Advertisement

Morphological Correlations of Human and Monkey Frontal Lobe

  • D. N. Pandya
  • E. H. Yeterian
Part of the Research and Perspectives in Neurosciences book series (NEUROSCIENCE)

Abstract

The prefrontal cortex has long been regarded as a major integrative subdivision of the forebrain. In particular, the results of clinical, experimental, and neuroimaging studies have established a role for this region in a variety of functions, such as planning and sequencing, emotional significance, attention, and representational memory. One question that arises is whether the discrete functions ascribed to the prefrontal cortex represent circumscribed processes at the neural level — that is, are subserved by a specific cortical subsector — or are dependent on the interactions of different prefrontal regions. A broader issue is the degree to which functions that appear to have the prefrontal cortex as a critical focus depend upon interactions with post-Rolandic cortices. Knowledge of the morphological characteristics of the prefrontal cortex may provide further insight into the underlying nature of these cognitive-behavioral functions. Therefore, in examining a complex process such as decision-making from a neural perspective, it may be beneficial to consider functional components in the context of cellular as well as connectional features of prefrontal areas.

A large amount of comparative research in monkeys on both structural and functional aspects of the prefrontal cortex has been carried out in recent years. Although the prefrontal cortex in humans has been shown to have a role in higher cognitive functions on the basis of clinical and neuroimaging techniques, such studies do not permit a detailed analysis of morphological underpinnings. There is a need to correlate data from human and monkey studies to gain a better understanding of cortical function. Several investigators have parcellated the human frontal cortex on the basis of architectonic features (e.g., Brodmann 1909; von Economo and Koskinas 1925; Sarkissov et al. 1955), and similar studies have been carried out in monkeys (e.g., Brodmann 1905; Vogt and Vogt 1919; Walker 1940). The cortical maps in humans and monkeys share basic similarities; however, they differ in regard to boundaries of specific areas and the numbers of areas identified. In an attempt to reconcile these differences, prefrontal areas have been examined from the perspective of progressive architectonic differentiation. Accordingly, the prefrontal cortex in both humans and monkeys can be organized in terms of two parallel trends. Thus, in both species a mediodorsal trend can be traced from the archicortex (hippocampal rudiment) on the medial surface around the corpus callosum. This trend proceeds through prosiocortical areas 24, 32, and 25, extends into medial areas 8B, 9B, and mediodorsal area 10, passes to dorsal areas 10 and 46, and ends in dorsal areas 9A/46 and 8A. A basoventral trend originates in the paleocortex (olfactory tubercle) on the orbital surface. This trend extends from orbital proisocortex to areas 13, 14, and 11, progresses through area 47/12 and ventral areas 10 and 46, and finally reaches areas 9/46, 8A, as well as areas 45 and 44 (Petrides and Pandya 1995).

Progressive architectonic differentiation has been correlated with cortical connections in monkeys (Pandya and Yeterian 1985; Barbas and Pandya 1989). The intrinsic connections of the prefrontal cortex are organized in a specific manner. Within each trend a given area projects in two directions, to a more differentiated region on the one hand and to a less differentiated region on the other. Likewise, long connections between prefrontal cortices and post-Rolandic sensory association regions — somatosensory, visual, and auditory — reflect progressive architectonic organization. Within each trend, frontal areas are related most strongly to post-Rolandic areas that appear to have a similar level of architectonic differentiation.

The data on the progressive architecture and intrinsic connectivity of the prefrontal cortex suggest a neural substrate for the continual interchange of information between proisocortices on the one hand and highly differentiated isocortices on the other. Conceptually with regard to decision-making, this intrinsic prefrontal circuitry may be thought of as providing systematic linkages between regions engaged in emotion (e.g., areas 13, 14, and 11) and motivation (e.g., areas 25 and 32); planning, sequencing and working memory (e.g., areas 9, 10 and 46); and attention (e.g., area 8). At the same time, the long association connections between the prefrontal cortex and post-Rolandic regions are integrated with the intrinsic prefrontal circuitry in a systematic manner, thereby allowing post-Rolandic influences such as complex long-term memories and immediate perceptions to play a role in ongoing decisional processes.

Keywords

Prefrontal Cortex Prefrontal Area Prefrontal Region Dorsal Area Morphological Correlation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abbie AA (1940) Cortical lamination in the Monotremata. J Comp Neurol 72:428–467Google Scholar
  2. Aggleton JP, Mishkin M (1983) Memory impairments following restricted medial thalamic lesions in monkeys. Exp Brain Res 52:199–209CrossRefPubMedGoogle Scholar
  3. Bachevalier J, Mishkin M (1986) Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys. Behav Brain Res 20:249–261CrossRefPubMedGoogle Scholar
  4. Barbas H, Pandya DN (1989) Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol 286:353–375CrossRefPubMedGoogle Scholar
  5. Bianchi L (1895) The function of the frontal lobes. Brain 18:497–522CrossRefGoogle Scholar
  6. Bonin G von, Bailey P (1947) The neocortex of Macaca mulatta. University of Illinois Press, Urbana Brodmann K (1909) Vergleichende Lokalisationlehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues, Barth, LeipzigGoogle Scholar
  7. Chavis D, Pandya DN (1976) Further observations on corticofrontal connections in the rhesus monkey. Brain Res 117:369–386CrossRefPubMedGoogle Scholar
  8. Damasio AR, Anderson, SW (1993) The frontal lobes. In: Heilman KM, Valenstein E (eds) Clinical neuropsychology. 3rd ed. Oxford University Press, New York, pp 409–460Google Scholar
  9. Damasio AR, Tranel D, Damasio HC (1991) Somatic markers and the guidance of behavior: Theory and preliminary testing. In: Levin H, Eisenberg H, Benton A (eds) Frontal lobe function and dysfunction. Oxford University Press, New York, pp 217–229Google Scholar
  10. Dart RA (1934) The dual structure of the neopallium: Its history and significance. J Anat 69:3–19PubMedGoogle Scholar
  11. Ferrier D (1876) The functions of the brain, Smith, Elder, LondonCrossRefGoogle Scholar
  12. Funahashi S, Bruce CJ, Goldman-Rakic PS (1989) Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. J Neurophysiol 61:331–349PubMedGoogle Scholar
  13. Fuster JM (1984) Behavioral electrophysiology of the prefrontal cortex. Trends Neurosci 7:408–414CrossRefGoogle Scholar
  14. Fuster JM (1989) The prefrontal cortex. 2nd ed. Raven Press, New YorkGoogle Scholar
  15. Giguere M, Goldman-Rakic PS (1988) Mediodorsal nucleus: Areal, laminar, and tangential distribution of afférents and efferents in the frontal lobe of rhesus monkeys. J Comp Neurol 277:195–213CrossRefPubMedGoogle Scholar
  16. Goldman-Rakic PS (1987) Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In: Mountcastle VB, Plum F (eds) Handbook of physiology. Vol 5, pt 1. American Physiological Society, Bethesda, MD, pp 373–417Google Scholar
  17. Hast MH, Fischer JM, Wetzel AB, Thompson VE (1974) Cortical motor representation of the laryngeal muscles in Macaca mulatta. Brain Res 73:229–240CrossRefPubMedGoogle Scholar
  18. Heilman KM, Pandya DN, Geschwind N (1970) Trimodal inattention following parietal lobe ablations. Trans Am Neurol Assoc 95:259–261PubMedGoogle Scholar
  19. Iversen SD, Mishkin M (1970) Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity. Exp Brain Res 11:376–386CrossRefPubMedGoogle Scholar
  20. Jacobsen CF (1935) Functions of the frontal association area in primates. Arch Neurol Psychiat 33:558-569Google Scholar
  21. Lugaresi E, Medori R, Montagna P, Baruzzi A, Cortelli P, Lugaresi A, Tinuper P, Zucconi M, Gambetti P (1986) Fatal familial insomnia and dysautonomia with selective degeneration of thalamic nuclei. New Engl J Med 315:997–1003CrossRefPubMedGoogle Scholar
  22. Luria AR (1973) The frontal lobes and the regulation of behavior. In: Pribram KH, Luria AR (eds) Psychophysiology of the frontal lobes. Academic Press, New York, pp 3–26Google Scholar
  23. Matelli M, Luppino G, Rizzolatti G (1985) Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey. Behav Brain Res 18:125–136CrossRefPubMedGoogle Scholar
  24. Nauta WJH (1971) The problem of the frontal lobe: A reinterpretation. J Psychiat Res 8:167–187CrossRefPubMedGoogle Scholar
  25. Pandya DN, Barnes CL (1987) Architecture and connections of the frontal lobe. In: Perecman E (ed) The frontal lobes revisited. IRBN Press, New York, pp 41–72Google Scholar
  26. Pandya DN, Sanides F (1973) Architectonic parcellation of the temporal operculum in rhesus monkey, and its projection pattern. Z Anat Entwicklungsgesch 139:127–161CrossRefPubMedGoogle Scholar
  27. Pandya DN, Seltzer B (1982) Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. J Comp Neurol 204:196–210CrossRefPubMedGoogle Scholar
  28. Pandya DN, Yeterian, EH (1985) Architecture and connections of cortical association areas. In: Peters A, Jones EG (eds) Cerebral cortex. Vol 4. Association and auditory cortices. Plenum Publishing Corp, New York, pp 3–61Google Scholar
  29. Pandya DN, Yeterian EH (1990) Prefrontal cortex in relation to other cortical areas in rhesus monkey: Architecture and connections. In: Uylings HBM, Van Eden CG, de Bruin JPC, Corner MA, Feenstra MPG (eds) Progress in brain research. Vol. 85. Elsevier Science Publishers BV, Amsterdam, pp 63–94Google Scholar
  30. Passingham RE (1985) Memory of monkeys (Macaca mulatta) with lesions in prefrontal cortex. Behav Neurosci 99:3–21CrossRefPubMedGoogle Scholar
  31. Petersen SE, Fox PT, Posner MI, Mintun M, Raichle ME (1988) Positron emission tomographic studies of the cortical anatomy of single word processing. Nature 331:585–589CrossRefPubMedGoogle Scholar
  32. Petersen SE, Fox PT, Posner MI, Mintun M, Raichle ME (1989) Positron emission tomographic studies of the processing of single words. J Cognit Neurosci 1:153–170CrossRefGoogle Scholar
  33. Petrides M (1991) Monitoring of selections of visual stimuli and the primate frontal cortex. Proc Roy Soc Lond B 246:293–298CrossRefGoogle Scholar
  34. Petrides M, Pandya DN (1995) Comparative architectonic analysis of the human and macaque frontal cortex. In: Grafman J, Boller F (eds) Handbook of neuropsychology. Elsevier Science Publishers BV, AmsterdamGoogle Scholar
  35. Petrides M, Alivasatos B, Evans AC, Meyer E (1993a) Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. Proc Natl Acad Sci USA 90:873–877CrossRefPubMedGoogle Scholar
  36. Petrides M, Alivasatos B, Meyer E, Evans AC (1993b) Functional activation of the human frontal cortex during the performance of verbal working memory tasks. Proc Natl Acad Sci USA 90:878–882CrossRefPubMedGoogle Scholar
  37. Preuss TM, Goldman-Rakic PS (1991) Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca. Proc Natl Acad Sci USA 90:878–882Google Scholar
  38. Rizzolatti G, Camarda R, Fogassi L, Gentilucci M, Luppino G, Matelli M (1988) Functional organization of inferior area 6 in the macaque monkey. Exp Brain Res 71:491–507CrossRefPubMedGoogle Scholar
  39. Rosene DL, Pandya DN (1983) Architectonics and connections of the posterior parahippocampal gyrus in the rhesus monkey. Soc Neurosci Abstr 9:222Google Scholar
  40. Rosenkilde CE (1979) Functional heterogeneity of the prefrontal cortex: A review. Behav Neural Biol 25:301–345CrossRefPubMedGoogle Scholar
  41. Sanides F (1969) Comparative architectonics of the neocortex of mammals and their evolutionary interpretation. Ann NY Acad Sci 167:404–423CrossRefGoogle Scholar
  42. Sarkissov SA, Filimonoff IN, Kononowa EP, Preobraschenskaja IS (1955) Atlas of the cytoarchitectonics of the human cerebral cortex. Medgiz, MoscowGoogle Scholar
  43. Seltzer B, Pandya DN (1989) Intrinsic connections and architectonics of the superior temporal sulcus in the rhesus monkey. J Comp Neurol 290:451–471CrossRefPubMedGoogle Scholar
  44. Shallice T, Burgess P (1991) Higher-order cognitive impairments and frontal lobe lesions in man. In: Levin HS, Eisenberg HM, Benton AL (eds) Frontal lobe function and dysfunction. Oxford University Press, New York, pp 125–138Google Scholar
  45. Siwek DF, Pandya DN (1991) Prefrontal projections to the mediodorsal nucleus of the thalamus in the rhesus monkey. J Comp Neurol 312: 509–524CrossRefPubMedGoogle Scholar
  46. Stamm JS (1973) Functional dissociation between the inferior and arcuate segments of dorsolateral prefrontal cortex in the monkey. Neuropsychologia 11:181–190CrossRefPubMedGoogle Scholar
  47. Stuss DT, Benson DF (1986) The frontal lobes. Raven Press, New YorkGoogle Scholar
  48. Teuber HL (1972) Unity and diversity of frontal lobe functions. Acta Neurobiol Exp 32:615–656Google Scholar
  49. Vogt C, Vogt O (1919) Allgemeinere Ergebnisse unserer Hirnforschung. J Psychol Neurol 25:279–461Google Scholar
  50. Wada T (1951) Dorsomedial thalamotomy I. The principles and methods particularly consulted with E.E.G. records. Folia Psych Neurol Jap 4:309–319Google Scholar
  51. Walker AE (1940) A cytoarchitectural study of the prefrontal areas of the macaque monkey. J Comp Neurol 73:59–86CrossRefGoogle Scholar
  52. Watanabe-Sawaguchi K, Kubota K, Arikuni T (1991) Cytoarchitecture and intrafrontal connections of the frontal cortex of the brain of the hamadryas baboon. J Comp Neurol 311:108–133CrossRefPubMedGoogle Scholar
  53. Welch K, Stuteville P (1958) Experimental production of unilateral neglect in monkeys. Brain 81:341–347CrossRefPubMedGoogle Scholar
  54. Wilson FAW, Scalhaide SPO, Goldman-Rakic PS (1993) Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260:1955–1958CrossRefPubMedGoogle Scholar
  55. Yeterian EH, Pandya DN (1988) Corticothalamic connections of paralimbic regions in the rhesus monkey. J Comp Neurol 269:130–146CrossRefPubMedGoogle Scholar
  56. Yeterian EH, Pandya DN (1991) Prefrontostriatal connections in relation to cortical architectonic organization in rhesus monkeys. J Comp Neurol 312:43–67CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1996

Authors and Affiliations

  • D. N. Pandya
    • 1
    • 3
    • 4
  • E. H. Yeterian
    • 2
  1. 1.Edith Nourse Rogers Memorial Veterans HospitalBedfordUSA
  2. 2.Department of PsychologyColby CollegeWatervilleUSA
  3. 3.Departments of Anatomy and NeurologyBoston University School of MedicineBostonUSA
  4. 4.Harvard Neurological UnitBeth Israel HospitalBostonUSA

Personalised recommendations