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. Author manuscript; available in PMC: 2018 May 1.
Published in final edited form as: Neurosci Biobehav Rev. 2016 Nov 4;76(Pt B):216–234. doi: 10.1016/j.neubiorev.2016.10.028

Table 1.

Examples of emotional contagion elicited by painful and fearful stimuli

Study Species (strain) Sex Demonstrator experience Observer experience Observer response Observer Pain Experience required? Familiarity required? Sensory Modality
Pain and/or restraint Li et al. 2014 Rat Subcutaneous injection with bee venom Observing the Demonstrator pain response + subcutaneous injection with bee venom Increased mechanical sensititvity and paw flinch reflex yes yes Not tested
Kavaliers et al. 2003 Mouse (CF-1) M Exposure to biting flies Observing the Demonstrator getting bit and exposure to non-biting flies on the following day Burying in the bedding while exposed to non-biting flies no no Not tested
Langford et al. 2006 Mouse (CD1) M and F Not treated Observing the pain response of the Demonstrator + 0.9% acetic acid Decrease in writhing yes yes Visual
0.9% acetic acid Increase in writhing and thermal hyperalgesia yes yes
no
1% or 5% formalin injection Observing the pain response of the Demonstrator + 1% or 5% formalin injection Decrease in paw licking in 5% f treated mice watching 1% treated mouse yes Not tested Not tested
Watanabe 2011 Mouse (c57BL/6J) M Restraint (single, group or single in the presence of cagemates Restraint or Observation of a restrained cagemate Step down in a fear conditioning (0.1mA every 1 sec) extinction trial no yes Not tested
Watanabe 2012 Mouse (c57BL/6J) M Restraint or formalin injection (hind paw) Conditioned place preference with a restrained or formalin injected cagemate in one of the chambers While restraint did not evoke conditioned place aversion (CPA), formalin injection, after a session of enhanced interest resulted with CPA. no Not tested Not tested
Watanabe 2015 Mouse (ICR) M Restraint none hyperthermia yes Not tested Not tested
Restraint cagemate No hyperthermia
Freely moving cagemate Increased hyperthermia
Martin et al. 2015 Mouse (CD-1) M 0.9% acetic acid Observing the pain response of the Demonstrator Analgesia reduced by naloxone and glucocorticoid synthesis inhibitor no Not tested
Observing the pain response of the Demonstrator + 0.9% acetic acid Pain response increased in cagemates only, glucocorticoid synthesis inhibitor enables similar reaction in strangers yes Yes (enhancement)
30 min restraint prior to observing the pain response of the Demonstrator Abolished hyperalgesia in both isolated mice and cagemates Not tested
Remote fear Knapska et al. 2006 Rat (Wistar) M Fear conditioning (9 × 1 sec, 1.3mA, 55 sec ITI) Interaction with a stressed cagemate in the home cage Increased exploration and acoustic startle response no Not tested Not tested
Knapska et al. 2010 Rat (Wistar) M Fear conditioning (9 × 1 sec, 1.3mA, 55 sec ITI) Interaction with a stressed cagemate in the home cage + avoidance training to 5 sec 1 mA shock (cue) Increased exploration and allogrooming of the Demonstrator. Improved acquisition and retention of avoidance yes Not tested Not tested
Fear conditioning (9 × 1 sec, 1.3mA, 55 sec ITI) Interaction with a stressed cagemate in the home cage + 1 sec 1 mA shock (context) Increased freezing to context yes No Not tested
Mikosz et al. 2015 Rat (Long-Evans) M and F Fear conditioning (10 × 1 sec, 1mA) Home cage interaction with a stressed cagemate Increase in social approach + better performance in two-way avoidance task no Not tested Not tested
Bredy and Barad 2009 Mouse (c57BL/6J) M Fear conditioning (3 × 2 sec, 1 mA, 120 sec ITI) Interaction with a stressed cagemate followed by fear conditioning Decreased freezing to cue yes Not tested Olfactory
Interaction with a stressed cagemate followed by fear conditioning and extinction Decreased freezing to cue (increased extinction) yes Not tested Olfactory
Fear conditioning (3 × 2 sec, 1 mA, 120 sec ITI) + 10 extinction trials Interaction with a stressed cagemate followed by fear conditioning and extinction Decreased freezing to cue (increased extinction) yes Not tested Non-olfactory
Nowak et al. 2013 Mouse (c57BL/6J) M Fear conditioning (5 × 1 sec, 0.6 mA, context A) + extinction (6 × 10 CS, context B) + test (10 CS, context B) Fear conditioning (5 × 1 sec, 0.6 mA, context A + test (10 CS, context B, tested together with the Demonstrator or separately) Animals tested together behave identically yes Not tested Not tested
Observer tested separately from the Demonstrator freezes more
Naïve + test (10 CS, context B, tested together with the Demonstrator) No freezing
Air puff to cue in the Intellicage learning unit, followed by extinction and rinstatement Air puff to cue in the Intellicage learning unit, followed by extinction Reinstatement of avoidance reaction Yes (group testing)
Meyza et al. 2015 Mouse (c57BL/6J and BTBR T+ Itpr3tf/J) M Fear conditioning (10 × 1 sec, 0.6 mA) Home cage interaction with a stressed cagemate c57: increased number and duration of social contacts, BTBR does not Not tested Not tested Not tested
Iminent fear Bruchey et al. 2010 Rat (Sprague-Dawley) M Fear conditioning (3 × 0.5 sec, 0.7 mA, 180 sec ITI) Observation of conditioned response of the Demonstrator Increased freezing to cue no Not tested Not tested
Observation of conditioned response of the Demonstrator + Fear conditioning (3 × 0.5 sec, 0.4 mA, 180 sec ITI) Increased freezing to cue yes Not tested Not tested
Naïve + Fear conditioning (3 × 0.5 sec, 0.4 mA, 180 sec ITI) Freezing yes Not tested Not tested
Kim et al. 2010 Rat (Sprague-Dawley) M Naïve or Fear conditioned (10 × 1 sec, 2 mA, 120 sec ITI) Naïve or Fear conditioned (10 × 1 sec, 2 mA, 120 sec ITI) Increased freezing to cue Yes Not tested Auditory
Atsak et al. 2011 Rat (Long Evans) F Fear conditioned (5 × 5 sec, 0.8 mA, 240 and 360 sec ITI) Naïve or Fear conditioned (4 × 1 sec, 0.8 mA, 240 and 360 sec ITI) + 1 × 1 sec 0.8mA prior to witnessing the conditioning of the Demonstrator Decrease in activity, increase in freezing (in experiences Observers) yes Not tested Not tested
none Naïve or Fear conditioned (4 × 1 sec, 0.8 mA, 240 and 360 sec ITI) + USVs from conditioning session Experienced animals freeze Auditory
Yusufishaq and Rosenkranz, 2013 Rat (Sprague-Dawley) M Fear conditioned (8 × 1 sec, 0.5–0.8 mA, 80 sec ITI) Observation of the fear conditioning session Increased freezing no Not tested but pair housed rats froze more than single housed ones Not tested
Jones et al. 2014 Rat (Sprague-Dawley) F Fear conditioning (3 × 0.5 sec, 0.7 mA, 180 sec ITI) Observation of conditioned response of the Demonstrator + cue Increased freezing to cue no Yes, familiarity enhances freezing Not tested
Carillo et al. 2015 Rat (Long Evans) M Fear conditioning 6 days of 5 × 1 sec, 1.5mA, 120–180 sec ISI Fear conditioning (4 × 1 sec, 0.8mA, 240–360 sec ISI) Observers freezing decreases (and yawning increases) with consecutive testing days. yes Not tested Not tested
Jones and Monfils 2016 Rat (Sprague-Dawley) M Fear conditioning (3 × 0.5 sec, 0.7 mA, 180 sec ITI) Observation of conditioned response of the Demonstrator + cue Subordinate individuals display stronger freezing response. Muscimol inactivation of anterior cingulate cortex disables social transfer of fear no Not tested 22 kHz USV contribute to the freezing response while 50 KHz impede social transfer of information
Chen et al. 2009 Mouse (c57BL/6J and BALB/c) M and F Fear conditioning (10 × 2 sec, 0.5 mA, 118 sec ITI) 2 sessions Observation of the fear conditioning session + exposure to cue Increased orientation towards the Demonstrator and freezing to cue Not tested but had previous shock experience no Auditory
Jeon and Shin 2011 (Jeon et al. 2010) Mouse (c57BL/6J) M or F Fear conditioning (24 × 2sec, 1mA, 10 sec ITI) Observation of the fear conditioning of the Demonstrator Increased freezing during the conditioning session and later for context No Enhanced by Visual
Sanders et al. 2013 Mouse (c57BL/6J) M and F Naïve or fear conditioned (6 × 1sec, 0.7mA, 15 sec ITI) Naïve + observation of the Demonstrator Only the previously experienced Observers froze during observation of the fear conditioning of the Demonstrator yes Not tested Not tested
Fear conditioning (6 × 1sec, 0.7mA, 15 sec ITI) + observation of the Demonstrator
Swim stress + observation of the fear conditioning of the Demonstrator
Gonzalez-Liencres et al. 2014 Mouse (c57BL/6J) M Fear conditioning (24 × 1 sec, 0.5 mA, 10 s ITI) Direct observation of the fear conditioning of the Demonstrator Enhanced freezing in pairs of familiar mice no yes Not tested
Ito et al. 2015 Mouse (129SvEv/C57BL/6N F1 hybrid) M Fear conditioning (24 × 2 sec, 1 mA, 10 s ITI) Direct observation of the fear conditioning of the Demonstrator + passive avoidance training (1sec, 0.15 mA) enhanced passive avoidance memory yes Not tested Not tested
Keum et al. 2016 Mouse (C57BL/6J, C57BL/6NTac, 129S1/SvImJ, 129S4/SvJae BTBR T(+) Itpr3(tf)/J, AKR/J, BALB/cByJ, C3H/HeJ, DBA/2J, FVB/NJ and NOD/ShiLtJ) M Fear conditioning (24 × 2sec, 1mA, 10 sec ITI) Observation of the fear conditioning of a same strain Demonstrator C57BL/6J, C57BL/6NTac, 129S1/SvImJ, 129S4/SvJae and BTBR T(+) Itpr3(tf)/J: Increased freezing during the conditioning session and later for context, AKR/J,
BALB/cByJ, C3H/HeJ, DBA/2J, FVB/NJ and NOD/ShiLtJ:
no observational fear learning
no Not tested Not tested
B6 Observers paired with B6J, 129S1 or FVB Demonstrators Display observational lfear learning