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Amygdalar connections of the macaque areas 45A and 45B

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Abstract

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.

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References

  • Adolphs R (2010) What does the amygdala contribute to social cognition? Ann NY Acad Sci 1191:42–61

    Article  PubMed Central  PubMed  Google Scholar 

  • Aggleton JP, Mishkin M (1984) Projections of the amygdala to the thalamus in the cynomolgus monkey. J Comp Neurol 222:56–68

    Article  CAS  PubMed  Google Scholar 

  • Amaral DG, Price JL (1984) Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 230:465–496

    Article  CAS  PubMed  Google Scholar 

  • Amaral D, Behniea H, Kelly J (2003) Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey. Neuroscience 118:1099–1120

    Article  CAS  PubMed  Google Scholar 

  • Barbas H (2007) Specialized elements of orbitofrontal cortex in primates. Ann NY Acad Sci 1121:10–32

    Article  PubMed  Google Scholar 

  • Barbas H, De Olmos J (1990) Projections from the amygdala to basoventral and mediodorsal prefrontal regions in the rhesus monkey. J Comp Neurol 300:549–571

    Article  CAS  PubMed  Google Scholar 

  • Barbas H, Zikopoulos B, Timbie C (2011) Sensory pathways and emotional context for action in primate prefrontal cortex. Biol Psychiatry 69:1133–1139

    Article  PubMed  Google Scholar 

  • 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 518:2570–2591

    PubMed  Google Scholar 

  • 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 31:12351–12363

    Article  CAS  PubMed  Google Scholar 

  • Carmichael ST, Price JL (1995) Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 363:615–641

    Article  CAS  PubMed  Google Scholar 

  • 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 32:1337–1353

    Article  PubMed  Google Scholar 

  • Dancause N, Barbay S, Frost SB, Plautz EJ, Chen D, Zoubina EV, Stowe AM (2005) Extensive cortical rewiring after brain injury. J Neurosci 25:10167–10179

    Article  CAS  PubMed  Google Scholar 

  • Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24:581–604

    Article  CAS  PubMed  Google Scholar 

  • Fecteau JH, Munoz DP (2006) Salience, relevance, and firing: a priority map for target selection. Trends Cogn Sci 10:382–390

    Article  PubMed  Google Scholar 

  • 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 212:269–301

    Article  PubMed  Google Scholar 

  • 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 20:141–168

    Article  PubMed  Google Scholar 

  • 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 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ghashghaei HT, Hilgetag CC, Barbas H (2007) Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 34:905–923

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ghazanfar AA, Nielsen K, Logothetis NK (2006) Eye movements of monkey observers viewing vocalizing conspecifics. Cognition 101:515–529

    Article  PubMed  Google Scholar 

  • Gonzalez Andino SL, de Peralta Grave, Menendez R (2012) Coding of saliency by ensemble bursting in the amygdala of primates. Front Behav Neurosci 6:38

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 97:1671–1683

    Article  CAS  PubMed  Google Scholar 

  • McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257–332

    Article  CAS  PubMed  Google Scholar 

  • Nelissen K, Luppino G, Vanduffel W, Rizzolatti G, Orban GA (2005) Observing others: multiple action representation in the frontal lobe. Science 310:332–336

    Article  CAS  PubMed  Google Scholar 

  • Paxinos G, Huang XF, Toga AW (2000) The rhesus monkey brain in stereotaxic coordinates. Academic Press, San Diego

    Google Scholar 

  • 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 17–58

    Google Scholar 

  • 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 16:291–310

    Article  CAS  PubMed  Google Scholar 

  • Pitkänen A, Amaral DG (1998) Organization of the intrinsic connections of the monkey amygdaloid complex: projections originating in the lateral nucleus. J Comp Neurol 398:431–458

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 279–381

    Google Scholar 

  • 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 337:1–31

    Article  CAS  PubMed  Google Scholar 

  • Romanski LM, Averbeck BB (2009) The primate cortical auditory system and neural representation of conspecific vocalizations. Annu Rev Neurosci 32:315–346

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 256:175–210

    Article  CAS  PubMed  Google Scholar 

  • Salzman CD, Fusi S (2010) Emotion, cognition, and mental state representation in amygdala and prefrontal cortex. Annu Rev Neurosci 33:173–202

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stefanacci L, Amaral DG (2000) Topographic organization of cortical inputs to the lateral nucleus of the macaque monkey amygdala. J Comp Neurol 421:52–79

    Article  CAS  PubMed  Google Scholar 

  • Stefanacci L, Amaral DG (2002) Some observations on cortical inputs to the macaque monkey amygdala: an anterograde tracing study. J Comp Neurol 451:301–323

    Article  PubMed  Google Scholar 

  • 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 169:287–301

    Article  CAS  PubMed  Google Scholar 

  • Tsao DY, Moeller S, Freiwald WA (2008) Comparing face patch systems in macaques and humans. Proc Natl Acad Sci USA 105:19514–19519

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 11:1095–1116

    CAS  PubMed  Google Scholar 

  • Yukie M (2002) Connections between the amygdala and auditory cortical areas in the macaque monkey. Neurosci Res 42:219–229

    Article  PubMed  Google Scholar 

  • 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, 2012

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Acknowledgments

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.

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Correspondence to Giuseppe Luppino.

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Marzio Gerbella and Matteo Baccarini equally contributed to this work.

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Gerbella, M., Baccarini, M., Borra, E. et al. Amygdalar connections of the macaque areas 45A and 45B. Brain Struct Funct 219, 831–842 (2014). https://doi.org/10.1007/s00429-013-0538-2

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  • DOI: https://doi.org/10.1007/s00429-013-0538-2

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