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 |