Potent and Quick Responses to Conspecific Faces and Snakes in the Anterior Cingulate Cortex of Monkeys

Overview

Journal Front Behav Neurosci

Specialty Psychology

Date 2020 Nov 2

PMID 33132857

Citations 1

Authors

Naho Konoike

Haruhiko Iwaoki

Katsuki Nakamura

Affiliations

Soon will be listed here.

Abstract

Appropriate processing of others' facial emotions is a fundamental ability of primates in social situations. Several moods and anxiety disorders such as depression cause a negative bias in the perception of facial emotions. Depressive patients show abnormalities of activity and gray matter volume in the perigenual portion of the anterior cingulate cortex (ACC) and an increase of activation in the amygdala. However, it is not known whether neurons in the ACC have a function in the processing of facial emotions. Furthermore, detecting predators quickly and taking avoidance behavior are important functions in a matter of life and death for wild monkeys. the existence of predators in their vicinity is life-and-death information for monkeys. In the present study, we recorded the activity of single neurons from the monkey ACC and examined the responsiveness of the ACC neurons to various visual stimuli including monkey faces, snakes, foods, and artificial objects. About one-fourth of the recorded neurons showed a significant change in activity in response to the stimuli. The ACC neurons exhibited high selectivity to certain stimuli, and more neurons exhibited the maximal response to monkey faces and snakes than to foods and objects. The responses to monkey faces and snakes were faster and stronger compared to those to foods and objects. Almost all of the neurons that responded to video stimuli responded strongly to negative facial stimuli, threats, and scream. Most of the responsive neurons were located in the cingulate gyrus or the ventral bank of the cingulate sulcus just above or anterior to the genu of the corpus callosum, that is, the perigenual portion of the ACC, which has a strong mutual connection with the amygdala. These results suggest that the perigenual portion of the ACC in addition to the amygdala processes emotional information, especially negative life-and-death information such as conspecifics' faces and snakes.

Citing Articles

The Saliency of Snake Scales and Leopard Rosettes to Infants: Its Relevance to Graphical Patterns Portrayed in Prehistoric Art.

Coss R, Charles E Front Psychol. 2021; 12:763436.

PMID: 34880813 PMC: 8645795. DOI: 10.3389/fpsyg.2021.763436.

References

Le Q, Isbell L, Matsumoto J, Nguyen M, Hori E, Maior R . Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes. Proc Natl Acad Sci U S A. 2013; 110(47):19000-5. PMC: 3839741. DOI: 10.1073/pnas.1312648110. View

Diehl M, Romanski L . Responses of prefrontal multisensory neurons to mismatching faces and vocalizations. J Neurosci. 2014; 34(34):11233-43. PMC: 4138335. DOI: 10.1523/JNEUROSCI.5168-13.2014. View

Hale 3rd W, Jansen J, Bouhuys A, Van Den Hoofdakker R . The judgement of facial expressions by depressed patients, their partners and controls. J Affect Disord. 1998; 47(1-3):63-70. DOI: 10.1016/s0165-0327(97)00112-2. View

Romanski L, Giguere M, Bates J, Goldman-Rakic P . Topographic organization of medial pulvinar connections with the prefrontal cortex in the rhesus monkey. J Comp Neurol. 1997; 379(3):313-32. View

Mayberg H, Liotti M, Brannan S, McGinnis S, Mahurin R, Jerabek P . Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry. 1999; 156(5):675-82. DOI: 10.1176/ajp.156.5.675. View

Ongur D, Drevets W, Price J . Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc Natl Acad Sci U S A. 1998; 95(22):13290-5. PMC: 23786. DOI: 10.1073/pnas.95.22.13290. View

Drevets W . Neuroimaging abnormalities in the amygdala in mood disorders. Ann N Y Acad Sci. 2003; 985:420-44. DOI: 10.1111/j.1749-6632.2003.tb07098.x. View

Bush , Luu , Posner . Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci. 2000; 4(6):215-222. DOI: 10.1016/s1364-6613(00)01483-2. View

Gur R, Erwin R, Gur R, Zwil A, Heimberg C, Kraemer H . Facial emotion discrimination: II. Behavioral findings in depression. Psychiatry Res. 1992; 42(3):241-51. DOI: 10.1016/0165-1781(92)90116-k. View

10.

Botvinick M . Conflict monitoring and decision making: reconciling two perspectives on anterior cingulate function. Cogn Affect Behav Neurosci. 2008; 7(4):356-66. DOI: 10.3758/cabn.7.4.356. View

11.

Botteron K, Raichle M, Drevets W, Heath A, Todd R . Volumetric reduction in left subgenual prefrontal cortex in early onset depression. Biol Psychiatry. 2002; 51(4):342-4. DOI: 10.1016/s0006-3223(01)01280-x. View

12.

Kim Y, Sakata H, Nejime M, Konoike N, Miyachi S, Nakamura K . Afferent connections of the dorsal, perigenual, and subgenual anterior cingulate cortices of the monkey: Amygdalar inputs and intrinsic connections. Neurosci Lett. 2018; 681:93-99. DOI: 10.1016/j.neulet.2018.05.028. View

13.

Saleem K, Kondo H, Price J . Complementary circuits connecting the orbital and medial prefrontal networks with the temporal, insular, and opercular cortex in the macaque monkey. J Comp Neurol. 2007; 506(4):659-93. DOI: 10.1002/cne.21577. View

14.

Pessoa L, Adolphs R . Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance. Nat Rev Neurosci. 2010; 11(11):773-83. PMC: 3025529. DOI: 10.1038/nrn2920. View

15.

Kuraoka K, Konoike N, Nakamura K . Functional differences in face processing between the amygdala and ventrolateral prefrontal cortex in monkeys. Neuroscience. 2015; 304:71-80. DOI: 10.1016/j.neuroscience.2015.07.047. View

16.

Hoffman K, Gothard K, Schmid M, Logothetis N . Facial-expression and gaze-selective responses in the monkey amygdala. Curr Biol. 2007; 17(9):766-72. DOI: 10.1016/j.cub.2007.03.040. View

17.

Blair R, Morris J, Frith C, Perrett D, Dolan R . Dissociable neural responses to facial expressions of sadness and anger. Brain. 1999; 122 ( Pt 5):883-93. DOI: 10.1093/brain/122.5.883. View

18.

Rudebeck P, Buckley M, Walton M, Rushworth M . A role for the macaque anterior cingulate gyrus in social valuation. Science. 2006; 313(5791):1310-2. DOI: 10.1126/science.1128197. View

19.

Tsao D, Schweers N, Moeller S, Freiwald W . Patches of face-selective cortex in the macaque frontal lobe. Nat Neurosci. 2008; 11(8):877-9. PMC: 8123225. DOI: 10.1038/nn.2158. View

20.

Kalin N, Shelton S, Davidson R . The role of the central nucleus of the amygdala in mediating fear and anxiety in the primate. J Neurosci. 2004; 24(24):5506-15. PMC: 6729317. DOI: 10.1523/JNEUROSCI.0292-04.2004. View