Living in a group has an adaptive value for a number of reasons. In the lab we focus on social interactions in different contexts, namely when individuals perceive a threat or when they are foraging for food. The neural mechanisms by which animals use social information to detect impending danger are largely unknown. We are studying how animals use defence behaviours of con-specifics as alarm cues. In addition, we study how the social context modulates defence behaviours. For example, we are studying how the presence of offspring affects defence behaviours displayed by mothers. We are also studying prosocial behaviour of rats using food foraging tasks. Here we would like to understand what drives an animal to coordinate with another or to perform an action that benefits another in the absence of self-benefit. To understand the mechanisms by which social interactions shape behaviour we use a combination of behavioural, pharmacological and optogenetic tools in rats and fruit flies.

Neural Mechanisms of trace auditory fear conditioning

This project focuses on the role of different memory systems in trace auditory fear conditioning (tAFC). Our aim is to unravel how the association between two stimuli separated in time is formed in the brain. Preliminary findings led us to hypothesize that the strategy used by the rats to learn the association between tone and shock depends on the length of the trace interval between the two stimuli. In accordance with these results we found that temporary inactivation of the hippocampus affects tAFC only when long trace intervals are used. In contrast, inactivation of either the medial prefrontal cortex (mPFC), thought to be important for working memory, or the amygdala, important for fear learning, disrupts learning irrespective of interval length. We have begun to test the role of mPFC –amygdala and mPFC-hippocampus connections in the acquisition tAFC with both short and long trace intervals.

Cooperation in social dilemmas in rats

Game theory has constituted a powerful tool in the study of the mechanisms of reciprocity. Having shown, in a Prisoner’s Dilemma game, that rats shape their behaviour according to the opponent’s strategy and the relative size of the payoff resulting from cooperative or defective moves, we now aim at dissecting the mechanisms underlying the decision-making process during such social dilemma games. We have designed and set-up an automated maze to study the behavior of rats in different social dilemma games, such as the Stag Hunt and the Snow drift game, which allow for dissection of the factors that govern cooperation between two rats.

Mechanism of vicarious fear

This project aims at investigating the mechanisms underlying vicarious fear in rats. It has been shown that rats can learn from social interactions, however the mechanisms underlying this form of learning are poorly understood. In this project we are focusing on social transmission of fear. In collaboration with Dr. Christian Keysers, we have developed a paradigm for studying vicarious fear in rats. We have found that a rat will show vicarious fear when observing a con-specific being shocked, provided that it has had prior experience with shock. This finding suggests that vicarious freezing in rats is empathic in nature. Furthermore, we found that the rat being shocked will freeze more in the presence of an experienced observer than in the presence of a naïve one and that the amount of freezing is correlated with the number of alarm calls emitted by the two rats.

Neural Mechanisms of discriminative auditory fear conditioning

This project aims at elucidating the role of the different auditory input pathways to the amygdala, a crucial structure for the acquisition of auditory fear conditioning. To this end we are performing lesions to each of these pathways and testing their role in the acquisition and expression of discriminative auditory fear. Previously we had found that both input pathways are necessary for intact auditory discrimination, in the context of fear learning. Thus, although either one alone is sufficient for the acquisition of fear of a sound, neither one can establish normal discrimination between a tone that is followed by shock and one that is not. Next, we tested the role of the two pathways in the recall of discriminative fear and found that only the direct thalamic, but not the cortical, projection to the amygdala was important for normal expression of discriminative fear. Finally, we found that the same thalamic pathway was important for the recall of fear extinction, suggesting a role of this pathway in the suppression of fear of neutral or safe auditory stimuli.

Marta Moita, PhD
Principal Investigator
marta.moita@neuro.fchampalimaud.org

Biography

Andreia Cruz, PhD
Postdoctoral Researcher
andreia.cruz@neuro.fchampalimaud.org

Anna Hobbiss, PhD
Postdoctoral Researcher
anna.hobbiss@neuro.fchampalimaud.org

Catarina Mendes
Technician
catarina.mendes@neuro.fchampalimaud.org

Clara Ferreira, PhD
Postdoctoral Researcher
clara.ferreira@neuro.fchampalimaud.org

Matheus Farias
2017 INDP PhD Student
matheus.farias@neuro.fchampalimaud.org

Mirjam Heinemans
2017 INDP PhD Student
mirjam.heinemans@research.fchampalimaud.org

Natalia Barrios, PhD
Postdoctoral Researcher
natalia.barrios@neuro.fchampalimaud.org

Ricardo Neto Silva, PhD
Postdoctoral Researcher
ricardo.silva@neuro.fchampalimaud.org

Ricardo Zacarias, PhD
Postdoctoral Researcher
ricardo.zacarias@neuro.fchampalimaud.org

Sofia Silva
Research Technician
sofia.silva@research.fchampalimaud.org

Lab Administration

António Raposo
Lab Administrator
antonio.raposo@research.fchampalimaud.org

PhD Student

Scott Rennie, PhD
INDP Alumni
scott.rennie@neuro.fchampalimaud.org

Zacarias R; Namiki S; Card G; Vasconcelos ML; Moita MA (2018) Speed dependent descending control of innate freezing behavior in Drosophila melanogaster Nat Commun (doi:10.1038/s41467-018-05875-1)

Rickenbacher E, Perry RE, Sullivan RM, Moita MA. (2017) Freezing suppression by oxytocin in central amygdala allows alternate defensive behaviours and mother-pup interactions. eLife 6 , pii: e24080. (doi:10.7554/eLife.24080)

Márquez C, Rennie SM, Costa DF, Moita MA (2015) Prosocial Choice in Rats Depends on Food-Seeking Behavior Displayed by Recipients. Curr. Biol. S0960-9822 (15), (in press) (doi:10.1016/j.cub.2015.05.018)

Rennie SM, Moita MM, Mainen ZF. (2013) Social cognition in the rodent: nothing to be sniffed at. Trends Cogn Sci. (doi:10.1016/j.tics.2013.04.011)

Pereira AG, Cruz A, Lima SQ, Moita MA. (2012) Silence resulting from the cessation of movement signals danger Curr. Biol. 22 (16), R627-R628 (doi:10.1016/j.cub.2012.06.015)

Guimarãis M, Gregório A, Cruz A, Guyon N, Moita MA (2011) Time determines the neural circuit underlying associative fear learning. Front Behav Neurosci 5 (89) (doi:10.3389/fnbeh.2011.00089)

Atsak P, Orre M, Bakker P, Cerliani L, Roozendaal B, Gazzola V*, Moita M* and Keysers C (2011) Experience Modulates Vicarious Freezing in Rats: A Model for Empathy. PLoS ONE 6 (7), e21855 (doi:10.1371/journal.pone.0021855)

Antunes R, Moita MA (2010) Discriminative auditory fear learning requires both tuned and nontuned auditory pathways to the amygdale. J. Neurosci. 30 (29), 9782-7 (doi:10.1523/JNEUROSCI.1037-10.2010.)

Viana DS, Gordo I, Sucena E, Moita MA (2010) Cognitive and motivational requirements for the emergence of cooperation in a rat social game. PLoS ONE 5 (1) (doi:20084113)

Blair HT, Sotres-Bayon F, Moita MAP, LeDoux JE (2005) The lateral amygdala processes the value of conditioned and unconditioned aversive stimuli Neuroscience 133 (2), 561-569 (doi:10.1016/j.neuroscience.2005.02.043)

Moita MA, Rosis S, Zhou Y, LeDoux JE, Blair HT (2004) Putting fear in its place: remapping of hippocampal place cells during fear conditioning. J. Neurosci. 24 (31), 7015-7023

Blair HT, Tinkelman A, Moita MAP, LeDoux JE (2003) Associative plasticity in neurons of the lateral amygdala during auditory fear conditioning. , 985

Moita MA, Rosis S, Zhou Y, LeDoux JE, Blair HT (2003) Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37 (3), 485-497

Moita MAP, Lamprecht R, Nader K & LeDoux JE (2002) Anchoring of PKA onto AKAP proteins in the amygdala is necessary for the consolidation of auditory fear memories. Nat. Neurosci. 5 (9), 837-8

de Bruin JP, Moita MP, de Brabander HM, Joosten RN (2001) Place and Response Learning of Rats in a Morris Water Maze: Differential Effects of Fimbria Fornix and Medial Prefrontal Cortex Lesions. Neurobiol Learn Mem 75 (2), 164-78