Abstract
Ideas from classical philosophy and psychology that emotion and cognition are distinct and separate have been challenged by evidence of their intricate interaction in the brain. Accumulated evidence shows that areas associated with emotions and cognition are strongly linked and influence each other according to principles based on the structural organization of the cortex. Subcortical structures that process information about needs and drives are old in phylogeny and innervate the prefrontal cortex, targeting strongly the posterior orbitofrontal cortex (pOFC) and the anterior cingulate cortex (ACC). These two prefrontal regions are part of the cortical component of the limbic system but are functionally distinct. Through widespread connections, the pOFC acts as an integrator of the internal and external environments for the perception of affective events. In contrast, the ACC specializes in the expression of emotions through robust pathways to central autonomic structures. Both prefrontal limbic regions are connected with lateral prefrontal areas associated with cognitive functions, effectively linking areas associated with emotion and cognition. Functional and circuit studies in animals and humans indicate that even simple tasks necessitate interaction between areas associated with cognition and emotions and suggest that their linkage is disrupted in several psychiatric and neurologic diseases.
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References
Anderson MC, Bunce JG, Barbas H (2015) Prefrontal-hippocampal pathways underlying inhibitory control over memory. Neurobiol Learn Mem. doi:10.1016/j.nlm.2015.11.008
Armstrong E (1991) The limbic system and culture: an allometric analysis of the neocortex and limbic nuclei. Hum Nat 2:117–136
Barbas H (1986) Pattern in the laminar origin of corticocortical connections. J Comp Neurol 252:415–422
Barbas H (1988) Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J Comp Neurol 276:313–342
Barbas H (1993) Organization of cortical afferent input to orbitofrontal areas in the rhesus monkey. Neuroscience 56:841–864
Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neurosci Biobehav Rev 19:499–510
Barbas H (1997) Two prefrontal limbic systems: their common and unique features. In: Sakata H, Mikami A, Fuster JM (eds) The association cortex: structure and function. Harwood Academic Publising, Amsterdam, pp 99–115
Barbas H (2000a) Complementary role of prefrontal cortical regions in cognition, memory and emotion in primates. Adv Neurol 84:87–110
Barbas H (2000b) Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices. Brain Res Bull 52:319–330
Barbas H (2015) General cortical and special prefrontal connections: principles from structure to function. Annu Rev Neurosci 38:269–289
Barbas H, Blatt GJ (1995) Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey. Hippocampus 5:511–533
Barbas H, García-Cabezas MA (2015) Motor cortex layer 4: less is more. Trends Neurosci 38(5):259–261
Barbas H, Mesulam MM (1981) Organization of afferent input to subdivisions of area 8 in the rhesus monkey. J Comp Neurol 200:407–431
Barbas H, Pandya DN (1989) Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J Comp Neurol 286(3):353–375
Barbas H, Rempel-Clower N (1997) Cortical structure predicts the pattern of corticocortical connections. Cereb Cortex 7:635–646
Barbas H, Henion TH, Dermon CR (1991) Diverse thalamic projections to the prefrontal cortex in the rhesus monkey. J Comp Neurol 313:65–94
Barbas H, Ghashghaei H, Dombrowski SM, Rempel-Clower NL (1999) Medial prefrontal cortices are unified by common connections with superior temporal cortices and distinguished by input from memory-related areas in the rhesus monkey. J Comp Neurol 410:343–367
Barbas H, Ghashghaei H, Rempel-Clower N, Xiao D (2002) Anatomic basis of functional specialization in prefrontal cortices in primates. In: Grafman J (ed) Handbook of neuropsychology, vol 7: the frontal lobes, vol 2. Elsevier Science B.V, Amsterdam, pp 1–27
Barbas H, Saha S, Rempel-Clower N, Ghashghaei T (2003) Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression. BMC Neurosci 4(1):25
Barbas H, Hilgetag CC, Saha S, Dermon CR, Suski JL (2005) Parallel organization of contralateral and ipsilateral prefrontal cortical projections in the rhesus monkey. BMC Neurosci 6(1):32
Benes FM, Vincent SL, Todtenkopf M (2001) The density of pyramidal and nonpyramidal neurons in anterior cingulate cortex of schizophrenic and bipolar subjects. Biol Psychiatry 50(6):395–406
Bereket A, Kiess W, Lustig RH, Muller HL, Goldstone AP, Weiss R, Yavuz Y, Hochberg Z (2012) Hypothalamic obesity in children. Obes Rev 13(9):780–798
Broca P (1878) Anatomie comparée des circonvolutions cérébrales: Le grand lobe limbique et la scissure limbique dans la série des mammifères. Rev D’anthropol 1:385–498
Brown JA, Woodworth HL, Leinninger GM (2015) To ingest or rest? Specialized roles of lateral hypothalamic area neurons in coordinating energy balance. Front Syst Neurosci 9:9. doi:10.3389/fnsys.2015.00009
Bunce JG, Barbas H (2011) Prefrontal pathways target excitatory and inhibitory systems in memory-related medial temporal cortices. Neuroimage 55(4):1461–1474
Bunce JG, Zikopoulos B, Feinberg M, Barbas H (2013) Parallel prefrontal pathways reach distinct excitatory and inhibitory systems in memory-related rhinal cortices. J Comp Neurol 512(18):4260–4283
Carmichael ST, Price JL (1995) Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 363:642–664
Carmichael ST, Clugnet MC, Price JL (1994) Central olfactory connections in the macaque monkey. J Comp Neurol 346(3):403–434
Carter CS, Botvinick MM, Cohen JD (1999) The contribution of the anterior cingulate cortex to executive processes in cognition. Rev Neurosci 10(1):49–57
Cavada C, Company T, Tejedor J, Cruz-Rizzolo RJ, Reinoso-Suarez F (2000) The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb Cortex 10:220–242
Damasio AR (1994) Descarte’s error: emotion, reason, and the human brain, vol 1. G. P. Putnam’s Sons, New York
Darwin C (1872) The expression of the emotions in man and animals. J. Murray, London
Davis M, Whalen PJ (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6(1):13–34
De Olmos J (1990) Amygdaloid nuclear gray complex. In: Paxinos G (ed) The human nervous system. Academic, San Diego, pp 583–710
Dermon CR, Barbas H (1994) Contralateral thalamic projections predominantly reach transitional cortices in the rhesus monkey. J Comp Neurol 344:508–531
Dreher JC, Koechlin E, Tierney M, Grafman J (2008) Damage to the fronto-polar cortex is associated with impaired multitasking. PLoS One 3(9):e3227
Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47
Funahashi S, Kubota K (1994) Working memory and prefrontal cortex. Neurosci Res 21:1–11
Fuster JM (1989) The prefrontal cortex, vol 2. Raven Press, New York
García-Cabezas MA, Barbas H (2016) Anterior cingulate pathways may affect emotions through orbitofrontal cortex. Cereb Cortex. doi:10.1093/cercor/bhw284
García-Cabezas MA, Barbas H (2014) Area 4 has layer IV in adult primates. Eur J Neurosci 39:1824–1834
Ghashghaei HT, Barbas H (2002) Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115:1261–1279
Ghashghaei HT, Hilgetag CC, Barbas H (2007) Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 34(3):905–923
Giguere M, Goldman-Rakic PS (1988) Mediodorsal nucleus: areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys. J Comp Neurol 277:195–213
Goldman-Rakic PS (1988) Topography of cognition: parallel distributed networks in primate association cortex. Annu Rev Neurosci 11:137–156
Gross CG (1992) Representation of visual stimuli in inferior temporal cortex. Philos Theol R Soc B 335:3–10
Gross CG, Bender DB, Rocha-Miranda CE (1969) Visual receptive fields of neurons in inferotemporal cortex of the monkey. Science 166:1303–1306
Hilgetag CC, Medalla M, Beul SF, Barbas H (2016) The primate connectome in context: Principles of connections of the cortical visual system. NeuroImage 134:685–702
Insausti R, Munoz M (2001) Cortical projections of the non-entorhinal hippocampal formation in the cynomolgus monkey (Macaca fascicularis). Eur J Neurosci 14(3):435–451
John YJ, Bullock D, Zikopoulos B, Barbas H (2013) Anatomy and computational modeling of networks underlying cognitive-emotional interaction. Front Hum Neurosci 7:101. doi:10.3389/fnhum.2013.00101
Johnston JB (1923) Further contributions to the study of the evolution of the forebrain. J Comp Neurol 35:337–481
Johnston K, Levin HM, Koval MJ, Everling S (2007) Top-down control-signal dynamics in anterior cingulate and prefrontal cortex neurons following task switching. Neuron 53(3):453–462
Jones EG (1985) The thalamus. Plenum Press, New York
Jongen-Relo AL, Amaral DG (1998) Evidence for a GABAergic projection from the central nucleus of the amygdala to the brainstem of the macaque monkey: a combined retrograde tracing and in situ hybridization study. Eur J Neurosci 10:2924–2933
Kievit J, Kuypers HGJM (1977) Organization of the thalamo-cortical connexions to the frontal lobe in the rhesus monkey. Exp Brain Res 29:299–322
Lanius RA, Bluhm R, Lanius U, Pain C (2006) A review of neuroimaging studies in PTSD: heterogeneity of response to symptom provocation. J Psychiatr Res 40(8):709–729
LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184
LeDoux J (2003) The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23(4–5):727–738
MacLean PD (1952) Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). Electroencephalogr Clin Neurophysiol 4(4):407–418
Mayberg HS (2007) Defining the neural circuitry of depression: toward a new nosology with therapeutic implications. Biol Psychiatry 61(6):729–730
Medalla M, Barbas H (2006) Diversity of laminar connections linking periarcuate and lateral intraparietal areas depends on cortical structure. Eur J Neurosci 23(1):161–179
Medalla M, Barbas H (2009) Synapses with inhibitory neurons differentiate anterior cingulate from dorsolateral prefrontal pathways associated with cognitive control. Neuron 61(4):609–620
Medalla M, Barbas H (2010) Anterior cingulate synapses in prefrontal areas 10 and 46 suggest differential influence in cognitive control. J Neurosci 30(48):16068–16081
Medalla M, Barbas H (2014) Specialized prefrontal “auditory fields”: organization of primate prefrontal-temporal pathways. Front Neurosci 8:77. doi:10.3389/fnins.2014.00077
Milad MR, Quirk GJ, Pitman RK, Orr SP, Fischl B, Rauch SL (2007) A role for the human dorsal anterior cingulate cortex in fear expression. Biol Psychiatry 62(10):1191–1194
Miller EK (2000) The prefrontal cortex and cognitive control. Nat Rev Neurosci 1:59–65
Morecraft RJ, Geula C, Mesulam MM (1992) Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey. J Comp Neurol 323:341–358
Mosher CP, Zimmerman PE, Gothard KM (2010) Response characteristics of basolateral and centromedial neurons in the primate amygdala. J Neurosci 30(48):16197–16207. doi:10.1523/JNEUROSCI.3225-10.2010
Murray EA (2007) The amygdala, reward and emotion. Trends Cogn Sci 11(11):489–497
Nauta WJH (1971) The problem of the frontal lobe: a reinterpretation. J Psychiatr Res 8:167–187
Nauta WJH (1979) Expanding borders of the limbic system concept. In: Rasmussen T, Marino R (eds) Functional neurosurgery. Raven Press, New York, pp 7–23
Nishijo H, Hori E, Tazumi T, Ono T (2008) Neural correlates to both emotion and cognitive functions in the monkey amygdala. Behav Brain Res 188(1):14–23
Olszewski J (1952) The thalamus of the Macaca mulatta. An atlas for use with the stereotaxic instrument. Karger, Basel
Pandya DN, Seltzer B, Barbas H (1988) Input-output organization of the primate cerebral cortex. In: Steklis HD, Erwin J (eds) Comparative primate biology, Neurosciences, vol 4. Alan R. Liss, New York, pp 39–80
Paré D, Smith Y (1993) The intercalated cell masses project to the central and medial nuclei of the amygdala in cats. Neuroscience 57:1077–1090
Paré D, Quirk GJ, LeDoux JE (2004) New vistas on amygdala networks in conditioned fear. J Neurophysiol 92(1):1–9
Paton JJ, Belova MA, Morrison SE, Salzman CD (2006) The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439(7078):865–870
Pessoa L (2013) The cognitive-emotional brain: from interactions to integration. The MIT Press, Cambridge, MA
Petrides M (1996) Lateral frontal cortical contribution to memory. Semin Neurosci 8:57–63
Petrovich GD, Gallagher M (2007) Control of food consumption by learned cues: a forebrain-hypothalamic network. Physiol Behav 91(4):397–403
Plato (1892/impression of 1931) Phaedrus. In: The dialogues of Plato translated into English with analysis and introductions, vol I, 3rd edn. Oxford University Press, London, pp 246–254
Poremba A, Mishkin M (2007) Exploring the extent and function of higher-order auditory cortex in rhesus monkeys. Hear Res 229(1–2):14–23
Porrino LJ, Crane AM, Goldman-Rakic PS (1981) Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys. J Comp Neurol 198:121–136
Rauch SL, Shin LM, Phelps EA (2006) Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research – past, present, and future. Biol Psychiatry 60(4):376–382
Rempel-Clower NL, Barbas H (1998) Topographic organization of connections between the hypothalamus and prefrontal cortex in the rhesus monkey. J Comp Neurol 398:393–419
Roberts AC, Wallis JD (2000) Inhibitory control and affective processing in the prefrontal cortex: neuropsychological studies in the common marmoset. Cereb Cortex 10:252–262
Rockel AJ, Hiorns RW, Powell TP (1980) The basic uniformity in structure of the neocortex. Brain 103(2):221–244
Romanski LM, Goldman-Rakic PS (2002) An auditory domain in primate prefrontal cortex. Nat Neurosci 5(1):15–16
Rosene DL, Van Hoesen GW (1977) Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science 198:315–317
Saha S, Batten TF, Henderson Z (2000) A GABAergic projection from the central nucleus of the amygdala to the nucleus of the solitary tract: a combined anterograde tracing and electron microscopic immunohistochemical study. Neuroscience 99(4):613–626
Sakagami M, Watanabe M (2007) Integration of cognitive and motivational information in the primate lateral prefrontal cortex. Ann N Y Acad Sci 1104:89–107
Sanides F (1970) Functional architecture of motor and sensory cortices in primates in the light of a new concept of neocortex evolution. In: Noback CR, Montagna W (eds) The primate brain: advances in primatology. Appleton-Century-Crofts Educational Division/Meredith Corporation, New York, pp 137–208
Schall JD, Morel A, King DJ, Bullier J (1995) Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams. J Neurosci 15:4464–4487
Schiller PH (1998) The neural control of visually guided eye movements. In: Richards JE (ed) Cognitive neuroscience of attention. Lawrence Erlbaum Assoc. Publ, New Jersey, pp 3–50
Shepherd GM (2007) Perspectives on olfactory processing, conscious perception, and orbitofrontal cortex. Ann N Y Acad Sci 1121:87–101
Shepherd GM (2012) Neurogastronomy: how the brain creates flavor and why it matters. Columbia University Press, New York
Siwek DF, Pandya DN (1991) Prefrontal projections to the mediodorsal nucleus of the thalamus in the rhesus monkey. J Comp Neurol 312:509–524
Timbie C, Barbas H (2014) Specialized pathways from the primate amygdala to posterior orbitofrontal cortex. J Neurosci 34(24):8106–8118
Timbie C, Barbas H (2015) Pathways for emotions: specializations in the amygdalar, mediodorsal thalamic, and posterior orbitofrontal network. J Neurosci 35(34):11976–11987
Vogt BA, Barbas H (1988) Structure and connections of the cingulate vocalization region in the rhesus monkey. In: Newman JD (ed) The physiological control of mammalian vocalization. Plenum Publ. Corp., New York, pp 203–225
Wang XJ, Tegner J, Constantinidis C, Goldman-Rakic PS (2004) Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory. Proc Natl Acad Sci U S A 101(5):1368–1373
Watanabe M (2007) Role of anticipated reward in cognitive behavioral control. Curr Opin Neurobiol 17(2):213–219
White EL (1989) Cortical circuits. Synaptic organization of the cerebral cortex. Structure, function and theory. Birkhäuser, Boston
Yakovlev PI (1948) Motility, behavior and the brain: stereodynamic organization and neurocoordinates of behavior. J Nerv Ment Dis 107:313–335
Yakovlev PI (1959) Pathoarchitectonic studies of cerebral malformations. III. Arrhinencephalies (holotelencephalies). J Neuropathol Exp Neurol 18(1):22–55
Zhang W, Schneider DM, Belova MA, Morrison SE, Paton JJ, Salzman CD (2013) Functional circuits and anatomical distribution of response properties in the primate amygdala. J Neurosci 33(2):722–733
Acknowledgments
This work is supported by grants from NIH (R01 MH057414, R01 NS024760 (HB)); M. Á. García-Cabezas was the recipient of a 2014 NARSAD Young Investigator Grant from the Brain & Behavior Research Foundation (grant number 22777, P&S Fund Investigator).
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Barbas, H., García-Cabezas, M.Á. (2017). Prefrontal Cortex Integration of Emotion and Cognition. In: Watanabe, M. (eds) The Prefrontal Cortex as an Executive, Emotional, and Social Brain. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56508-6_4
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