundus of the endorhinal sulcus to the fundus of the sulcus semiannularis. In the cases were the sulcus semiannularis cannot be identified, the approximate ventral limit of PCA was determined by the intersection of the line extending from the white matter under the amygdala medial extension of the external capsule to the surface of the brain, as defined previously 50 for the entorhinal cortex.
The entire thickness of the cortex was included into the PCA. In more caudal sections where the rostral end of the hippocampus uncus appears Figs 3D, 4H—I, and 5 , the PCA is defined accordingly.
At the caudal end of the amygdala Figs 3E, 4J—K and 5 , the gyrus ambiens, including the medial intermediate subfield of the entorhinal cortex, is replaced by the amygdalo-hippocampal area and the uncus, which is composed of the subiculum and the CA1 subfield 64 , At this level, the endorhinal sulcus becomes very narrow and locates in close proximity to the optic tract.
The last section, in which the PCA was present, was usually coincident with the opening of the hippocampal fissure Figs 3F, 4K and 5. The outlines of the PCA were drawn as in Step 5. Once the PCA cortices were outlined on each of the coronal images, the final volume was calculated by using a program developed in-house for a standard work console.
As it is generally accepted that interindividual variability in head size affects the volumes of brain regions, we corrected the PCA volume to the individual brain area obtained at the level of the anterior commissure, according to Cendes et al 67 with modifications Briefly, we used the formula: Ten randomly assigned control subjects were selected for intra - and interobserver tests, by using the method introduced by Bland and Altman Repeated measurements were performed for 10 control subjects.
The mean difference in volume was near zero and thus, not considered significant. Scatter plots show the intra - and inter-observer variability of repeated measurements in the assessment of the right and left volume of the PCA of 10 control subjects.
A, shows intra-observer measurement P. The limits of agreement between the first and second measurements are expressed as the mean difference in volume: Inserts in the lower left corner show the association between the first x-axis and second y-axis.
For statistical analysis, the patients were divided into two groups according to localization of the seizure focus: Because the initial statistical survey indicated that the parameters studied were not normally distributed and the number of subjects in each study group was small, nonparametric analyses were used.
Differences between the study groups were determined by using the Mann-Whitney test with the Bonferroni adjustment x 3 for multiple comparisons. To assess the degree of volume asymmetry, the PCA asymmetry ratio was calculated according to Bernasconi et al Subsequently, patients were divided accordingly to their measured hippocampal volumes HCvol in HS patients, if the volume was less than two SD from the control mean and without HS if HCvol was at least two SD from the control mean.
A P value of less than. Figure 7 is the plot of the volume estimation for the PCA areas in the seven hemispheres quantified. In addition, the contribution of the point counting to the overall coefficient of error was approximately half of the contribution of the variability between sections.
Values obtained were smaller compared with MR imaging determinations. Plot of the individual volume estimation of the PCA, obtained by the stereological assessment of seven brain hemispheres see Materials and Methods section for details.
Each square represents a case. The mean normalized volumes and the asymmetry ratios of the PCA volumes in control subjects are shown in Table 2. There was no significant right—left asymmetry in the mean volumes. There was no sex difference in the PCA volumes.
Also, there was no correlation between PCA volume and age. Normalized volumes and asymmetry ratio of the right and left piriform-cortical amygdala in control subjects and patients groups and subgroups.
The sex distribution and mean age did not differ between control subjects and patients with TLE. When control subjects and patients with right or left TLE were compared, there were differences in the mean PCA volumes between groups.
The mean contralateral PCA volume did not differ from that in control subjects Table 2. The mean right PCA did not differ from that in control subjects. We assessed whether the volume reduction within the PCA is associated with hippocampal, amygdaloid, or entorhinal atrophy Table 1.
Scatter plots show the correlation between the ipsilateral and contralateral volumes of the PCA and the volumes of the hippocampus A, amygdala B, and entorhinal cortex C in patients with TLE. PCA volumes correlated with the atrophy in the hippocampus, amygdala, and entorhinal cortex.
Closed circles refer to the ipsilateral values and open circles to the contralateral values. There were no patients with an entorhinal cortex volume reduction of less than two SDs from the mean of the control subjects The volume of the ipsilateral or contralateral PCA did not correlate with the lifetime seizure number.
In the present study, we developed a method to measure the volume of the PCA in coronal MR images of the human brain. This method allowed us to assess the occurrence and severity of PCA atrophy in patients with TLE and its co-occurrence with volume reduction in the hippocampus, amygdala, or entorhinal cortex.
Only patients with an unknown etiology for TLE were included in the study. After establishing the adequate methodological considerations, the study revealed four major findings. First, there was no hemispheric asymmetry of the PCA in control subjects.
Also, the volume did not vary depending on the sex or age of the subjects. Fourth, there was no association between the PCA volumes and lifetime seizure number. The purpose of this study was to investigate the occurrence of damage in the PC and the cortical amygdala in patients with TLE by means of quantitative MR imaging.
Based on histologic analysis, we have elaborated a protocol that can be used to measure the volume of the human PCA in 2. Our MR protocol was designed based on anatomic landmarks derived from the analysis of histologic sections from postmortem brains of healthy subjects.
Thus, we were able to locate the different segments of the PCA and extrapolate the findings to determine the boundaries on MR images. The major difficulty was in determining the thickness of the piriform cortex.
This cortical area appears embedded in the endorhinal sulcus on the first three MR images, starting at the LI, and there are no clear reference points to delineate this region on MR images. Therefore, we used the thickness of the neighboring perirhinal cortex as a reference.
Consequently, it is possible that atrophy of the perirhinal cortex can bias the estimation of the volume of the PCA. Also, volume reduction of the perirhinal cortex is relatively uncommon, even in patients with intractable epilepsy 8 , 10 , Therefore, we concluded that the use of the perirhinal cortex to define the thickness of the piriform component of the PCA does not significantly affect the data evaluation.
The thickness and orientation of the MR images was set according to identical thickness and orientation of the histologic sections, facilitating in this way the identification of the boundaries and minimizing partial volume effects.
Even so, partial voluming is an inherent property of the discretized image and would still persist if the contrast between tissues were maximal or if the thickness was sub-milimetric. Therefore, it is advisable to employ identical section thickness to use the minimum number of MR partitions to estimate the volumes Except for the hippocampus and amygdala, focal atrophies of the para-hippocampal cortices are virtually indiscernible with current cross-sectional high-resolution imaging.
Similarly, PCA atrophies can only be detected quantitatively. It is possible, however, that MR imaging performed at higher fields than 1. Still, we were unable to confirm our data histologically.
Indeed, to date there exists no gold standard consisting of MR imaging and histologic analysis of the same TLE cases. Future post-surgical or autopsy-based studies are needed to substantiate our data and to definitively establish the role that the human PC and cortical amygdala have as critical areas in epileptogenesis.
The results indicate a high concordance between PCA atrophies on one hand, and the EEG findings and the hippocampal atrophies, on the other. These data suggest that a reduced PCA volume or abnormal asymmetry index can be a useful addition to the tools currently used to determine the side of the seizure focus.
Volumetric MR imaging measurements of the amygdala 7 , 67 , entorhinal 54 , 70 , perirhinal 10 and parahippocampal 71 cortices, thalamus, lenticular and caudate nuclei 78 , fornix, and mammillary bodies 79 , 80 support the concept that tissue damage in TLE is not limited to the hippocampus, but involves other associated limbic structures.
These data are consistent with previous data suggesting that structural atrophy secondary to cell loss often extends outside the hippocampus. Furthermore, in the absence of clearly identifiable HS in TLE, extra-hippocampal damage, including that in the PCA, can be part of the epileptogenic zone responsible for the symptomatic findings.
Whether the damage in these various brain areas occurs at the same time or develops in parallel or sequentially later during the epileptogenic process 6 remains to be studied, along with the relative sensitivity, specificity and predictive value of the various quantitative MR imaging protocols that we have at our disposal to characterize the overall brain damage induced by TLE.
Atrophy of the PCA occurs in a subgroup of patients with TLE and the severity of the volume reduction correlates with hippocampal atrophy. These data demonstrate that the PCA is one component of the damaged temporal lobe network in humans.
Furthermore, volumetric assessment of the PCA provides additional information to determine the lateralization of seizure focus. We thank Professor Fernando Lopes da Silva for his constructive comments on the final version of this article.
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Skip to main content. American Journal of Neuroradiology February, 26 2 ;. The study includes the estimation of the contribution of the point counting to the precision of the Cavalieri estimate of volume of the PCA according to the following equation, Thus, the contribution to the overall CE due to the variation between section areas of the PCA can be predicted from the equation, where subscript s and t means section and total respectively.
View inline View popup. Definition of the PC and Cortical Amygdala Borders in Histologic Sections The histologic appearance and location of the PC area 51 of Brodmann [ 56 ] , the cortical amygdaloid nuclei including the anterior cortical nucleus, medial nucleus, and periamygdaloid cortex, as well as the amygdalo-hippocampal area are shown in Figure 1 for nomenclature of the human amygdala, see [ 57 ].
Step 4 On the next 2. Step 5 Starting approximately 12 mm from the LI, the amygdala is at its largest and the temporal horn of the lateral ventricle appears ventrolateral to the amygdala Figs 3C, 4G and 5.
Atlas of the human brain, 3rd edition. Coronal Atlas — Plate 8 anterior view. Cameron; Rommelfanger, Karen S. Epithelium glands mucosa Sustentacular cell Tufted cell. Anatomy of the cerebral cortex of the human brain. Superior frontal gyrus 4 6 8 Middle frontal gyrus 9 10 46 Inferior frontal gyrus: Precentral gyrus Precentral sulcus.
Paracentral lobule 4 Paracentral sulcus. Primary motor cortex 4 Premotor cortex 6 Supplementary motor area 6 Supplementary eye field 6 Frontal eye fields 8. Superior parietal lobule 5 7 Inferior parietal lobule 40 - Supramarginal gyrus 39 - Angular gyrus Parietal operculum 43 Intraparietal sulcus.
Paracentral lobule 1 2 3 5 Precuneus 7 Marginal sulcus. Occipital pole of cerebrum Lateral occipital gyrus 18 19 Lunate sulcus Transverse occipital sulcus. Visual cortex 17 Cuneus Lingual gyrus Calcarine sulcus. Fusiform gyrus 37 Medial temporal lobe 27 28 34 35 36 Inferior temporal gyrus 20 Inferior temporal sulcus.
Subgenual area 25 Anterior cingulate 24 32 33 Posterior cingulate 23 31 Isthmus of cingulate gyrus: Retrosplenial cortex 26 29 Hippocampal sulcus Fimbria of hippocampus Dentate gyrus Rhinal sulcus. Lighter projections to the posterior piriform cortex originated in the dorsolateral division of the lateral nucleus, the magnocellular and parvicellular divisions of the basal and accessory basal nuclei, and the anterior cortical nucleus.
The projections to the anterior piriform cortex were light and originated in the dorsolateral and medial divisions of the lateral nucleus, the magnocellular division of the basal and accessory basal nuclei, the anterior and posterior cortical nuclei, and the periamygdaloid subfield of the periamygdaloid cortex.
The results indicate that only selective amygdaloid nuclei or their subdivisions project to the piriform cortex. In addition, substantial projections from several amygdaloid nuclei converge in the medial aspect of the posterior piriform cortex.
Via these projections, the amygdaloid complex can modulate the processing of olfactory information in the piriform cortex. In pathologic conditions such as epilepsy, these connections might provide pathways for the spread of seizure activity from the amygdala to extra-amygdaloid regions.
Under these conditions, exposure to the small volume of alcohol may have provided sufficient olfactory stimulation to increase pCaMKIIT IR in the piriform directly or through odor-based memory processing. Cue-induced reinstatement of alcohol-seeking behavior is associated with increased CaMKII T phosphorylation in the reward pathway of mice.
In addition, the CxA receives more projections from the rostral or prepiriform area, Haberly and Price, a, b than from the caudal Pir, whereas it projects more strongly to the caudal Pir innervating mainly layers I and III.
In agreement with this observation, the posterior Pir presents more bidirectional connections with the amygdala than the anterior Pir Haberly, ; Majak et al. Therefore, the connectivity of the CxA suggests that it is a transition area between the Pir and the amygdala, and it does not clearly belong to either the layer Ib system or the layer II system as defined by Haberly and Price a, b.
Further characterization of this pathway, including plasticity is ongoing. Finally, the results emphasize that understanding odor processing in the PCX must not only take into account the spatiotemporal patterns of OB input, it must also take into account the context of inputs from regions such orbitofrontal cortex Illig, ; Cohen et al.
PCX connectivity with this broader context is both state - Kay and Freeman, ; Wilson and Yan, and experience-dependent Cohen et al. Discover more publications, questions and projects in Cortex.
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As the piriform/amygdala is a critical circuit for Canadian Journal of Physiology and Canadian Journal of Physiology and Pharmacology, MR Volumetric Analysis of The Piriform Cortex and Cortical Amygdala in Drug-Refractory Temporal Lobe Epilepsy. The amygdala, hippocampus, piriform cortex, Complex view on poisoning with nerve agents and organophosphates. Journal of Neuroinflammation. ISSN:
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