The prefrontal areas and cerebral hemispheres of the neotropical Cebus apella and their correlations with cognitive processes

Borges, Kellen Christina Malheiros; Ferreira, Jussara Rocha; Caixeta, Leonardo Ferreira

doi:10.1590/S1980-57642010DN40300006

Abstract

The organization of the prefrontal cortex can hold important clues to understanding its functioning. The Cebus apella present cerebral particularities and behavioral and cognitive flexibility, possessing abilities that demonstrate an overlap with those of big primates.

Objectives:

To provide evidence of correlations between anatomical particularities of the brain areas analyzed and some cognitive abilities previously described in these simians.

Methods:

The relative size of the cerebral hemispheres and prefrontal areas (PFA) were measured using a Universal caliper, in 24 hemispheres of C. apella fixed with 10% formaldehyde and kept in 70% alcoholic solution.

Results:

Data gathered allowed the calculation of the approximate volume (cm³⁾ of the areas under study: right antimere 35.2 cm³ (±5.3), left antimere 31.3 cm³ (±5.4) and of the left PFA 6.0 cm³ (±1.5) and right PFA 6.9 cm³ (±1.7).

Conclusions:

We concluded that the PFA represents about 20% of the cerebral volume of this primate. No significant differences were found in the antimeres in terms of volume and area of the hemispheres and likewise for the PFA. These animals have a proportionally bigger brain than that of other neotropical primates in the literature. This allows us to infer that the frontal lobe of C. apella is also larger; possibly related to its maturity and developed cognitive functions indicative of the culture transfers characteristic of this species.

Key words:
Cebus apella; brain; cerebral hemispheres; prefrontal area; cognitive processes

Resumo

A organização do córtex pré-frontal pode conter dados importantes para a compreensão de seu funcionamento. Os Cebus apella apresentam particularidades cerebrais e flexibilidade comportamental e cognitiva, possuindo habilidades que demonstram destacada sobreposição sobre grandes primatas.

Objetivos:

Fornecer subsídios para realização de correlações entre particularidades anatômicas das regiões encefálicas analisadas e algumas habilidades cognitivas já descritas nestes símios.

Métodos:

Analisamos o tamanho relativo dos hemisférios cerebrais e da região pré-frontal (RPF), utilizando paquímetro universal, em 24 hemisférios cerebrais de C. apella fixados em formol a 10% e conservados em solução alcoólica a 70%.

Resultados:

Os dados obtidos permitiram-nos calcular o volume (cm³⁾ aproximado das áreas estudadas: antímero direito 35,2 cm³ (±5,3), antímero esquerdo 31,3 cm³ (±5,4) e das RPF esquerda 6,0 cm³ (±1,5) e a direita 6,9 cm³ (±1,7).

Conclusões:

Concluímos que a RPF representa aproximadamente 20% do volume cerebral deste primata. Não constatamos diferenças significativas nos antímeros em relação aos volumes e às áreas tanto dos hemisférios cerebrais como das RPF. Estes animais apresentaram tamanho cerebral proporcionalmente maior que os demais primatas neotropicais quando comparamos nossos achados com a literatura disponível, permitindo-nos inclusive inferir que há uma grande amplitude do lobo frontal em C. apella; possivelmente relacionada à maturidade e às funções cognitivas elaboradas indicativas de transferência de cultura características deste animal.

Palavras-chave:
Cebus apella; hemisférios cerebrais; região pré-frontal; processos cognitivos

Texto completo disponível apenas em PDF.

Full text available only in PDF format.

References

Barbas H. Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neurosci Biobehav Rev 1995;193:499-510.
Fuster JM. The Prefrontal Cortex: Anatomy, physiology, and neuropsychology of the frontal lobe. Philadelphia: Lippincott-Raven; 1997.
Roberts AC, Wallis JD. Inhibitory control and affective processing in the prefrontal cortex: neuropsychological studies in the common marmoset. Cereb Cortex 2000;10:252-262.
Miller EK, Freedman DJ, Wallis JD. The prefrontal cortex: categories, concepts and cognition. Philos Trans R Soc Lond B Biol Sci 2002;357(1424):1123-1136.
Wood J, Grafman J. Human prefrontal cortex: processing and representational perspectives. Nat Neurosci 2003;4:139-147.
Fuster JM. Memory in the cerebral cortex. Cambridge, MA: MIT Press; 1995.
Fuster JM. Memory systems in the brain. New York: Raven Press; 2000.
Miller EK. The prefrontal cortex and cognitive control. Nat Neurosci 2000;01:59-65.
Semendeferi K, Damasio H, Frank R, Van Hoesen GW. The evolution of the frontal lobes: a volumetric analysis based on three-dimensional reconstructions of magnetic resonance scans of human and ape brains. J Hum Evol 1997;32:375-388.
Dorus S, Vallender EJ, Evans PD, et al. Accelerated evolution of nervous system genes in the origin of Homo sapiens. Cell 2004;119:1027-1040.
Phillips KA. Tool use in wild capuchin monkeys (Cebus albifrons trinitatis). Am J Primatol 1998;46:259-261.
Boinski S. Object manipulation and tool use by brown capuchins in Suriname. Am J Phys Anthropol 2000;109:30.
Jalles-Filho E, da Cunha RGT, Salm RA. Transport of tools and mental representation: is capuchin monkey tool behaviour a useful model of Plio-Pleistocene hominid technology? J Hum Evol 2001;40:365-377.
Cleveland A, Rocca AM, Wendt EL, Westergaard GC. Transport of tools to food sites in tufted capuchin monkeys (Cebus apella). Anim Cog 2004; 7:193-198.
Ottoni EB, Mannu M. Semi-free-ranging tufted capuchin monkeys (Cebus apella) spontaneously use tools to crack open nuts. Int J Primatol 2001;22:347-358.
Resende BD, Ottoni EB. Brincadeira e aprendizagem do uso de ferramentas em macacos-prego (Cebus apella). Est Psicol 2002;7:173-180.
Visalberghi E, Néel C. Tufted capuchins (Cebus apella) use weight and sound to choose between full and empty nuts. Ecol Psychol 2003;15:215-228.
Fragaszy DM, Izar P, Visalberghi E, Ottoni EB, Oliveira MG. Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools. Am J Primatol 2004;64:359-366.
Chevalier-Skolnikoff S. Spontaneous tool use and sensorimotor intelligence in Cebus compared with other monkeys and apes. Behav Brain Sci 1989;12:561-627.
Mendes FDC, Martins LBR, Pereira JA, Marquezan RF. Fishing with a bait: a note on behavioural flexibility in Cebus apella Folia Primatologica; Int J Primatol 2000;71:350-352.
de Waal FBM, Davis JM. Capuchin cognitive ecology: cooperation based on projected returns. Neuropsychologia 2003; 41:221-228.
de Waal FBM, Dindo M, Freeman CA, Hall MJ. The monkey in the mirror: Hardly a stranger. Proc Natl Acad Sci U S A. 2005;102:11140-11147.
Pandya DN, Yeterian EH. Comparison of prefrontal architecture and connections. Philos Trans R Soc Lond B Biol Sci 1996;351(1346):1423-1432.
Barbas H. Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices. Brain Res Bull 2000;52:319-330.
Chiavaras MM, Petrides M. Orbitofrontal sulci of the human and macaque monkey brain. Journal of Comparative Neurology 2000;422:35-54.
Petrides M, Pandya DN. Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur J Neurosci 2002;16:291-310.
Ongur D, Ferry AT, Price JL. Architectonic subdivision of the human orbital and medial prefrontal cortex. J Comp Neurol 2003;460:425-449.
Schoenemann PT, Sheehan MJ, Glotzer LD. Prefrontal white matter volume is disproportionately larger in humans than in other primates. Nat Neurosci 2005;8:242-252.
Barbas H, Pandya DN. Architecture and intrinsic connections of the prefrontal cortex in the Rhesus monkey. J Comp Neurol 1989;286:353-375.
Barbas, H. Architecture and cortical connections of the prefrontal cortex in the rhesus monkey. Adv Neurol 1992;57:91-115.
Romanski LM. Domain specificity in the primate prefrontal cortex. Cog Affec Behav Neurosci 2004;4:421-429.
Roth G, Dicke U. Evolution of the brain and intelligence. Trends Cog Sci 2005; 9:250-257.
Byrne RW, Whiten A. Machiavellian intelligence. In: Whiten A, Byrne RW (eds). Machiavellian intelligence II. Extensions and evaluations. Cambridge, UK: Cambridge Univ Press; 1997:1-23.
Jerison HJ. The evolution of the brain and intelligence. New York: Academic Press; 1973.
Rilling JK, Insel TR. The primate neocortex in comparative perspective using magnetic resonance imaging. J Hum Evol 1999;37:191-223.
Westergaard GC, Gregory C. The subsistence technology of capuchins. Int J Primatol 1994;15:899-906.
Westergaard GC, Gregory C, Suomi SJ. The stone tools of capuchins (Cebus apella). Int J Primatol 1995;16:1017-1024.
de Waal FBM. Attitudinal reciprocity in food sharing among brown capuchin monkeys. Anim Behav 2000;60:253-261.
Anderson JR. Chimpanzees and capuchin monkeys: comparative cognition. In Russon AE, Bard KA, Parker ST (eds). Reaching into thought: The minds of the great apes. Cambridge: Cambridge University Press; 1996:23-56.
Johnson-Frey SH, Newman-Norlund R, Grafton ST. A distributed left hemisphere network active during planning of everyday tool use skills. Cereb Cortex 2005;15:681-695.

Publication Dates

Publication in this collection
Jul-Sep 2010

History

Received
05 Nov 2009
Accepted
28 June 2010

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] Barbas H. Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neurosci Biobehav Rev 1995;193:499-510.

[2] Fuster JM. The Prefrontal Cortex: Anatomy, physiology, and neuropsychology of the frontal lobe. Philadelphia: Lippincott-Raven; 1997.

[3] Roberts AC, Wallis JD. Inhibitory control and affective processing in the prefrontal cortex: neuropsychological studies in the common marmoset. Cereb Cortex 2000;10:252-262.

[4] Miller EK, Freedman DJ, Wallis JD. The prefrontal cortex: categories, concepts and cognition. Philos Trans R Soc Lond B Biol Sci 2002;357(1424):1123-1136.

[5] Wood J, Grafman J. Human prefrontal cortex: processing and representational perspectives. Nat Neurosci 2003;4:139-147.

[6] Fuster JM. Memory in the cerebral cortex. Cambridge, MA: MIT Press; 1995.

[7] Fuster JM. Memory systems in the brain. New York: Raven Press; 2000.

[8] Miller EK. The prefrontal cortex and cognitive control. Nat Neurosci 2000;01:59-65.

[9] Semendeferi K, Damasio H, Frank R, Van Hoesen GW. The evolution of the frontal lobes: a volumetric analysis based on three-dimensional reconstructions of magnetic resonance scans of human and ape brains. J Hum Evol 1997;32:375-388.

[10] Dorus S, Vallender EJ, Evans PD, et al. Accelerated evolution of nervous system genes in the origin of Homo sapiens. Cell 2004;119:1027-1040.

[11] Phillips KA. Tool use in wild capuchin monkeys (Cebus albifrons trinitatis). Am J Primatol 1998;46:259-261.

[12] Boinski S. Object manipulation and tool use by brown capuchins in Suriname. Am J Phys Anthropol 2000;109:30.

[13] Jalles-Filho E, da Cunha RGT, Salm RA. Transport of tools and mental representation: is capuchin monkey tool behaviour a useful model of Plio-Pleistocene hominid technology? J Hum Evol 2001;40:365-377.

[14] Cleveland A, Rocca AM, Wendt EL, Westergaard GC. Transport of tools to food sites in tufted capuchin monkeys (Cebus apella). Anim Cog 2004; 7:193-198.

[15] Ottoni EB, Mannu M. Semi-free-ranging tufted capuchin monkeys (Cebus apella) spontaneously use tools to crack open nuts. Int J Primatol 2001;22:347-358.

[16] Resende BD, Ottoni EB. Brincadeira e aprendizagem do uso de ferramentas em macacos-prego (Cebus apella). Est Psicol 2002;7:173-180.

[17] Visalberghi E, Néel C. Tufted capuchins (Cebus apella) use weight and sound to choose between full and empty nuts. Ecol Psychol 2003;15:215-228.

[18] Fragaszy DM, Izar P, Visalberghi E, Ottoni EB, Oliveira MG. Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools. Am J Primatol 2004;64:359-366.

[19] Chevalier-Skolnikoff S. Spontaneous tool use and sensorimotor intelligence in Cebus compared with other monkeys and apes. Behav Brain Sci 1989;12:561-627.

[20] Mendes FDC, Martins LBR, Pereira JA, Marquezan RF. Fishing with a bait: a note on behavioural flexibility in Cebus apella Folia Primatologica; Int J Primatol 2000;71:350-352.

[21] de Waal FBM, Davis JM. Capuchin cognitive ecology: cooperation based on projected returns. Neuropsychologia 2003; 41:221-228.

[22] de Waal FBM, Dindo M, Freeman CA, Hall MJ. The monkey in the mirror: Hardly a stranger. Proc Natl Acad Sci U S A. 2005;102:11140-11147.

[23] Pandya DN, Yeterian EH. Comparison of prefrontal architecture and connections. Philos Trans R Soc Lond B Biol Sci 1996;351(1346):1423-1432.

[24] Barbas H. Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices. Brain Res Bull 2000;52:319-330.

[25] Chiavaras MM, Petrides M. Orbitofrontal sulci of the human and macaque monkey brain. Journal of Comparative Neurology 2000;422:35-54.

[26] Petrides M, Pandya DN. Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur J Neurosci 2002;16:291-310.

[27] Ongur D, Ferry AT, Price JL. Architectonic subdivision of the human orbital and medial prefrontal cortex. J Comp Neurol 2003;460:425-449.

[28] Schoenemann PT, Sheehan MJ, Glotzer LD. Prefrontal white matter volume is disproportionately larger in humans than in other primates. Nat Neurosci 2005;8:242-252.

[29] Barbas H, Pandya DN. Architecture and intrinsic connections of the prefrontal cortex in the Rhesus monkey. J Comp Neurol 1989;286:353-375.

[30] Barbas, H. Architecture and cortical connections of the prefrontal cortex in the rhesus monkey. Adv Neurol 1992;57:91-115.

[31] Romanski LM. Domain specificity in the primate prefrontal cortex. Cog Affec Behav Neurosci 2004;4:421-429.

[32] Roth G, Dicke U. Evolution of the brain and intelligence. Trends Cog Sci 2005; 9:250-257.

[33] Byrne RW, Whiten A. Machiavellian intelligence. In: Whiten A, Byrne RW (eds). Machiavellian intelligence II. Extensions and evaluations. Cambridge, UK: Cambridge Univ Press; 1997:1-23.

[34] Jerison HJ. The evolution of the brain and intelligence. New York: Academic Press; 1973.

[35] Rilling JK, Insel TR. The primate neocortex in comparative perspective using magnetic resonance imaging. J Hum Evol 1999;37:191-223.

[36] Westergaard GC, Gregory C. The subsistence technology of capuchins. Int J Primatol 1994;15:899-906.

[37] Westergaard GC, Gregory C, Suomi SJ. The stone tools of capuchins (Cebus apella). Int J Primatol 1995;16:1017-1024.

[38] de Waal FBM. Attitudinal reciprocity in food sharing among brown capuchin monkeys. Anim Behav 2000;60:253-261.

[39] Anderson JR. Chimpanzees and capuchin monkeys: comparative cognition. In Russon AE, Bard KA, Parker ST (eds). Reaching into thought: The minds of the great apes. Cambridge: Cambridge University Press; 1996:23-56.

[40] Johnson-Frey SH, Newman-Norlund R, Grafton ST. A distributed left hemisphere network active during planning of everyday tool use skills. Cereb Cortex 2005;15:681-695.

Brasil