Neural mechanisms of social empathy in the anterior cingulate cortex
Empathy is a prosocial behavior that perceives the emotional state of others, expresses similar perceptions that match those of others, and mediates different social behaviors. Empathic behaviors for pain and fear also exist in primates and rodents. In the past decades, the neural mechanisms of empathy have been defined as a result of various sensations and perceptions, such as visual and hearing stimuli, which cause mirror activations in brain regions, such as the insular, the inferior frontal, and the medial frontal cortices, among which the anterior cingulate cortex (ACC) has been identified as a core region of the neural network that is associated with the empathic activity in mammals. Most studies on the neural mechanisms underlying empathy have been based on rodent models, which allowed for single-cell resolution mapping of neuronal activity; moreover, the application of optogenetic techniques in rodent models has led to a deeper delineation of neural circuits. Here, we review the role of the ACC in two behavioral paradigms, pain and fear empathy, in rodents at the neuronal and neural circuit levels. Understanding how the ACC mediates empathic behavior in the brain will provide new targets in the treatment for neuropsychiatric disorders characterized by empathic disorders.
De Waal FB, 2008, Putting the altruism back into altruism: The evolution of empathy. Annu Rev Psychol, 59: 279–300. https://doi.org/10.1146/annurev.psych.59.103006.093625
Sivaselvachandran S, Acland EL, Abdallah S, et al., 2018, Behavioral and mechanistic insight into rodent empathy. Neurosci Biobehav Rev, 91: 130–137. https://doi.org/10.1016/j.neubiorev.2016.06.007
Ben-Ami Bartal I, Decety J, Mason P, 2011, Empathy and pro-social behavior in rats. Science, 334: 1427–1430. https://doi.org/10.1126/science.1210789
Burkett JP, Andari E, Johnson ZV, et al., 2016, Oxytocin-dependent consolation behavior in rodents. Science, 351: 375–378. https://doi.org/10.1126/science.aac4785
Wardwell J, Watanasriyakul WT, Normann MC, et al., 2020, Physiological and behavioral responses to observing a sibling experience a direct stressor in prairie voles. Stress (Amsterdam, Netherlands), 23: 444–456. https://doi.org/10.1080/10253890.2020.1724950
Decety J, Bartal IB, Uzefovsky F, et al., 2016, Empathy as a driver of prosocial behaviour: Highly conserved neurobehavioural mechanisms across species. Philos Trans R Soc Lond B Biol Sci, 371: 20150077. https://doi.org/10.1098/rstb.2015.0077
Kiyokawa Y, 2017, Social odors: Alarm pheromones and social buffering. Curr Top Behav Neurosci, 30: 47–65. https://doi.org/10.1007/7854_2015_406
Baron-Cohen S, Wheelwright S, 2004, The empathy quotient: An investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J Autism Dev Disord, 34: 163–175. https://doi.org/10.1023/b:jadd.0000022607.19833.00
Derntl B, Seidel EM, Schneider F, et al., 2012, How specific are emotional deficits? A comparison of empathic abilities in schizophrenia, bipolar and depressed patients. Schizophr Res, 142: 58–64. https://doi.org/10.1016/j.schres.2012.09.020
Keum S, Shin HS, 2019, Neural basis of observational fear learning: A potential model of affective empathy. Neuron, 104: 78–86. https://doi.org/10.1016/j.neuron.2019.09.013
Meyza K, Knapska E, 2018, What can rodents teach us about empathy? Curr Opin Psychol, 24: 15–20. https://doi.org/10.1016/j.copsyc.2018.03.002
Paradiso E, Gazzola V, Keysers C, 2021, Neural mechanisms necessary for empathy-related phenomena across species. Curr Opin Neurobiol, 68: 107–115. https://doi.org/10.1016/j.conb.2021.02.005
Jauniaux J, Khatibi A, Rainville P, et al., 2019, A meta-analysis of neuroimaging studies on pain empathy: Investigating the role of visual information and observers’ perspective. Soc Cogn Affect Neurosci, 14: 789–813. https://doi.org/10.1093/scan/nsz055
Jeon D, Kim S, Chetana M, et al., 2010, Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nat Neurosci, 13: 482–488. https://doi.org/10.1038/nn.2504
Ethofer T, Stegmaier S, Koch K, et al., 2020, Are you laughing at me? Neural correlates of social intent attribution to auditory and visual laughter. Hum Brain Mapp, 41: 353–361. https://doi.org/10.1002/hbm.24806
Zhang S, Xu M, Chang WC, et al., 2016, Organization of long-range inputs and outputs of frontal cortex for top-down control. Nat Neurosci, 19: 1733–1742. https://doi.org/10.1038/nn.4417
Zhang S, Xu M, Kamigaki T, et al., 2014, Selective attention. Long-range and local circuits for top-down modulation of visual cortex processing. Science, 345: 660–665. https://doi.org/10.1126/science.1254126
Keehn RJ, Pueschel EB, Gao Y, et al., 2021, Underconnectivity between visual and salience networks and links with sensory abnormalities in autism spectrum disorders. J Am Acad Child Adolesc Psychiatry, 60: 274–285. https://doi.org/10.1016/j.jaac.2020.02.007
Lamm C, Decety J, Singer T, 2011, Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. Neuroimage, 54: 2492–2502. https://doi.org/10.1016/j.neuroimage.2010.10.014
Meffert H, Gazzola V, Den Boer JA, et al., 2013, Reduced spontaneous but relatively normal deliberate vicarious representations in psychopathy. Brain, 136(Pt 8): 2550–2562. https://doi.org/10.1093/brain/awt190
Singer T, Seymour B, O’doherty J, et al., 2004, Empathy for pain involves the affective but not sensory components of pain. Science, 303: 1157–1162. https://doi.org/10.1126/science.1093535
Cruz A, Heinemans M, Márquez C, et al., 2020, Freezing displayed by others is a learned cue of danger resulting from co-experiencing own freezing and shock. Curr Biol, 30: 1128–1135.e6. https://doi.org/10.1016/j.cub.2020.01.025
Van Heukelum S, Mars RB, Guthrie M, et al., 2020, Where is cingulate cortex? A cross-species view. Trends Neurosci, 43: 285–299. https://doi.org/10.1016/j.tins.2020.03.007
Vogt BA, Paxinos G, 2014, Cytoarchitecture of mouse and rat cingulate cortex with human homologies. Brain Struct Funct, 219: 185–192. https://doi.org/10.1007/s00429–012–0493–3
Vogt BA, 2005, Pain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci, 6: 533–544. https://doi.org/10.1038/nrn1704
Preuss TM, 1995, Do rats have prefrontal cortex? The rose-woolsey-akert program reconsidered. J Cogn Neurosci, 7: 1–24. https://doi.org/10.1162/jocn.1995.7.1.1
Laubach M, Amarante LM, Swanson K, et al., 2018, What, if anything, is rodent prefrontal cortex? eNeuro, 5: e0315-e0318. https://doi.org/10.1523/eneuro.0315–18.2018
Liang J, Xu W, Hsu YT, et al., 2015, Conditional neuroligin-2 knockout in adult medial prefrontal cortex links chronic changes in synaptic inhibition to cognitive impairments. Mol Psychiatry, 20: 850–859. https://doi.org/10.1038/mp.2015.31
Van De Werd HJ, Rajkowska G, Evers P, et al., 2010, Cytoarchitectonic and chemoarchitectonic characterization of the prefrontal cortical areas in the mouse. Brain Struct Funct, 214: 339–353. https://doi.org/10.1007/s00429–010–0247–z
Van De Werd HJ, Uylings HB, 2014, Comparison of (stereotactic) parcellations in mouse prefrontal cortex. Brain Struct Funct, 219: 433–459. https://doi.org/10.1007/s00429–013–0630–7
Carlson D, David LK, Gallagher NM, et al., 2017, Dynamically timed stimulation of corticolimbic circuitry activates a stress-compensatory pathway. Biol Psychiatry, 82: 904–913. https://doi.org/10.1016/j.biopsych.2017.06.008
Vachon-Presseau E, Roy M, Martel MO, et al., 2012, Neural processing of sensory and emotional-communicative information associated with the perception of vicarious pain. Neuroimage, 63: 54–62. https://doi.org/10.1016/j.neuroimage.2012.06.030
Panksepp JB, Lahvis GP, 2011, Rodent empathy and affective neuroscience. Neurosci Biobehav Rev, 35: 1864–1875. https://doi.org/10.1016/j.neubiorev.2011.05.013
Langford DJ, Crager SE, Shehzad Z, et al., 2006, Social modulation of pain as evidence for empathy in mice. Science, 312: 1967–1970. https://doi.org/10.1126/science.1128322
Smith ML, Asada N, Malenka RC, 2021, Anterior cingulate inputs to nucleus accumbens control the social transfer of pain and analgesia. Science, 371: 153–159. https://doi.org/10.1126/science.abe3040
Smith ML, Hostetler CM, Heinricher MM, et al., 2016, Social transfer of pain in mice. Sci Adv, 2: e1600855. https://doi.org/10.1126/sciadv.1600855
Smith ML, Walcott AT, Heinricher MM, et al., 2017, Anterior cingulate cortex contributes to alcohol withdrawal-induced and socially transferred hyperalgesia. eNeuro, 4: e0087-17. https://doi.org/10.1523/eneuro.0087–17.2017
Gasquoine PG, 2013, Localization of function in anterior cingulate cortex: From psychosurgery to functional neuroimaging. Neurosci Biobehav Rev, 37: 340–348. https://doi.org/10.1016/j.neubiorev.2013.01.002
Li Z, Lu YF, Li CL, et al., 2014, Social interaction with a cagemate in pain facilitates subsequent spinal nociception via activation of the medial prefrontal cortex in rats. Pain, 155: 1253–1261. https://doi.org/10.1016/j.pain.2014.03.019
Zaki J, Wager TD, Singer T, et al., 2016, The anatomy of suffering: Understanding the relationship between nociceptive and empathic pain. Trends Cogn Sci, 20: 249–259. https://doi.org/10.1016/j.tics.2016.02.003
Xiao X, Zhang YQ, 2018, A new perspective on the anterior cingulate cortex and affective pain. Neurosci Biobehav Rev, 90: 200–211. https://doi.org/10.1016/j.neubiorev.2018.03.022
Lockwood PL, 2016, The anatomy of empathy: Vicarious experience and disorders of social cognition. Behav Brain Res, 311: 255–266. https://doi.org/10.1016/j.bbr.2016.05.048
Zhuo M, 2016, Neural mechanisms underlying anxiety-chronic pain interactions. Trends Neurosci, 39: 136–145. https://doi.org/10.1016/j.tins.2016.01.006
Kim S, Mátyás F, Lee S, et al., 2012, Lateralization of observational fear learning at the cortical but not thalamic level in mice. Proc Natl Acad Sci U S A, 109: 15497–15501. https://doi.org/10.1073/pnas.1213903109
Allsop SA, Wichmann R, Mills F, et al., 2018, Corticoamygdala transfer of socially derived information gates observational learning. Cell, 173: 1329–1342.e18. https://doi.org/10.1016/j.cell.2018.04.004
Keum S, Kim A, Shin JJ, et al., 2018, A missense variant at the Nrxn3 locus enhances empathy fear in the mouse. Neuron, 98: 588–601.e5. https://doi.org/10.1016/j.neuron.2018.03.041
Bliss TV, Collingridge GL, Kaang BK, et al., 2016, Synaptic plasticity in the anterior cingulate cortex in acute and chronic pain. Nat Rev Neurosci, 17: 485–496. https://doi.org/10.1038/nrn.2016.68
Carrillo M, Han Y, Migliorati F, et al., 2019, Emotional mirror neurons in the rat’s anterior cingulate cortex. Curr Biol, 29: 1301–1312.e6. https://doi.org/10.1016/j.cub.2019.03.024
Wang YQ, Wang J, Xia SH, et al., 2021, Neuropathic pain generates silent synapses in thalamic projection to anterior cingulate cortex. Pain, 162: 1322–1333. https://doi.org/10.1097/j.pain.0000000000002149
Gallese V, Keysers C, Rizzolatti G, 2004, A unifying view of the basis of social cognition. Trends Cogn Sci, 8: 396–403. https://doi.org/10.1016/j.tics.2004.07.002
Wager TD, Atlas LY, Botvinick MM, et al., 2016, Pain in the ACC? Proc Natl Acad Sci U S A, 113: E2474–E2475. https://doi.org/10.1073/pnas.1600282113
Krishnan A, Woo CW, Chang LJ, et al., 2016, Somatic and vicarious pain are represented by dissociable multivariate brain patterns. Elife, 5: e15166. https://doi.org/10.7554/eLife.15166
Corradi-Dell’acqua C, Tusche A, Vuilleumier P, et al., 2016, Cross-modal representations of first-hand and vicarious pain, disgust and fairness in insular and cingulate cortex. Nat Commun, 7: 10904. https://doi.org/10.1038/ncomms10904
Sakaguchi T, Iwasaki S, Okada M, et al., 2018, Ethanol facilitates socially evoked memory recall in mice by recruiting pain-sensitive anterior cingulate cortical neurons. Nat Commun, 9: 3526. https://doi.org/10.1038/s41467–018–05894–y
Rizzolatti G, Craighero L, 2004, The mirror-neuron system. Annu Rev Neurosci, 27: 169–192. https://doi.org/10.1146/annurev.neuro.27.070203.144230
Yesudas EH, Lee TM, 2015, The role of cingulate cortex in vicarious pain. Biomed Res Int, 2015: 719615. https://doi.org/10.1155/2015/719615
Urban-Ciecko J, Fanselow EE, Barth AL, 2015, Neocortical somatostatin neurons reversibly silence excitatory transmission via GABAb receptors. Curr Biol, 25: 722–731. https://doi.org/10.1016/j.cub.2015.01.035
Scheggia D, Manago F, Maltese F, et al., 2020, Somatostatin interneurons in the prefrontal cortex control affective state discrimination in mice. Nat Neurosci, 23: 47–60. https://doi.org/10.1038/s41593–019–0551–8
Yizhar O, Fenno LE, Prigge M, et al., 2011, Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature, 477: 171–178. https://doi.org/10.1038/nature10360
Ma Y, Hu H, Berrebi AS, et al., 2006, Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci, 26: 5069–5082. https://doi.org/10.1523/jneurosci.0661-06.2006
Xu X, Callaway EM, 2009, Laminar specificity of functional input to distinct types of inhibitory cortical neurons. J Neurosci, 29: 70–85. https://doi.org/10.1523/jneurosci.4104-08.2009
Lü YF, Yang Y, Li CL, et al., 2017, The locus coeruleus-norepinephrine system mediates empathy for pain through selective up-regulation of P2X3 receptor in dorsal root ganglia in rats. Front Neural Circuits, 11: 66. https://doi.org/10.3389/fncir.2017.00066
Jodo E, Chiang C, Aston-Jones G, 1998, Potent excitatory influence of prefrontal cortex activity on noradrenergic locus coeruleus neurons. Neuroscience, 83: 63–79. https://doi.org/10.1016/s0306-4522(97)00372-2
Arnsten AF, Goldman-Rakic PS, 1984, Selective prefrontal cortical projections to the region of the locus coeruleus and raphe nuclei in the rhesus monkey. Brain Res, 306: 9–18. https://doi.org/10.1016/0006-8993(84)90351-2
Luo WJ, Li CL, Geng KW, et al., 2020, The similar past pain experience evokes both observational contagious pain and consolation in stranger rat observers. Neurosci Lett, 722: 134840. https://doi.org/10.1016/j.neulet.2020.134840
Barroso AR, Araya EI, De Souza CP, et al., 2019, Characterization of rat ultrasonic vocalization in the orofacial formalin test: Influence of the social context. Eur Neuropsychopharmacol, 29: 1213–1226. https://doi.org/10.1016/j.euroneuro.2019.08.298
Kim A, Keum S, Shin HS, 2019, Observational fear behavior in rodents as a model for empathy. Genes Brain Behav, 18: e12521. https://doi.org/10.1111/gbb.12521
Apps MA, Rushworth MF, Chang SW, 2016, The anterior cingulate gyrus and social cognition: Tracking the motivation of others. Neuron, 90: 692–707. https://doi.org/10.1016/j.neuron.2016.04.018
Chang SW, Fagan NA, Toda K, et al., 2015, Neural mechanisms of social decision-making in the primate amygdala. Proc Natl Acad Sci U S A, 112: 16012–16017. https://doi.org/10.1073/pnas.1514761112
Kim SW, Kim M, Baek J, et al., 2022, Hemispherically lateralized rhythmic oscillations in the cingulate-amygdala circuit drive affective empathy in mice. Neuron, 111: 418- 429. https://doi.org/10.1016/j.neuron.2022.11.001
Chang SW, Dal Monte O, 2018, Shining light on social learning circuits. Trends Cogn Sci, 22: 673–675. https://doi.org/10.1016/j.tics.2018.05.002
Kim SW, Kim M, Shin HS, 2021, Affective empathy and prosocial behavior in rodents. Curr Opin Neurobiol, 68: 181–189. https://doi.org/10.1016/j.conb.2021.05.002
Ito W, Erisir A, Morozov A, 2015, Observation of distressed conspecific as a model of emotional trauma generates silent synapses in the prefrontal-amygdala pathway and enhances fear learning, but ketamine abolishes those effects. Neuropsychopharmacology, 40: 2536–2545. https://doi.org/10.1038/npp.2015.100
Ito W, Morozov A, 2019, Prefrontal-amygdala plasticity enabled by observational fear. Neuropsychopharmacology, 44: 1778–1787. https://doi.org/10.1038/s41386-019-0342-7
Rajasethupathy P, Sankaran S, Marshel JH, et al., 2015, Projections from neocortex mediate top-down control of memory retrieval. Nature, 526: 653–659. https://doi.org/10.1038/nature15389
Bruchey AK, Jones CE, Monfils MH, 2010, Fear conditioning by-proxy: Social transmission of fear during memory retrieval. Behav Brain Res, 214: 80–84. https://doi.org/10.1016/j.bbr.2010.04.047
Zheng C, Huang Y, Bo B, et al., 2020, Projection from the anterior cingulate cortex to the lateral part of mediodorsal thalamus modulates vicarious freezing behavior. Neurosci Bull, 36: 217–229. https://doi.org/10.1007/s12264-019-00427-z
Nomura H, Teshirogi C, Nakayama D, et al., 2019, Prior observation of fear learning enhances subsequent self-experienced fear learning with an overlapping neuronal ensemble in the dorsal hippocampus. Mol Brain, 12: 21. https://doi.org/10.1186/s13041-019-0443-6
Wang J, Li J, Yang Q, et al., 2021, Basal forebrain mediates prosocial behavior via disinhibition of midbrain dopamine neurons. Proc Natl Acad Sci U S A, 118: e2019295118. https://doi.org/10.1073/pnas.2019295118
Gungor NZ, Johansen J, 2019, A chronic pain in the ACC. Neuron, 102: 903–905. https://doi.org/10.1016/j.neuron.2019.05.021
Meda KS, Patel T, Braz JM, et al., 2019, Microcircuit mechanisms through which mediodorsal thalamic input to anterior cingulate cortex exacerbates pain-related aversion. Neuron, 102: 944–959.e3. https://doi.org/10.1016/j.neuron.2019.03.042
Tremblay R, Lee S, Rudy B, 2016, GABAergic interneurons in the neocortex: From cellular properties to circuits. Neuron, 91: 260–292. https://doi.org/10.1016/j.neuron.2016.06.033
Zhang L, Qin Z, Ricke KM, et al., 2020, Hyperactivated PTP1B phosphatase in parvalbumin neurons alters anterior cingulate inhibitory circuits and induces autism-like behaviors. Nat Commun, 11: 1017. https://doi.org/10.1038/s41467-020-14813-z
Taylor SF, Grove TB, Ellingrod VL, et al., 2019, The fragile brain: Stress vulnerability, negative affect and GABaergic neurocircuits in psychosis. Schizophr Bull, 45: 1170–1183. https://doi.org/10.1093/schbul/sbz046
Kepecs A, Fishell G, 2014, Interneuron cell types are fit to function. Nature, 505: 318–326. https://doi.org/10.1038/nature12983
Ährlund-Richter S, Xuan Y, Van Lunteren JA, et al., 2019, A whole-brain atlas of monosynaptic input targeting four different cell types in the medial prefrontal cortex of the mouse. Nat Neurosci, 22: 657–668. https://doi.org/10.1038/s41593–019–0354–y
Mitchell AS, 2015, The mediodorsal thalamus as a higher order thalamic relay nucleus important for learning and decision-making. Neurosci Biobehav Rev, 54: 76–88. https://doi.org/10.1016/j.neubiorev.2015.03.001
Delevich K, Tucciarone J, Huang ZJ, et al., 2015, The mediodorsal thalamus drives feedforward inhibition in the anterior cingulate cortex via parvalbumin interneurons. J Neurosci, 35: 5743–5753. https://doi.org/10.1523/jneurosci.4565-14.2015
Hattori R, Kuchibhotla KV, Froemke RC, et al., 2017, Functions and dysfunctions of neocortical inhibitory neuron subtypes. Nat Neurosci, 20: 1199–1208. https://doi.org/10.1038/nn.4619
Karnani MM, Jackson J, Ayzenshtat I, et al., 2016, Cooperative subnetworks of molecularly similar interneurons in mouse neocortex. Neuron, 90: 86–100. https://doi.org/10.1016/j.neuron.2016.02.037
Mitani A, Dong M, Komiyama T, 2018, Brain-computer interface with inhibitory neurons reveals subtype-specific strategies. curr Biol, 28: 77–83.e4. https://doi.org/10.1016/j.cub.2017.11.035
Antoine MW, Langberg T, Schnepel P, et al., 2019, Increased excitation-inhibition ratio stabilizes synapse and circuit excitability in four autism mouse models. Neuron, 101: 648– 661.e4. https://doi.org/10.1016/j.neuron.2018.12.026
Li XH, Matsuura T, Xue M, et al., 2021, Oxytocin in the anterior cingulate cortex attenuates neuropathic pain and emotional anxiety by inhibiting presynaptic long-term potentiation. Cell Rep, 36: 109411. https://doi.org/10.1016/j.celrep.2021.109411
Kleberg JL, Selbing I, Lundqvist D, et al., 2015, Spontaneous eye movements and trait empathy predict vicarious learning of fear. Int J Psychophysiol, 98: 577–583. https://doi.org/10.1016/j.ijpsycho.2015.04.001
Keehn B, Westerfield M, Townsend J, 2019, Brief report: Cross-modal capture: Preliminary evidence of inefficient filtering in children with autism spectrum disorder. J Autism Dev Disord, 49: 385–390. https://doi.org/10.1007/s10803-018-3674-y
Hashemi E, Ariza J, Rogers H, et al., 2017, The number of parvalbumin-expressing interneurons is decreased in the prefrontal cortex in autism. Cereb Cortex, 27: 1931–1943. https://doi.org/10.1093/cercor/bhw021
Filice F, Vörckel KJ, Sungur A, et al., 2016, Reduction in parvalbumin expression not loss of the parvalbumin-expressing GABA interneuron subpopulation in genetic parvalbumin and shank mouse models of autism. Mol Brain, 9: 10. https://doi.org/10.1186/s13041-016-0192-8
Martinez M, Multani N, Anor CJ, et al., 2018, Emotion detection deficits and decreased empathy in patients with Alzheimer’s disease and Parkinson’s disease affect caregiver mood and burden. Front Aging Neurosci, 10: 120. https://doi.org/10.3389/fnagi.2018.00120
Shi LJ, Zhou HY, Wang Y, et al., 2020, Altered empathy-related resting-state functional connectivity in adolescents with early-onset schizophrenia and autism spectrum disorders. Asian J Psychiatr, 53: 102167. https://doi.org/10.1016/j.ajp.2020.102167
Penagos-Corzo JC, Cosio Van-Hasselt M, Escobar D, et al., 2022, Mirror neurons and empathy-related regions in psychopathy: Systematic review, meta-analysis, and a working model. Social Neurosci, 17: 462–479. https://doi.org/10.1080/17470919.2022.2128868
Chow TE, Veziris CR, La Joie R, et al., 2022, Increasing empathic concern relates to salience network hyperconnectivity in cognitively healthy older adults with elevated amyloid-β burden. NeuroImage Clin, 37: 103282. https://doi.org/10.1016/j.nicl.2022.103282
Rieffe C, O’connor R, Bülow A, et al., 2021, Quantity and quality of empathic responding by autistic and non-autistic adolescent girls and boys. Autism, 25: 199–209. https://doi.org/10.1177/1362361320956422
Mckenzie K, Russell A, Golm D, et al., 2022, Empathic accuracy and cognitive and affective empathy in young adults with and without autism spectrum disorder. J Autism Dev Disord, 52: 2004–2018. https://doi.org/10.1007/s10803-021-05093-7
Butera CD, Harrison L, Kilroy E, et al., 2022, Relationships between alexithymia, interoception, and emotional empathy in autism spectrum disorder. Autism, 4: 571070. https://doi.org/10.1177/13623613221111310
Fletcher-Watson S, Bird G, 2020, Autism and empathy: What are the real links? Autism, 24: 3–6. https://doi.org/10.1177/1362361319883506
Khalil R, Tindle R, Boraud T, et al., 2018, Social decision making in autism: On the impact of mirror neurons, motor control, and imitative behaviors. CNS Neurosci Ther, 24: 669–676. https://doi.org/10.1111/cns.13001
Watanabe R, Kim Y, Kuruma H, et al., 2022, Imitation encourages empathic capacity toward other individuals with physical disabilities. Neuroimage, 264: 119710. https://doi.org/10.1016/j.neuroimage.2022.119710
Herscu P, Handen BL, Arnold LE, et al., 2020, The SOFIA study: Negative multi-center study of low dose fluoxetine on repetitive behaviors in children and adolescents with autistic disorder. J Autism Dev Disord, 50: 3233–3244. https://doi.org/10.1007/s10803-019-04120-y
Reddihough DS, Marraffa C, Mouti A, et al., 2019, Effect of fluoxetine on obsessive-compulsive behaviors in children and adolescents with autism spectrum disorders: A randomized clinical trial. JAMA, 322: 1561–1569. https://doi.org/10.1001/jama.2019.14685
Zhao F, Zhang H, Wang P, et al., 2022, Oxytocin and serotonin in the modulation of neural function: Neurobiological underpinnings of autism-related behavior. Front Neurosci, 16: 919890. https://doi.org/10.3389/fnins.2022.919890
Pisansky MT, Hanson LR, Gottesman II, et al., 2017, Oxytocin enhances observational fear in mice. Nat Commun, 8: 2102. https://doi.org/10.1038/s41467-017-02279-5
Festante F, Ferrari PF, Thorpe SG, et al., 2020, Intranasal oxytocin enhances EEG mu rhythm desynchronization during execution and observation of social action: An exploratory study. Psychoneuroendocrinology, 111: 104467. https://doi.org/10.1016/j.psyneuen.2019.104467
Okada N, Yahata N, Koshiyama D, et al., 2020, Neurometabolic underpinning of the intergenerational transmission of prosociality. Neuroimage, 218: 116965. https://doi.org/10.1016/j.neuroimage.2020.116965
Samuni L, Preis A, Deschner T, et al., 2019, Cortisol and oxytocin show independent activity during chimpanzee intergroup conflict. Psychoneuroendocrinology, 104: 165–173. https://doi.org/10.1016/j.psyneuen.2019.02.007