Anatomical Characteristics of Cingulate Cortex and ... - Science Direct

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ScienceDirect Procedia - Social and Behavioral Sciences 86 (2013) 128 – 133

V Congress of Russian Psychological Society

Anatomical Characteristics of Cingulate Cortex and Neuropsychological Memory Tests Performance Kozlovskiy Stanislava*, Vartanov Alexandera, Pyasik Mariaa, Nikonova Evgeniaa, Velichkovsky Borisa a

Lomonosov Moscow State University, Moscow, Russia

Abstract The absolute squares of cingulate cortex (anterior, posterior ventral, posterior dorsal, retrosplenial regions) were calculated on magnetic resonance images of 29 subjects (60-76 years old) and compared with subje demonstrate significant correlations between overall performance and the amount of different types of errors in neuropsychological memory tests and the relative size of these regions. The discovered correlations pattern can be explained by a hypothesis of reciprocal functional influence of two major areas of cingulate cortex (anterior and dorsal posterior regions) on the processes of external and internal interference, which results in neuropsychological memory tests performance.

© 2013 The Authors. Published by Elsevier Ltd. Open access under CC BY-NC-ND license. Selection peer-review under responsibility of Russian Psychological Society Society. Selectionand/or and/or peer-review under responsibility of Russian Psychological Keywords: cingulate cortex; magnetic resonance morphometryic analysis; human neuropsychology; memory

1. Introduction The functional role of cingulate cortex is still being discussed despite the large amount of studies and hypotheses. Being a part of Papez circuit, this brain structure receives afferent signals from anterior nuclei of the thalamus while efferent signals from the cingulate cortex are transferred to parahippocampal gyrus and then to hippocampus. Furthermore, cingulate cortex has many bilateral connections with frontal, temporal and occipital cortex of both hemispheres of the brain. It is important to note, that cingulate cortex is very heterogenic. According to cerebral cytoarchitectonics cingulate cortex is divided into 7 Brodmann areas (BA) areas 23, 24, 26, 29, 30, 31. However, due to the difficulty of visual separation of these areas on tomographic images, cingulate cortex is divided into three bigger areas anterior cingulate cortex (BA 24 and 33), posterior cingulate

*

Corresponding author. Tel.:+7-926-230-8623; fax: +7-495-629-6075. E-mail address: [email protected]

1877-0428 © 2013 The Authors. Published by Elsevier Ltd. Open access under CC BY-NC-ND license. Selection and/or peer-review under responsibility of Russian Psychological Society doi:10.1016/j.sbspro.2013.08.537

Kozlovskiy Stanislav et al. / Procedia - Social and Behavioral Sciences 86 (2013) 128 – 133

cortex (BA 23 and 31) and retrosplenial cingulate cortex (BA 26, 29 and 30). In addition, sometimes posterior cingulate cortex is divided into ventral (BA 23) and dorsal (BA 31) parts. Most studies concern anterior cingulate cortex. For example, many studies show that the activity of anterior cingulate cortex increases while subjects solve tasks involving cognitive control (such as error detection, conflict monitoring and/or dual tasks for attention and tests for the executive component of working memory). Clinical records of the lesions of this brain area in humans show that the damage of posterior cingulate cortex results in troubles with solving cognitive control tasks [1-4]. Morphometric analysis studies revealed decreased size of anterior cingulate cortex in subjects with schizophrenia [5]. Far less is known about posterior cingulate cortex. According to PubMed data base, there are almost six times less references of it in published works than of anterior cingulate cortex. It is known, that posterior cingulate cortex activates in healthy humans while retrieving memories from autobiographic episodic memory [6]. However, if information is retrieved from episodic memory but not from autobiographic one, this area of the brain remains inactivated [7]. Also some studies revealed that posterior cingulate cortex activates with recognition of familiar words, objects and places [8], [9]. Published works about functional role of retrosplenial cingulate cortex are even less common. It is known that the damage of this brain region causes serious anterograde amnesia [10], [11]. Other studies show that retrosplenial cingulate cortex is involved in emotional processes, for example, this area activates while subject perceives emotionally significant words [12]. This area of the brain is also involved in spatial navigation; hippocampus and/or parahippocampal gyrus activate in memorizing new routes in three-dimensional space, whereas navigation in familiar places causes activation of retrosplenial cingulate cortex [13], [14]. There is a described case of patient with a hemorrhage in the left retrosplenial area, who lost his ability of spatial orientation but could still solve tasks for spatial thinking [15]. Recent studies of different brain regions involvement in cognitive processes use magnetic resonance morphometric analysis. For example, some studies show that the volume of hippocampus and its subdivisions [16-18] and the sizes of corpus callosum regions [19] correlate with memory processes. Nevertheless, morphometric analysis of cingulate cortex involvement in cognitive processes previously has been used only in clinical studies. This study is the first attempt to use the method of magnetic resonance morphometric analysis in order to reveal the role of the main cingulate cortex subdivisions of both hemispheres in memory processes of healthy subjects of older age. 2. Methods 67.7 5.1 years old) with no previous brain Subjects: 29 right-handed females 60-76 years old (mean age trauma, strokes, psychological or neurological disorders. Procedure: The study consisted of two parts, an MRI study and neuropsychological assessment. During the MRI study all participants were scanned on a 3.0 MRI-scanner; T1 three-dimensional images of the brain were obtained. On sagittal slices of the images (standardized in each direction) we highlighted areas, which included cingulate cortex of both hemispheres. In each hemisphere we divided cingulate cortex into four regions anterior (BA 24, 33), posterior ventral (BA 23), posterior dorsal (BA 31) and retrosplenial (BA 26, 29, 30) areas. We calculated absolute squares of all highlighted cingulate cortex regions surface (in mm2). modified by J.M. Glozman [20], [21] allows quantitative analysis of memory processes. The following tests were used: immediate and delayed recall of 10 words, two groups of words and sentences, semantic coding test (memorizing 12 words by including them in random sentences and recalling them after 10 minutes of heterogenic interference), visual memory tests (recall of simple and complex geometric objects), visuospatial memory tests (copying the geometric figures and their delayed recall), associative memory tests (memorizing pairs of words, recall of the second word after hearing the first one). For each memory type we defined memory capacity (total of recalled elements), permanency (total of delayed recall) and memory errors. We separated several kinds of errors, such as replacement of one element with another one, confabulations (inclusion of new elements),

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contaminations (several elements mixture), perseverations (recalling single element more than once), and sequence errors. Obtained data was statistically analyzed by calculating non-parametric correlations (Spearman correlation coefficient) between individual behavioral and anatomical measurements. Further analysis included only statistically significant correlations (p < 0.05). 3. Results According to the obtained data, cingulate cortex size in both hemispheres does not correlate significantly with ficant correlations between the age and the sizes of different cingulate cortex regions were also found, which can be explained by rather homogeneous sample group. However, which is far more interesting, we discovered significant correlations between cingulate cortex size and neuropsychological tests results. Moreover, these correlations vary in different cingulate cortex areas. Overall results for anterior cingulate cortex (BA 24) of both hemispheres are summarized in Table 1. Table 1. Overall correlations between memory tests results and the size of anterior cingulate cortex. Left hemisphere Right hemisphere Both hemispheres Total of confabulations in semantic coding test Total of confabulations in immediate recall of 10 words Total recall of 10 words Total recall in visual memory test

-0,51 -0,32 -0,37

-0,32 -0,33

Data in Table 1 reveal memory tests results correlation with the size of anterior cingulate cortex. For example, size of left cingulate cortex correlates negatively with the amount of confabulations in semantic coding and word recall tests, thus increasing precision of recall. Furthermore, right anterior cingulate cortex correlates negatively with total amount of verbal and, especially, non-verbal recall, so the bigger the surface of this brain area, the worse the recall of previous stimuli. Visual memory tests results tend to correlate with the size of right anterior cingulate cortex, while semantic coding and digit recall tests correlate with the size of left anterior cingulate cortex. We also discovered significant correlations between neuropsychological tests results and the size of ventral posterior cingulate cortex (BA 23). It is obvious from Tab. 2 that the size of this brain region in right hemisphere correlates negatively with the amount of errors in semantic memory tests. Though, in subjects with relatively big left ventral area frequent sequence errors and perseverations occurred in both verbal and non-verbal tests. Table 2. Overall correlations between memory tests results and the size of ventral posterior cingulate cortex Left hemisphere Right hemisphere Both hemisphere Total of confabulations in semantic coding test Total recall in visual memory test Sequence errors in recall of two groups of words and sentences Sequence errors in visual memory test Sequence errors in digit recall Perseverations errors in recall of two groups of words and sentences Perseverations errors in visual memory test

-0,40 -0,44 0,32 0,41 0,37 0,33

0,41

0,40

Table 3 illustrates neuropsychological memory tests results correlations with the size of posterior dorsal cingulate cortex (BA 31); more correlations were revealed for this brain region than for the other ones. The size of posterior dorsal cingulate cortex correlates negatively with verbal and non-verbal memory capacity; it also increases the influence of interfering factors and the amount of confabulations in word recall tests. Furthermore, it correlates negatively with the amount of sequence errors in visual memory test.

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Table 3. Overall correlations with memory tests results and the size of posterior dorsal cingulate cortex Left hemispere Right hemisphere Both hemisperes Total of confabulations in group recall test Sequence errors in visual memory test Total recall of 10 words (before interfering stimuli) Total recall of 10 words (after interfering stimuli) Total recall of groups of words and sentences Total recall in visual memory test Total recall in visual memory test (after interfering stimuli)

0,44 -0,46 -0,49 -0,39 -0,45 -0,45 -0,41

-0,41 -0,39 -0,41 -0,38

Finally, we revealed few significant correlations between neuropsychological tests results and the size of retrosplenial cingulate cortex (BA 26, 29 and 30). The results for left and right hemispheres are showed in Tab. 4. Table 4. Overall correlations between memory tests results and the size of retrosplenial cingulate cortex. Left hemisphere Right hemisphere Both hemispheres Total of contaminations in groups recall Total recall in visual memory test Total recall in visual memory test (after interfering stimuli)

-0,42 -0,39 -0,38

-0,43 -0,53 -0,45

Results in Table 4 reveal no significant differences in left and right hemispheres. Increased size of this brain region correlates with decrease of contaminations, but also with a severe decrease in the amount of recalled elements in visual memory tests. This decrease remains independent from the influence of interfering stimuli. 4. Discussion and conclusions The results of this study show that the increase of several cingulate cortex regions correlates with decrease in amount of errors in memory tests. However, decrease in amount of errors not only does not improve overall memory performance, but it actually tends to deteriorate total recall. Revealed correlations can be summarized under the idea of an anterioposterior gradient of cortical function development and interhemispheric functional differences [22, 23]. Being evolutionary younger, anterior regions of the cortex correspond less with particularly modal effects and more with semantic information processing, which, in case of this study, results in contamination suppressing. Furthermore, left hemisphere structures reveal more sufficient correlations with verbal tests results in comparison with right hemisphere structures. Thus, there is a negative correlation between the size of anterior cingulate cortex and the amount of confabulations in semantic coding test; this appears to be an important characteristic of prefrontal functions integrity (see [24]). What seems to be rather counterintuitive in such correlation between test results and the size of most cingulate cortex areas can be explained by the fact that cingulate cortex is usually referred to as central controller of cognitive activity, which filters irrelevant information. Dorsal cingulate cortex (BA 31), on the other hand, has controversial qualities, being more correlated with memory tests results than other cingulate cortex areas and being the only area, which correlates positively with the amount of confabulations. We assume that the role of anterior cingulate cortex in memory functioning is filtering irrelevant information in order to protect memory processes from interfering stimuli. In terms of signal-detection theory it can be called filtration and noise suppression system. This explains why overdeveloped anterior cingulate cortex correlates with the decrease of memory errors, such as confabulations, but also with the decrease of overall recall: conservative decisioninformation, thus generating potential signals in the noise. Generally, we suggest, that cingulate cortex consists of

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two basic subsystems, which have reciprocal influence on neuropsychological memory tests performance, and possibly, on other cognitive processes. This explanation corresponds with the results of other studies. If anterior cingulate cortex is a noise suppressing system, it becomes clear why this brain region activates during filtering tasks. It also applies for information recall, because this process also demands filtering and denying some false and uncertain memories, imagination, etc. This explains anterior cingulate cortex activity in information recall from spatial [25], episodic [26], working [27], verbal declarative [28] and emotional [29] memory. Based on our hypothesis of cingulate cortex functions, it can be suggested that confabulations occur while the functioning of this brain region severe confabulations [30]; anterior cingulate cortex atrophy is also discovered in schizophrenics, who suffer from memory errors, such as confabulations [5]. The idea that posterior dorsal cingulate cortex (BA 31) extracts s well. For example, it can explain posterior cingulate cortex activation in recognition of familiar words, objects or places [8, 9]. The present study also revealed a functional transection of anatomically close brain regions. This can be again explained by the gradient principle described above. For example, posterior ventral cingulate cortex (BA 23), being situated on transection of two reciprocal systems, has less expressed properties of either of them. Overdevelopment of this brain region corresponds with the increase in the amount of sequence errors and perseverations, as well as with successful suppression of semantic errors, confabulations and contaminations. It is also important to study the dorsoventral gradient of brain function differences. For anterior cingulate cortex, the specialization of different regions along the dorsoventral gradient may change from information processing under the condition of cognitive conflict to information processing under the condition of affective-emotional conflict. References [1] Botvinick MM, Cohen JD, Carter CS. Conflict monitoring and anterior cingulate cortex: an update. Trends in Cogn. Sci., 2004; 8: 539 46. [2] Kerns JG, Cohen JD, MacDonald AW, Cho RY, Stenger VA, Carter CS. Anterior cingulate conflict monitoring and adjustments in control. Science, 2004; 303:1023 26. [3] Lenartowicz A, McIntosh AR The role of anterior cingulate cortex in working memory is shaped by functional connectivity. J Cogn Neurosci, 2005; 17(7):1026-42. [4] Otsuka Y, Osaka N, Morishita M, Kondo H, Osaka M Decreased activation of anterior cingulate cortex in the working memory of the elderly. Neuroreport, 2006; 17(14):1479-82. [5] Choi JS, Kang DH, Kim JJ, Ha TH, Roh KS, Youn T. Decreased caudal anterior cingulate gyrus volume and positive symptoms in schizophrenia. Psychiatry Res, 2005; 139(3):239-47. [6] Maddock RJ, Garrett AS, Buonocore MH Remembering familiar people: the posterior cingulate cortex and autobiographical memory retrieval. Neuroscience, 2001; 104(3):667-76. [7] Ries ML, Schmitz TW, Kawahara TN, Torgerson BM, Trivedi MA, Johnson SC Task-dependent posterior cingulate activation in mild cognitive impairment. Neuroimage, 2006; 29(2):485-92. [8] Heun R, Freymann K, Erb M, Leube DT, Jessen F, Kircher TT. Successful verbal retrieval in elderly subjects is related to concurrent hippocampal and posterior cingulate activation. Dement Geriatr Cogn Disord, 2006; 22(2):165-72. [9] Sugiura M, Shah NJ, Zilles K, Fink GR Cortical representations of personally familiar objects and places: functional organization of the human posterior cingulate cortex. J Cogn Neurosci, 2005;17(2):183-98. [10] Kim JH, Park KY, Seo SW, Na DL, Chung CS, Lee KH. Reversible verbal and visual memory deficits after left retrosplenial infarction. J Clin Neurol, 2007; 3(1):62-6. [11] Oka Y, Maeshima S, Morita S, Ishida K, Kunimoto K, Yoshida M, et al. A case of amnesia caused by a subcortical hematoma in the left retrosplenial region. No Shinkei Geka, 2003; 31(3):289-95.


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