Cingulate cortex

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Cingulate cortex
Gray727 cingulate gyrus.png
Medial surface of left cerebral hemisphere, with cingulate gyrus and cingulate sulcus highlighted.
Details
Part of Cerebral cortex
Artery Anterior cerebral
Vein Superior sagittal sinus
Identifiers
Latin cortex cingularis, gyrus cinguli
Acronym(s)Cg
MeSH D006179
NeuroNames 159
NeuroLex ID birnlex_798
TA98 A14.1.09.231
TA2 5513
FMA 62434
Anatomical terms of neuroanatomy
Sagittal MRI slice with highlighting indicating location of the cingulate cortex. MRI cingulate cortex.png
Sagittal MRI slice with highlighting indicating location of the cingulate cortex.
Coronal section of brain. Cingulate cortex is shown in yellow. Gray743 cingulate gyrus.png
Coronal section of brain. Cingulate cortex is shown in yellow.

The cingulate cortex is a part of the brain situated in the medial aspect of the cerebral cortex. The cingulate cortex includes the entire cingulate gyrus, which lies immediately above the corpus callosum, and the continuation of this in the cingulate sulcus. The cingulate cortex is usually considered part of the limbic lobe.

Contents

It receives inputs from the thalamus and the neocortex, and projects to the entorhinal cortex via the cingulum. It is an integral part of the limbic system, which is involved with emotion formation and processing, [1] learning, [2] and memory. [3] [4] The combination of these three functions makes the cingulate gyrus highly influential in linking motivational outcomes to behavior (e.g. a certain action induced a positive emotional response, which results in learning). [5] This role makes the cingulate cortex highly important in disorders such as depression [6] and schizophrenia. [7] It also plays a role in executive function and respiratory control.

Brodmann areas of a medial section of the right hemisphere. Gray727-Brodman.png
Brodmann areas of a medial section of the right hemisphere.

Etymology

The term cingulate is derived from the Latin cingulātus (meaning "girdled"). [8]

Structure

Based on cerebral cytoarchitectonics it has been divided into the Brodmann areas 23, 24, 26, 29, 30, 31, 32 and 33. The areas 26, 29 and 30 are usually referred to as the retrosplenial areas.

Micrograph showing spindle neurons of the cingulate cortex. HE-LFB stain. Spindle neurons - very high mag.jpg
Micrograph showing spindle neurons of the cingulate cortex. HE-LFB stain.

Anterior cingulate cortex

This corresponds to areas 24, 32 and 33 of Brodmann and LA of Constantin von Economo and Bailey and von Bonin. It is continued anteriorly by the subgenual area (Brodmann area 25), located below the genu of the corpus callosum). It is cytoarchitectonically agranular. It has a gyral and a sulcal part. Anterior cingulate cortex can further be divided in the perigenual anterior cingulate cortex (near the genu) and midcingulate cortex. The anterior cingulate cortex receives primarily its afferent axons from the intralaminar and midline thalamic nuclei (see thalamus). The nucleus anterior receives mamillo-thalamic afferences. The mamillary neurons receive axons from the subiculum. The whole forms a neural circuit in the limbic system known as the Papez circuit. [9] The anterior cingulate cortex sends axons to the anterior nucleus and through the cingulum to other Broca's limbic areas. The ACC is involved in error and conflict detection processes.

Posterior cingulate cortex

This corresponds to areas 23 and 31 of Brodmann LP of von Economo and Bailey and von Bonin. Its cellular structure is granular. It is followed posteriorly by the retrosplenial cortex (area 29).[ citation needed ] Dorsally is the granular area 31. The posterior cingulate cortex receives a great part of its afferent axons from the superficial nucleus (or nucleus superior- falsely LD-[ citation needed ]) of the thalamus (see thalamus), which itself receives axons from the subiculum. To some extent it thus duplicates Papez' circuit. It receives also direct afferents from the subiculum of the hippocampus. Posterior cingulate cortex hypometabolism (with 18F-FDG PET) has been defined in Alzheimer's disease.

Inputs of the anterior cingulate gyrus

A retrograde tracing experiment on macaque monkeys revealed that the ventral anterior nucleus (VA) and the ventral lateral nucleus (VL) of the thalamus are connected with motor areas of the cingulate sulcus. [10] The retrosplenial region (Brodmann's area 26, 29 and 30) of cingulate gyrus can be divided into three parts: i.e., retrosplenial granular cortex A, retrosplenial granular cortex B and retrosplenial dysgranular cortex. The hippocampal formation sends dense projections to retrosplenial granular cortex A and B and fewer projections to the retrosplenial dysgranular cortex. The postsubiculum sends projections to retrosplenial granular cortex A and B and to the retrosplenial dysgranular cortex. The dorsal subiculum sends projections to retrosplenial granular cortex B, while ventral subiculum sends projections to retrosplenial granular cortex A. Entorhinal cortex – caudal parts – sends projections to the retrosplenial dysgranular cortex. [11]

Outputs of the anterior cingulate gyrus

The rostral cingulate gyrus (Brodmanns's area 32) projects to the rostral superior temporal gyrus, midorbitofrontal cortex and lateral prefrontal cortex. [12] The ventral anterior cingulate (Brodmann's area 24) sends projections to the anterior insular cortex, premotor cortex (Brodmann's area 6), Brodmann's area 8, the perirhinal area, the orbitofrontal cortex (Brodmann's area 12), the laterobasal nucleus of amygdala, and the rostral part of the inferior parietal lobule. [12] Injecting wheat germ agglutinin and horseradish peroxidase conjugate into the anterior cingulate gyrus of cats, revealed that the anterior cingulate gyrus has reciprocal connections with the rostral part of the thalamic posterior lateral nucleus and rostral end of the pulvinar. [13] The postsubiculum receives projections from the retrosplenial dysgranular cortex and the retrosplenial granular cortex A and B. The parasubiculum receives projections from the retrosplenial dysgranular cortex and retrosplenial granular cortex A. Caudal and lateral parts of the entorhinal cortex get projections from the retrosplenial dysgranular cortex, while the caudal medial entorhinal cortex receives projections from the retrosplenial granular cortex A. The retrosplenial dysgranular cortex sends projections to the perirhinal cortex. The retrosplenial granular cortex A sends projection to the rostral presubiculum. [11]

Outputs of the posterior cingulate gyrus

The posterior cingulate cortex (Brodmann's area 23) sends projections to dorsolateral prefrontal cortex (Brodmann's area 9), anterior prefrontal cortex (Brodmann's area 10), orbitofrontal cortex (Brodmanns’ area 11), the parahippocampal gyrus, posterior part of the inferior parietal lobule, the presubiculum, the superior temporal sulcus and the retrosplenial region. [12] The retrosplenial cortex and caudal part of the cingulate cortex are connected with rostral prefrontal cortex via cingulate fascicule in macaque monkeys [14] Ventral posterior cingulate cortex was found to be reciprocally connected with the caudal part of the posterior parietal lobe in rhesus monkeys. [15] Also the medial posterior parietal cortex is connected with posterior ventral bank of the cingulate sulcus. [15]

Other connections

The anterior cingulate is connected to the posterior cingulate at least in rabbits. Posterior cingulate gyrus is connected with retrosplenial cortex and this connection is part of the dorsal splenium of the corpus callosum. The anterior and posterior cingulate gyrus and retrosplenial cortex send projections to subiculum and presubiculum. [16]

Clinical significance in schizophrenia

Using a three-dimensional magnetic resonance imaging procedure to measure the volume of the rostral anterior cingulate gyrus (perigenual cingulate gyrus), Takahashi et al. (2003) found that the rostral anterior cingulate gyrus is larger in control (healthy) females than males, but this sex difference was not found in people with schizophrenia. People with schizophrenia also had a smaller volume of perigenual cingulate gyrus than control subjects. [17]

Haznedar et al. (2004) studied metabolic rate of glucose in anterior and posterior cingulate gyrus in people with schizophrenia, schizotypal personality disorder (SPD) and compared them with a control group. The metabolic rate of glucose was found to be lower in the left anterior cingulate gyrus and the right posterior cingulate gyrus in people with schizophrenia relative to controls. Although people with SPD were expected to show a glucose metabolic rate somewhere between the individual with schizophrenia and controls, they actually had higher metabolic glucose rate in the left posterior cingulate gyrus. The volume of the left anterior cingulate gyrus was reduced in people with schizophrenia as compared with controls, but there was not any difference between people with SPD and people with schizophrenia. From these results it appears that the schizophrenia and SPD are two different disorders. [18]

A study of the volume of the gray and white matter in the anterior cingulate gyrus in people with schizophrenia and their healthy first and second degree relatives revealed no significant difference in the volume of the white matter in the people with schizophrenia and their healthy relatives. Nonetheless a significant difference in the volume of gray matter was detected, people with schizophrenia had smaller volume of gray matter than their second degree relatives, but not relative to their first degree relatives. Both the person with schizophrenia and their first degree healthy relatives have smaller gray matter volume than the second degree healthy relatives. It appears that genes are responsible for the decreased volume of gray matter in people with schizophrenia. [19]

Fujiwara et al. (2007) did an experiment in which they correlated the size of anterior cingulate gyrus in people with schizophrenia with their functioning on social cognition, psychopathology and emotions with control group. The smaller the size of anterior cingulate gyrus, the lower was the level of social functioning and the higher was the psychopathology in the people with schizophrenia. The anterior cingulate gyrus was found to be bilaterally smaller in people with schizophrenia as compared with control group. No difference in IQ tests and basic visuoperceptual ability with facial stimuli was found between people with schizophrenia and the control. [20]

Summary

People with schizophrenia have differences in the anterior cingulate gyrus when compared with controls. The anterior cingulate gyrus was found to be smaller in people with schizophrenia. [20] The volume of the gray matter in the anterior cingulate gyrus was found to be lower in people with schizophrenia. [18] [19] Healthy females have larger rostral anterior cingulate gyrus than males, this sex difference in size is absent in people with schizophrenia. [17] The metabolic rate of glucose was lower in the left anterior cingulate gyrus and in the right posterior cingulate gyrus. [18]

In addition to changes in the cingulate cortex more brain structures show changes in people with schizophrenia as compared to controls. The hippocampus in people with schizophrenia was found to be smaller in size when compared with controls of the same age group, [21] and, similarly, the caudate and putamen were found to be smaller in volume in a longitudinal study of people with schizophrenia. [22] While the volume of gray matter is smaller, the size of the lateral and third ventricles is larger in people with schizophrenia. [23]

History

Cingulum means "belt" in Latin. The name was likely chosen because this cortex, in great part, surrounds the corpus callosum. The cingulate cortex is a part of the "grand lobe limbique" of Broca (1878) that consisted of a superior cingulate part (supracallosal) and an inferior hippocampic part (infracallosal). [24] The limbic lobe was separated from the remainder of the cortex by Broca for two reasons: first because it is not convoluted, and second because the gyri are directed parasagittally (contrary to the transverse gyrification). Since the parasagittal gyrification is observed in non-primate species, the limbic lobe was thus declared to be "bestial". As with other parts of the cortex, there have been and continue to be discrepancies concerning boundaries and naming. Brodmann (1909) further distinguished Areas 24 (anterior cingulate) and 23 (posterior) based on granularity. More recently, it was included as a part of the limbic lobe in the Terminologia Anatomica (1998) [25] following von Economo's (1925) system. [26]

Additional images

Related Research Articles

<span class="mw-page-title-main">Brodmann area</span> Region of the brain

A Brodmann area is a region of the cerebral cortex, in the human or other primate brain, defined by its cytoarchitecture, or histological structure and organization of cells. The concept was first introduced by the German anatomist Korbinian Brodmann in the early 20th century. Brodmann mapped the human brain based on the varied cellular structure across the cortex and identified 52 distinct regions, which he numbered 1 to 52. These regions, or Brodmann areas, correspond with diverse functions including sensation, motor control, and cognition.

<span class="mw-page-title-main">Brodmann area 23</span>

Brodmann area 23 (BA23) is a region in the brain that lies inside the posterior cingulate cortex. It lies between Brodmann area 30 and Brodmann area 31 and is located on the medial wall of the cingulate gyrus between the callosal sulcus and the cingulate sulcus.

<span class="mw-page-title-main">Precuneus</span> Region of the parietal lobe of the brain

In neuroanatomy, the precuneus is the portion of the superior parietal lobule on the medial surface of each brain hemisphere. It is located in front of the cuneus. The precuneus is bounded in front by the marginal branch of the cingulate sulcus, at the rear by the parieto-occipital sulcus, and underneath by the subparietal sulcus. It is involved with episodic memory, visuospatial processing, reflections upon self, and aspects of consciousness.

<span class="mw-page-title-main">Brodmann area 10</span> Brain area

Brodmann area 10 is the anterior-most portion of the prefrontal cortex in the human brain. BA10 was originally defined broadly in terms of its cytoarchitectonic traits as they were observed in the brains of cadavers, but because modern functional imaging cannot precisely identify these boundaries, the terms anterior prefrontal cortex, rostral prefrontal cortex and frontopolar prefrontal cortex are used to refer to the area in the most anterior part of the frontal cortex that approximately covers BA10—simply to emphasize the fact that BA10 does not include all parts of the prefrontal cortex.

<span class="mw-page-title-main">Internal capsule</span> White matter structure situated in the inferomedial part of each cerebral hemisphere of the brain

The internal capsule is a white matter structure situated in the inferomedial part of each cerebral hemisphere of the brain. It carries information past the basal ganglia, separating the caudate nucleus and the thalamus from the putamen and the globus pallidus. The internal capsule contains both ascending and descending axons, going to and coming from the cerebral cortex. It also separates the caudate nucleus and the putamen in the dorsal striatum, a brain region involved in motor and reward pathways.

<span class="mw-page-title-main">Primary somatosensory cortex</span> Region of the brain which processes touch

In neuroanatomy, the primary somatosensory cortex is located in the postcentral gyrus of the brain's parietal lobe, and is part of the somatosensory system. It was initially defined from surface stimulation studies of Wilder Penfield, and parallel surface potential studies of Bard, Woolsey, and Marshall. Although initially defined to be roughly the same as Brodmann areas 3, 1 and 2, more recent work by Kaas has suggested that for homogeny with other sensory fields only area 3 should be referred to as "primary somatosensory cortex", as it receives the bulk of the thalamocortical projections from the sensory input fields.

<span class="mw-page-title-main">Lobes of the brain</span> Parts of the cerebrum

The lobes of the brain are the major identifiable zones of the human cerebral cortex, and they comprise the surface of each hemisphere of the cerebrum. The two hemispheres are roughly symmetrical in structure, and are connected by the corpus callosum. They traditionally have been divided into four lobes, but are today considered as having six lobes each. The lobes are large areas that are anatomically distinguishable, and are also functionally distinct to some degree. Each lobe of the brain has numerous ridges, or gyri, and furrows, the sulci that constitute further subzones of the cortex. The expression "lobes of the brain" usually refers only to those of the cerebrum, not to the distinct areas of the cerebellum.

<span class="mw-page-title-main">Brodmann area 24</span> Brain area

Brodmann area 24 is part of the anterior cingulate in the human brain.

<span class="mw-page-title-main">Brodmann area 32</span> Brain area

The Brodmann area 32, also known in the human brain as the dorsal anterior cingulate area 32, refers to a subdivision of the cytoarchitecturally defined cingulate cortex. In the human it forms an outer arc around the anterior cingulate gyrus. The cingulate sulcus defines approximately its inner boundary and the superior rostral sulcus (H) its ventral boundary; rostrally it extends almost to the margin of the frontal lobe. Cytoarchitecturally it is bounded internally by the ventral anterior cingulate area 24, externally by medial margins of the agranular frontal area 6, intermediate frontal area 8, granular frontal area 9, frontopolar area 10, and prefrontal area 11-1909. (Brodmann19-09).

<span class="mw-page-title-main">Brodmann area 13</span> Brain area

Area 13 is part of the Orbitofrontal cortex, a subdivision of the cerebral cortex as defined by cytoarchitecture.

<span class="mw-page-title-main">Brodmann area 30</span>

Brodmann area 30, also known as agranular retrolimbic area 30, is a subdivision of the cytoarchitecturally defined retrosplenial region of the cerebral cortex. In the human it is located in the isthmus of cingulate gyrus. Cytoarchitecturally it is bounded internally by the granular retrolimbic area 29, dorsally by the ventral posterior cingulate area 23 and ventrolaterally by the ectorhinal area 36 (Brodmann-1909).

The zona incerta (ZI) is a horizontally elongated region of gray matter in the subthalamus below the thalamus. Its connections project extensively over the brain from the cerebral cortex down into the spinal cord.

<span class="mw-page-title-main">Posterior cingulate cortex</span> Caudal part of the cingulate cortex of the brain

The posterior cingulate cortex (PCC) is the caudal part of the cingulate cortex, located posterior to the anterior cingulate cortex. This is the upper part of the "limbic lobe". The cingulate cortex is made up of an area around the midline of the brain. Surrounding areas include the retrosplenial cortex and the precuneus.

The amygdalofugal pathway is one of the three major efferent pathways of the amygdala, meaning that it is one of the three principal pathways by which fibers leave the amygdala. It leads from the basolateral nucleus and central nucleus of the amygdala. The amygdala is a limbic structure in the medial temporal lobe of the brain. The other main efferent pathways from the amygdala are the stria terminalis and anterior commissure.

The perirhinal cortex is a cortical region in the medial temporal lobe that is made up of Brodmann areas 35 and 36. It receives highly processed sensory information from all sensory regions, and is generally accepted to be an important region for memory. It is bordered caudally by postrhinal cortex or parahippocampal cortex and ventrally and medially by entorhinal cortex.

The isothalamus is a division used by some researchers in describing the thalamus.

<span class="mw-page-title-main">Retrosplenial cortex</span> Part of the brains cerebral cortex

The retrosplenial cortex (RSC) is a cortical area in the brain comprising Brodmann areas 29 and 30. It is secondary association cortex, making connections with numerous other brain regions. The region's name refers to its anatomical location immediately behind the splenium of the corpus callosum in primates, although in rodents it is located more towards the brain surface and is relatively larger. Its function is currently not well understood, but its location close to visual areas and also to the hippocampal spatial/memory system suggest it may have a role in mediating between perceptual and memory functions, particularly in the spatial domain. However, its exact contribution to either space or memory processing has been hard to pin down.

The trisynaptic circuit or trisynaptic loop is a relay of synaptic transmission in the hippocampus. The circuit was initially described by the neuroanatomist Santiago Ramon y Cajal, in the early twentieth century, using the Golgi staining method. After the discovery of the trisynaptic circuit, a series of research has been conducted to determine the mechanisms driving this circuit. Today, research is focused on how this loop interacts with other parts of the brain, and how it influences human physiology and behaviour. For example, it has been shown that disruptions within the trisynaptic circuit lead to behavioural changes in rodent and feline models.

<span class="mw-page-title-main">Hippocampus anatomy</span>

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References

  1. ↑ Hadland, K. A.; Rushworth M.F.; et al. (2003). "The effect of cingulate lesions on social behaviour and emotion". Neuropsychologia. 41 (8): 919–931. doi:10.1016/s0028-3932(02)00325-1. PMID   12667528. S2CID   16475051.
  2. ↑ "Cingulate binds learning". Trends Cogn Sci. 1 (1): 2. 1997. doi:10.1016/s1364-6613(97)85002-4. PMID   21223838. S2CID   33697898.
  3. ↑ Kozlovskiy, S.; Vartanov A.; Pyasik M.; Nikonova E.; Velichkovsky B. (10 October 2013). "Anatomical Characteristics of Cingulate Cortex and Neuropsychological Memory Tests Performance". Procedia - Social and Behavioral Sciences. 86: 128–133. doi: 10.1016/j.sbspro.2013.08.537 .
  4. ↑ Kozlovskiy, S.A.; Vartanov A.V.; Nikonova E.Y.; Pyasik M.M.; Velichkovsky B.M. (2012). "The Cingulate Cortex and Human Memory Processes". Psychology in Russia: State of the Art. 5: 231–243. doi: 10.11621/pir.2012.0014 .
  5. ↑ Hayden, B. Y.; Platt, M. L. (2010). "Neurons in Anterior Cingulate Cortex Multiplex Information about Reward and Action". Journal of Neuroscience. 30 (9): 3339–3346. doi:10.1523/JNEUROSCI.4874-09.2010. PMC   2847481 . PMID   20203193.
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  7. ↑ Adams, R.; David, A. S. (2007). "Patterns of anterior cingulate activation in schizophrenia: A selective review". Neuropsychiatric Disease and Treatment. 3 (1): 87–101. doi: 10.2147/nedt.2007.3.1.87 . PMC   2654525 . PMID   19300540.
  8. ↑ "cingulate" . Oxford English Dictionary (Online ed.). Oxford University Press.(Subscription or participating institution membership required.)
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  11. 1 2 Wyass, J. M.; Van Groen, T. (1992). "Connections between the retrosplenial cortex and the hippocampal formation in the rat: A review". Hippocampus. 2 (1): 1–11. doi:10.1002/hipo.450020102. PMID   1308170. S2CID   14385024.
  12. 1 2 3 Pandya, D. N.; Hoesen, G. W.; Mesulam, M. -M. (1981). "Efferent connections of the cingulate gyrus in the rhesus monkey". Experimental Brain Research. 42–42 (3–4): 319–330. doi:10.1007/BF00237497. PMID   6165607. S2CID   12274921.
  13. ↑ Fujii, M. (1983). "Fiber connections between the thalamic posterior lateral nucleus and the cingulate gyrus in the cat". Neuroscience Letters. 39 (2): 137–142. doi:10.1016/0304-3940(83)90066-6. PMID   6688863. S2CID   34795697.
  14. ↑ Petrides, M; Pandya, DN (Oct 24, 2007). "Efferent association pathways from the rostral prefrontal cortex in the macaque monkey". The Journal of Neuroscience. 27 (43): 11573–86. doi:10.1523/JNEUROSCI.2419-07.2007. PMC   6673207 . PMID   17959800.
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  16. ↑ Adey, W. R. (1951). "An Experimental Study of the Hippocampal Connexions of the Cingulate Cortex in the Rabbit". Brain. 74 (2): 233–247. doi: 10.1093/brain/74.2.233 . PMID   14858747.
  17. 1 2 Takahashi, T.; Suzuki, M.; Kawasaki, Y.; Hagino, H.; Yamashita, I.; Nohara, S.; Nakamura, K.; Seto, H.; Kurachi, M. (2003). "Perigenual cingulate gyrus volume in patients with schizophrenia: A magnetic resonance imaging study". Biological Psychiatry. 53 (7): 593–600. doi:10.1016/S0006-3223(02)01483-X. PMID   12679237. S2CID   11482948.
  18. 1 2 3 Haznedar, M. M.; Buchsbaum, M. S.; Hazlett, E. A.; Shihabuddin, L.; New, A.; Siever, L. J. (2004). "Cingulate gyrus volume and metabolism in the schizophrenia spectrum". Schizophrenia Research. 71 (2–3): 249–262. doi:10.1016/j.schres.2004.02.025. PMID   15474896. S2CID   28889346.
  19. 1 2 Costain, G.; Ho, A.; Crawley, A. P.; Mikulis, D. J.; Brzustowicz, L. M.; Chow, E. W. C.; Bassett, A. S. (2010). "Reduced gray matter in the anterior cingulate gyrus in familial schizophrenia: A preliminary report". Schizophrenia Research. 122 (1–3): 81–84. doi:10.1016/j.schres.2010.06.014. PMC   3129334 . PMID   20638248.
  20. 1 2 Fujiwara, H.; Hirao, K.; Namiki, C.; Yamada, M.; Shimizu, M.; Fukuyama, H.; Hayashi, T.; Murai, T. (2007). "Anterior cingulate pathology and social cognition in schizophrenia: A study of gray matter, white matter and sulcal morphometry" (PDF). NeuroImage. 36 (4): 1236–1245. doi:10.1016/j.neuroimage.2007.03.068. hdl: 2433/124279 . PMID   17524666. S2CID   25750603.
  21. ↑ Koolschijn, P. C. D. M. P.; Van Haren, N. E. M.; Cahn, W.; Schnack, H. G.; Janssen, J.; Klumpers, F.; Hulshoff Pol, H. E.; Kahn, R. S. (2010). "Hippocampal Volume Change in Schizophrenia". The Journal of Clinical Psychiatry. 71 (6): 737–744. doi:10.4088/JCP.08m04574yel. PMID   20492835.
  22. ↑ Mitelman, S. A.; Canfield, E. L.; Chu, K. W.; Brickman, A. M.; Shihabuddin, L.; Hazlett, E. A.; Buchsbaum, M. S. (2009). "Poor outcome in chronic schizophrenia is associated with progressive loss of volume of the putamen". Schizophrenia Research. 113 (2–3): 241–245. doi:10.1016/j.schres.2009.06.022. PMC   2763420 . PMID   19616411.
  23. ↑ Kempton, M. J.; Stahl, D.; Williams, S. C. R.; Delisi, L. E. (2010). "Progressive lateral ventricular enlargement in schizophrenia: A meta-analysis of longitudinal MRI studies" (PDF). Schizophrenia Research. 120 (1–3): 54–62. doi:10.1016/j.schres.2010.03.036. PMID   20537866. S2CID   25389387.
  24. ↑ Broca, P (1878). "Anatomie comparee des circonvolutions cerebrales: Le grand lobe limbique et la scissure limbique dans la serie des mammifères". Revue d'Anthropologie. 1: 385–498
  25. ↑ TA A14.1.09.230
  26. ↑ Economo, C., Koskinas, G.N. (1925). Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. Wien: Springer Verlag.
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