Brain Structure and Function

, Volume 219, Issue 3, pp 831–842 | Cite as

Amygdalar connections of the macaque areas 45A and 45B

  • Marzio Gerbella
  • Matteo Baccarini
  • Elena Borra
  • Stefano Rozzi
  • Giuseppe Luppino
Original Article


In the present study, based on injections of retro- or retro-anterograde tracers at the cortical level, we analyzed the amygdalar connections of the caudal ventrolateral prefrontal areas 45A and 45B of the macaque and compared them with those of the adjacent areas 8/FEF, 8r, 46v, and 12r. The results showed that areas 45A and 45B display reciprocal amygdalar connections, which appear to be considerably richer than those of their neighboring areas. Specifically, these two areas are a target of differentially weighted projections originating predominantly from the magnocellular and the intermediate subdivisions of the basal nucleus and are a source of projections mostly directed to the magnocellular subdivision of the basal nucleus and the dorsal part of the lateral nucleus. The present data, together with previous data on the thalamic connectivity of areas 45A and 45B (Contini et al. Eur J Neurosci 32:1337–53, 2010), suggest that direct and indirect—trans-thalamic—amygdalar connectivity is a characterizing connectional feature of these two areas. Specifically, the amygdalar connections of area 45A, for which a role in communication behavior has been proposed, could convey information on the emotional significance of communicative signals to this area, where it could play a crucial role in guiding appropriate social interactions. Furthermore, the amygdalar connections of area 45B, possibly involved in higher-order aspects of visual guidance of gaze, could convey information related to the relevance of visual stimuli, which could contribute to a representation of priority maps in this VLPF area.


Ventrolateral prefrontal cortex Communication behavior Oculomotor behavior Primates 



The work was supported by Ministero dell’Istruzione, dell’Università e della Ricerca (Grant number: PRIN 2008, no. 2008J7YFNR_002); European Commission Grant Cogsystems FP7-250013.


  1. Adolphs R (2010) What does the amygdala contribute to social cognition? Ann NY Acad Sci 1191:42–61PubMedCentralPubMedCrossRefGoogle Scholar
  2. Aggleton JP, Mishkin M (1984) Projections of the amygdala to the thalamus in the cynomolgus monkey. J Comp Neurol 222:56–68PubMedCrossRefGoogle Scholar
  3. Amaral DG, Price JL (1984) Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 230:465–496PubMedCrossRefGoogle Scholar
  4. Amaral D, Behniea H, Kelly J (2003) Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey. Neuroscience 118:1099–1120PubMedCrossRefGoogle Scholar
  5. Barbas H (2007) Specialized elements of orbitofrontal cortex in primates. Ann NY Acad Sci 1121:10–32PubMedCrossRefGoogle Scholar
  6. Barbas H, De Olmos J (1990) Projections from the amygdala to basoventral and mediodorsal prefrontal regions in the rhesus monkey. J Comp Neurol 300:549–571PubMedCrossRefGoogle Scholar
  7. Barbas H, Zikopoulos B, Timbie C (2011) Sensory pathways and emotional context for action in primate prefrontal cortex. Biol Psychiatry 69:1133–1139PubMedCrossRefGoogle Scholar
  8. Borra E, Belmalih A, Gerbella M, Rozzi S, Luppino G (2010) Projections of the hand field of the macaque ventral premotor area F5 to the brainstem and spinal cord. J Comp Neurol 518:2570–2591PubMedGoogle Scholar
  9. Borra E, Gerbella M, Rozzi S, Luppino G (2011) Anatomical evidence for the involvement of the macaque ventrolateral prefrontal area 12r in controlling goal-directed actions. J Neurosci 31:12351–12363PubMedCrossRefGoogle Scholar
  10. Carmichael ST, Price JL (1995) Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 363:615–641PubMedCrossRefGoogle Scholar
  11. Contini M, Baccarini M, Borra E, Gerbella M, Rozzi S, Luppino G (2010) Thalamic projections to the macaque caudal ventrolateral prefrontal areas 45A and 45B. Eur J Neurosci 32:1337–1353PubMedCrossRefGoogle Scholar
  12. Dancause N, Barbay S, Frost SB, Plautz EJ, Chen D, Zoubina EV, Stowe AM (2005) Extensive cortical rewiring after brain injury. J Neurosci 25:10167–10179PubMedCrossRefGoogle Scholar
  13. Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24:581–604PubMedCrossRefGoogle Scholar
  14. Fecteau JH, Munoz DP (2006) Salience, relevance, and firing: a priority map for target selection. Trends Cogn Sci 10:382–390PubMedCrossRefGoogle Scholar
  15. Gerbella M, Belmalih A, Borra E, Rozzi S, Luppino G (2007) Multimodal architectonic subdivision of the caudal ventrolateral prefrontal cortex of the macaque monkey. Brain Struct Funct 212:269–301PubMedCrossRefGoogle Scholar
  16. Gerbella M, Belmalih A, Borra E, Rozzi S, Luppino G (2010) Cortical connections of the macaque caudal ventrolateral prefrontal areas 45A and 45B. Cereb Cortex 20:141–168PubMedCrossRefGoogle Scholar
  17. Gerbella M, Borra E, Tonelli S, Rozzi S, Luppino G (2012) Connectional heterogeneity of the ventral part of the Macaque Area 46. Cereb Cortex. doi: 10.1093/cercor/bhs096.Online Google Scholar
  18. Ghashghaei HT, Barbas H (2002) Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115:1261–1279PubMedCrossRefGoogle Scholar
  19. Ghashghaei HT, Hilgetag CC, Barbas H (2007) Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 34:905–923PubMedCentralPubMedCrossRefGoogle Scholar
  20. Ghazanfar AA, Nielsen K, Logothetis NK (2006) Eye movements of monkey observers viewing vocalizing conspecifics. Cognition 101:515–529PubMedCrossRefGoogle Scholar
  21. Gonzalez Andino SL, de Peralta Grave, Menendez R (2012) Coding of saliency by ensemble bursting in the amygdala of primates. Front Behav Neurosci 6:38PubMedCentralPubMedCrossRefGoogle Scholar
  22. Gothard KM, Battaglia FP, Erickson CA, Spitler KM, Amaral DG (2007) Neural responses to facial expression and face identity in the monkey amygdala. J Neurophysiol 97:1671–1683PubMedCrossRefGoogle Scholar
  23. McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257–332PubMedCrossRefGoogle Scholar
  24. Nelissen K, Luppino G, Vanduffel W, Rizzolatti G, Orban GA (2005) Observing others: multiple action representation in the frontal lobe. Science 310:332–336PubMedCrossRefGoogle Scholar
  25. Paxinos G, Huang XF, Toga AW (2000) The rhesus monkey brain in stereotaxic coordinates. Academic Press, San DiegoGoogle Scholar
  26. Petrides M, Pandya DN (1994) Comparative architectonic analysis of the human and the macaque frontal cortex. In: Boller F, Grafman J (eds) Handbook of neuropsychology, vol 9. Elsevier, Amsterdam, pp 17–58Google Scholar
  27. Petrides M, Pandya DN (2002) Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and cortico-cortical connection patterns in the monkey. Eur J Neurosci 16:291–310PubMedCrossRefGoogle Scholar
  28. Pitkänen A, Amaral DG (1998) Organization of the intrinsic connections of the monkey amygdaloid complex: projections originating in the lateral nucleus. J Comp Neurol 398:431–458PubMedCrossRefGoogle Scholar
  29. 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 198:121–136PubMedCrossRefGoogle Scholar
  30. Price JL, Russchen FT, Amaral DG (1987) The limbic region. II. The amygdaloid complex. In: Bjorkland A, Hokfelt T, Swanson L (eds) Handbook of chemical neuroanatomy. Elsevier, Amsterdam, pp 279–381Google Scholar
  31. Ray JP, Price JL (1993) The organization of projections from the mediodorsal nucleus of the thalamus to orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 337:1–31PubMedCrossRefGoogle Scholar
  32. Romanski LM, Averbeck BB (2009) The primate cortical auditory system and neural representation of conspecific vocalizations. Annu Rev Neurosci 32:315–346PubMedCentralPubMedCrossRefGoogle Scholar
  33. Russchen FT, Amaral DG, Price JL (1987) The afferent input to the magnocellular division of the mediodorsal thalamic nucleus in the monkey Macaca fascicularis. J Comp Neurol 256:175–210PubMedCrossRefGoogle Scholar
  34. Salzman CD, Fusi S (2010) Emotion, cognition, and mental state representation in amygdala and prefrontal cortex. Annu Rev Neurosci 33:173–202PubMedCentralPubMedCrossRefGoogle Scholar
  35. Stefanacci L, Amaral DG (2000) Topographic organization of cortical inputs to the lateral nucleus of the macaque monkey amygdala. J Comp Neurol 421:52–79PubMedCrossRefGoogle Scholar
  36. Stefanacci L, Amaral DG (2002) Some observations on cortical inputs to the macaque monkey amygdala: an anterograde tracing study. J Comp Neurol 451:301–323PubMedCrossRefGoogle Scholar
  37. Tazumi T, Hori E, Maior RS, Ono T, Nishijo H (2010) Neural correlates to seen gaze-direction and head orientation in the macaque monkey amygdala. Neuroscience 169:287–301PubMedCrossRefGoogle Scholar
  38. Tsao DY, Moeller S, Freiwald WA (2008) Comparing face patch systems in macaques and humans. Proc Natl Acad Sci USA 105:19514–19519PubMedCentralPubMedCrossRefGoogle Scholar
  39. Webster MJ, Ungerleider LG, Bachevalier J (1991) Connections of inferior temporal areas TE and TEO with medial temporal-lobe structures in infant and adult monkeys. J Neurosci 11:1095–1116PubMedGoogle Scholar
  40. Yukie M (2002) Connections between the amygdala and auditory cortical areas in the macaque monkey. Neurosci Res 42:219–229PubMedCrossRefGoogle Scholar
  41. Zimmerman PE, Mosher C, Gothard KM (2012) Looking at the eyes engages single unit activity in the primate amygdala during naturalistic social interactions. Program No. 402.02. Neuroscience Meeting Planner. New Orleans, LA: Society for Neuroscience, 2012Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Marzio Gerbella
    • 1
  • Matteo Baccarini
    • 1
    • 2
  • Elena Borra
    • 1
  • Stefano Rozzi
    • 1
  • Giuseppe Luppino
    • 1
    • 3
  1. 1.Dipartimento di NeuroscienzeUniversità di Parma and Rete Multidisciplinare Tecnologica, Istituto Italiano di Tecnologia (IIT)ParmaItaly
  2. 2.Centro di NeuroscienzeUniversità di FerraraFerraraItaly
  3. 3.Unità di Fisiologia, Dipartimento di NeuroscienzeUniversità di ParmaParmaItaly

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