Group leader: Valérie Doyère

Memory, Emotion & Time

In brief

The team’s projects are oriented towards understanding the neural networks and the mechanisms underlying the formation and updating of associative memory, with a special focus on the temporal component which controls the anticipatory aspect of behavior and is fundamental for error detection and learning.

We focus on a large interconnected network formed by the amygdala, the hippocampus, the prefrontal cortex (PFC) and the striatum. The network of interest may constitute a functional connectome, at the service of integrative functions, such as memory and timing, itself involving working memory and long-term memory processes, and their distortions by emotion, whether positive or negative. We follow two main strategies:
(1) Deciphering the neuronal correlates of interval timing at different stages of learning, and analyzing the impact of the disruption of network functioning
(2) Assessing the impact of altering network function on timing and emotional memory at different moments during post-natal development until adulthood
The methodology used is based on the complementarity of pharmacological, molecular, electrophysiology (in vivo and ex vivo), and behavioral techniques in rats.

Our team is associated with the doctoral school ED419 Bio-sigNE of the University Paris-Saclay.

Selected publications

  • Kononowicz T, van Wassenhove V & Doyère V (2022) Rodents monitor their error in self-generated duration on a single trial basis. PNAS, 119(9): e2108850119. doi: 10.1073/pnas.2108850119. hal-03587286v1. CNRS press release: rats can estimate their timing accuracy. Highlight in Nature: 10.1038/d41586-022-00490-z. Commentary in PNAS by F. Balci: 10.1073/pnas.2201001119
  • Joly F, Jeckel P, Griebel M, Raut S, El Massioui N, Vaillend C, Johnson L, Volkmer H & Doyère V (2022) Disruption of amygdala Tsc2 in adolescence leads to changed prelimbic cellular activity and generalized fear responses at adulthood in rats. Cerebral Cortex. doi: 10.1093/cercor/bhab506 hal-03582450v1
  • Tallot L & Doyère V (2020). Neural encoding of time in the animal brain. Neuroscience and Biobehavioral Revew. DOI: 10.1016/j.neubiorev.2019.12.033
  • Bossi S, Romain Helleringer, Micaela Galante, Ester Monlleó, Ana Trapero, Xavier Rovira, Hervé Daniel, Amadeu Llebaria, Heather McLean (2018). A Light-Controlled Allosteric Modulator Unveils a Role for mGlu4 Receptors During Early Stages of Ischemia in the Rodent Cerebellar Cortex. Frontiers in Cellular Neuroscience, 12:449. DOI: 10.3389/fncel.2018.00449
  • Scholler P, Damien Nevoltris, Dimitri de Bundel, Simon Bossi, David Moreno-Delgado, Xavier Rovira , Thor C. Møller , Driss El Moustaine, Michaël Mathieu, Emilie Blanc, Heather McLean, Elodie Dupuis, Gérard Mathis, Eric Trinquet, Hervé Daniel, Emmanuel Valjent, Daniel Baty, Patrick Chames, Philippe Rondard, Jean-Philippe Pin (2018). Allosteric nanobodies uncover a role of hippocampal mGlu2 receptor homodimers in contextual fear consolidation. Nature Communication, DOI: 10.1038/s41467-017-01489-1
  • Dallérac G, Graupner M, Knippenberg J, Chacon Ruiz Martinez R, Ferreira Tavares T, Tallot L, El Massioui N, Verschueren A, Höhn S, > Boulanger Bertolus J, Reyes A, LeDoux J, Schafe G, Diaz-Mataix L, Doyère V (2017). Updating Temporal Expectancy of an Aversive Event Engages Striatal Plasticity under Amygdala Control. Nature Communication, 8:13920. DOI: 10.1038/ncomms13920

Team leader

Members

Peer-reviewed Articles

2023

• Tavares TF, Bueno JLO & Doyère V (2023) Temporal prediction error triggers amygdala-dependent memory updating in appetitive operant conditioning in rats. Front Behav Neurosci, 16:1060587. 10.3389/fnbeh.2022.1060587. hal-04170284v1.

• Fuat Balci, Suliann Ben Hamed, Thomas Boraud, Sébastien Bouret, Thomas Brochier, et al.. A response to claims of emergent intelligence and sentience in a dish. Neuron, 2023, 111 (5), pp.604-605. doi: 10.1016/j.neuron.2023.02.009. hal-04012408.

• Sloane Paulcan, Anne Giersch, Virginie van Wassenhove, Valérie Doyère. Temporal order processing in rats depends on the training protocol.. Journal of Experimental Psychology: Animal Learning and Cognition, 2023, 49 (1), pp.31-45. doi: 10.1037/xan0000347. hal-04170258.

2022

• Lisa Saleille, Lucille Tallot, Bruce L. Brown, Sylvia Wirth, Valérie Doyère. Gap in the conditioned stimulus: Differential impacts on temporal expectancy in appetitive and aversive conditions in rats. Behavioural Processes, 2022, 203, pp.104762. doi: 10.1016/j.beproc.2022.104762. hal-03939548.

• Kononowicz T, van Wassenhove V & Doyère V (2022) Rodents monitor their error in self-generated duration on a single trial basis. PNAS, 119(9): e2108850119. doi: 10.1073/pnas.2108850119. hal-03587286v1. CNRS press release: rats can estimate their timing accuracy. Highlight in Nature: 10.1038/d41586-022-00490-z. Commentary in PNAS by F. Balci: 10.1073/pnas.2201001119

• Joly F, Jeckel P, Griebel M, Raut S, El Massioui N, Vaillend C, Johnson L, Volkmer H & Doyère V (2022) Disruption of amygdala Tsc2 in adolescence leads to changed prelimbic cellular activity and generalized fear responses at adulthood in rats. Cerebral Cortex. doi: 10.1093/cercor/bhab506 hal-03582450v1

2021

• Derouet J, Droit-Volet S & Doyère V (2021) Asymmetry in updating long-term memory for time. Learning & Memory, 28:40-43. doi: 10.1101/lm.051789.120 hal-03123433v1

• Boulanger-Bertolus J, Parrot S, Doyère V & Mouly AM (2021) Dorsal striatum and the temporal expectancy of an aversive event in Pavlovian odor fear conditioning. Neurobiology of Learning and Memory, 182:107446. doi: 10.1016/j.nlm.2021.107446 hal-03236119

2020

• Lamirault C, Nguyen HP, Doyère V & El Massioui N (2020) Age-related alteration of emotional regulation in the BACHD rat model of Huntington disease. Genes, Brain & Behav. 19(5):e12633. doi: 10.1111/gbb.12633 hal-02465769v1

• Tallot L, Graupner M, Diaz-Mataix L & Doyère V (2020) Beyond freezing: Temporal expectancy of an aversive event engages the amygdalo-prefronto-dorsostriatal network. Cerebral Cortex, 30(10):5257-5269. doi: 10.1093/cercor/bhaa100 hal-02912527v1

• Tallot L & Doyère V (2020) – Neural encoding of time in the animal brain. Neurosci Biobehav Rev. 115:146-163. doi: 10.1016/j.neubiorev.2019.12.033. hal-02912685v1

• Lamirault C, Doyère V, Juchaux M, Pouzoulet F, Patriarca A, Nauraye C, El Massioui N & Prezado Y (2020) Short and long term evaluation of the impact of proton minibeam radiation therapy on motor, emotional and cognitive functions. Scientific Reports, 10:13511. doi: 10.1038/s41598-020-70371-w hal-pasteur-02916038v1

• Araiba S, El Massioui N, Brown BL & Doyère V (2020) – Non-symmetrical effects in the temporal bisection after selective food devaluation in rats. Behav. Process., 180:104244. doi: 10.1016/j.beproc.2020.104244 hal-02974316v1

• Dupin M, Garcia S, Messaoudi B, Doyère V & Mouly A-M (2020) Respiration and brain neural dynamics associated with interval timing during odor fear learning in rats. Scientific Reports, 10:17643. doi: 10.1038/s41598-020-74741-2 hal-02992673v1

2019

• The Disruption of Memory Consolidation of Duration Introduces Noise While Lengthening the Long-Term Memory Representation of Time in Humans. Derouet J, Doyère V, Droit-Volet S (2019) Frontiers in Psychology, 10:745. doi : 10.3389/fpsyg.2019.00745

• The Strength of Alpha-Beta Oscillatory Coupling Predicts Motor Timing Precision. Grabot L, Kononowicz TW, Dupré la Tour T, Gramfort A, Doyère V, van Wassenhove V (2019) Journal of Neuroscience, 24 ;39(17):3277-3291. doi : 10.1523/JNEUROSCI.2473-18.2018 Epub 2019 Feb 21.

• Malet-Karas A, Noulhiane M & Doyère V (2019) Dynamics of spatio-temporal binding in rats. Timing & Time Perception, 7(1):27-47. doi: 10.1163/22134468-20181124 hal-02194906

2018

• Araiba S., El Massioui N., Brown B.L., Doyère V. (2018) Duration-specific effects of outcome devaluation in temporal control are differentially sensitive to amount of training. Learning & Memory, 25, 629-633. 10.1101/lm.047878.118

• Garces D, El Massioui N, Lamirault C, Riess O, Nguyen HP, Brown BL, Doyère V (2018) The alteration of emotion regulation precedes the deficits in interval timing in the BACHD rat model for Huntington’s disease. Frontiers in Integrative Neurosciences. 9:12-14. doi: 10.3389/fnint.2018.00014

2017

• Non-linear auto-regressive models for cross-frequency coupling in neural time series. Dupré la Tour T, Tallot L, Grabot L, Doyère V, van Wassenhove V, Grenier Y, Gramfort A (2017). PLoS Comput Biol 13(12) : e1005893. bioRxiv (2017). doi : 10.1371/journal.pcbi.1005893

• Dissociation between decision-making under risk and decision-making under ambiguity in premanifest and manifest patients with Huntington’s disease. Adjeroud N, Besnard J, Prudean A, Scherer C, Gohier B, Bonneau D, Verny C, El Massioui N & Allain P (2017) Neuropsychologia, 103:87-95. doi: 10.1016/j.neuropsychologia.2017.07.011

• Updating Temporal Expectancy of an Aversive Event Engages Striatal Plasticity under Amygdala Control. Dallérac G, Graupner M, Knippenberg J, Chacon Ruiz Martinez R, Ferreira Tavares T, Tallot L, El Massioui, Verschueren A, Höhn S, Boulanger Bertolus J, Reyes A, LeDoux J, Schafe G, Diaz-Mataix L & Doyère V (2017) Nature Communication. 8:13920. doi: 10.1038/ncomms13920

• Altered reactivity of central amygdala to GABAAR antagonist in the BACHD rat model of Huntington disease. Lamirault C, Yu-Taeger L, Doyère V, Riess O, Nguyen H & El Massioui N. (2017) Neuropharmacology, 123:136-147. doi: 10.1016/j.neuropharm.2017.05.032

• Updating of aversive memories after temporal error detection is differentially modulated by mTOR across development. Tallot L, Diaz-Mataix L, Perry RE, Wood K, LeDoux JE, Mouly AM, Sullivan RM & Doyère V. (2017) Learning & Memory, 24(3):115-122. doi: 10.1101/lm.043083.116

2016

• Theory of Mind and Empathy in Preclinical and Clinical Huntington’s Disease. Adjeroud N, Besnard J, El Massioui N, Verny C, Prudean A, Scherer C, Gohier B, Bonneau D & Allain P (2016) Social Cognitive and Affective Neuroscience, 1-11. doi: 10.1093/scan/nsv093

• A subcortical circuit for time & action : insights from animal research. Doyère Valérie & El Massioui Nicole (2016) Current Opinion in Behavioral Sciences, Issue “Interval Timing and Skill Learning : The Multisensory Representation of Time and Action”, doi: 10.1016/j.cobeha.2016.02.008

• Impaired decision making and loss of inhibitory-control in early symptomatic tgHD rats, model of Huntington disease. El Massioui N, Lamirault C, Yagüe S, Adjeroud N, Garces D, Maillard A, , Tallot L, Yu-Taeger L, Samson N, von Hörsten S, Riess O, Nguyen HP, Allain P & Doyère V (2016) Frontiers in Behavioral Neuroscience. 10:204. doi: 10.3389/fnbeh.2016.00204

• The amygdalo-nigro-striatal network is critical for an optimal temporal performance. Es-seddiqi M, El Massioui N, Desvignes N, Brown BL & Doyère V (2016) Learning & Memory, 23(3):104-7. doi: 10.1101/lm.041152.115

• Impulsivity trait in the early symptomatic BACHD transgenic rat model of Huntington Disease. Manfré G, Doyère V, Bossi S, Riess O, Nguyen HP & El Massioui N (2016). Behavioral Brain Research, 299:6-10. doi: 10.1016/j.bbr.2015.11.007

• Developmental emergence of fear/threat learning : neurobiology, associations and timing. Tallot L, Doyère V & Sullivan RM. (2016) Genes Brain Behavior, 15(1):144-54. doi: 10.1111/gbb.12261

• Individual trial analysis evidences clock and non-clock based conditioned suppression behaviors in rats. Tallot L, Capela D, Brown BL & Doyère V. (2016) Behavioral Processes, 124:97-107. doi: 10.1016/j.beproc.2016.01.003

2015

• Reduced impact of emotion on choice behavior in presymptomatic BACHD rats, a transgenic rodent model for Huntington Disease. Adjeroud N, Yagüe S, Yu-Taeger L, Bozon B, Leblanc-Veyrac P, Riess O, Allain A, Nguyen H, Doyère V & El Massioui N (2015) Neurobiology of Learning and Memory, 125 : 249–257. doi: 10.1016/j.nlm.2015.10.003

• Cognitive dysfunction in the dystrophin-deficient mouse model of Duchenne Muscular Dystrophy : A reappraisal from sensory to executive processes. Chaussenot R, Edeline JM, Le Bec B, El Massioui N, Laroche S & Vaillend C (2015) Neurobiology Learning Memory, 124:111-22. doi: 10.1016/j.nlm.2015.07.006

2014

• Infant rats can learn time intervals before the maturation of the striatum : evidence from odor fear conditioning. Boulanger Bertolus J, Hegoburu C, Ahers JL, Londen E, Rousselot J, Szyba K, Thévenet M, Sullivan-Wilson TA, Doyère V, Sullivan RM & Mouly AM. (2014) Frontiers Behavioral Neuroscience, 8:176.
• Memory consolidation for duration. Cocenas-Silva R, Bueno JL, Doyère V & Droit-Volet S. (2014) Quarterly Journal Experimental Psychology (Hove), 67(7):1401-14.
• The amygdala : a potential player in timing CS-US intervals. Díaz-Mataix L, Tallot L & Doyère V. (2014) Behavioral Processes, 101:112-22.
• Multiple spine boutons are formed after long-lasting LTP in the awake rat. Medvedev NI, Dallérac G, Popov VI, Rodriguez Arellano JJ, Davies HA, Kraev IV, Doyère V & Stewart MG. (2014) Brain Structure Function, 219(1):407-14.
• Disrupted sensorimotor synchronization, but intact rhythm discrimination, in children treated for a cerebellar medulloblastoma. Provasi J, Doyère V, Zélanti PS, Kieffer V, Perdrix H, El Massioui N, Brown BL, Dellatolas G, Grill J & Droit-Volet S (2014) Research in Developmental Disabilities, 35 : 2053-2068.

2013

• Cerebellar deep nuclei involvement in cognitive adaptation and automaticity. Callu D, Lopez J & El Massioui N (2013) Learning & Memory, 20:344-347.
• NCAM function in the adult brain : lessons from mimetic peptides and therapeutic potential. Dallérac G, Rampon C & Doyère V. (2013) Neurochemical Research, 38(6):1163-73.
• The selectivity of aversive memory reconsolidation and extinction processes depends on the initial encoding of the Pavlovian association. Debiec J, Diaz-Mataix L, Bush DE, Doyère V & LeDoux JE. (2013) Learning & Memory, 20(12):695-9.
• Detection of a temporal error triggers reconsolidation of amygdala-dependent memories. Díaz-Mataix L, Ruiz Martinez RC, Schafe GE, LeDoux JE & Doyère V. (2013) Current Biology, 23(6):467-72.
• Time perception in children treated for a cerebellar medulloblastoma. Droit-Volet S, Zélanti P, Dellatolas G, Kieffer V, El Massioui N, Brown BL, Doyère V, Provasi J & Grill J (2013). Research in Developmental Disabilities, 34(1):480-494.
• Modified impact of emotion on temporal discrimination in a transgenic rat model of Huntington disease. Faure A, Es-seddiqi M, Brown BL, Nguyen H, Riess O, von Hörsten S, Le Blanc P, Desvignes N, El Massioui N & Doyère V (2013) Frontiers in Behavioral Neurosciences, 7 : 130-138.
• A naturally-occurring histone acetyltransferase inhibitor derived from Garcinia indica impairs newly acquired and reactivated fear memories. Maddox SA, Watts CS, Doyère V & Schafe GE. (2013) PLoS One, 8(1):e54463.
• It’s time to fear ! Interval timing in odor fear conditioning in rats. Shionoya K, Hegoburu C, Brown BL, Sullivan RM, Doyère V & Mouly AM. (2013). Frontiers Behavioral Neurosciences, 27 ;7:128.

2012

• Interval timing and time-based decision making. Meck WH, Doyère V & Gruart A. (2012) Frontiers Integrative Neurosciences, 6:13.

2011

• Temporal sensitivity changes with extended training in a bisection task in a transgenic rat model. Brown BL, Höhn S, Faure A, von Hörsten S, Le Blanc P, Desvignes N, El Massioui N & Doyere V. (2011). Frontiers in Integrative Neuroscience, 5:44.
• The neural cell adhesion molecule-derived peptide FGL facilitates long-term plasticity in the dentate gyrus in vivo. Dallérac G, Zerwas M, Novikova T, Callu D, Leblanc-Veyrac P, Bock E, Berezin V, Rampon C & Doyère V. (2011) Learning & Memory, 18(5):306-13.
• Sensory-specific associations stored in the lateral amygdala allow for selective alteration of fear memories. Díaz-Mataix L, Debiec J, LeDoux JE & Doyère V. (2011) Journal of Neuroscience, 31(26):9538-43.
• Altered emotional and motivational processing in the transgenic rat model for Huntington’s disease. Faure A, Höhn S, von Hörsten S, Delatour B, Doyère V & El Massioui N (2011) Neurobiology of Learning and Memory, 95(1):92-101.
• Behavioral and in vivo electrophysiological evidence for presymptomatic alteration of prefronto-striatal processing in the transgenic rat model for Huntington’s disease. Höhn S, Dallérac G, Faure A, Nguyen HHP, Riess O, von Hörsten S, Le Blanc P, Desvignes N, El Massioui N, Brown BL & Doyère V (2011) Journal of Neuroscience, 31(24):8986-97.

2010

• The amygdala encodes specific sensory features of an aversive reinforcer. Debiec J, Díaz-Mataix L, Bush DE, Doyère V & Ledoux JE. (2010) Nature Neuroscience, 13(5):536-7.
• Dopamine agonists increase perseverative instrumental responses but do not restore habit formation in a rat model of Parkinsonism. Faure A, Leblanc-Veyrac P & El Massioui N (2010) Neuroscience, 168(2):477-86.
• Alterations in synaptic curvature in the dentate gyrus following induction of long-term potentiation, long-term depression, and treatment with the N-methyl-D-aspartate receptor antagonist CPP. Medvedev NI, Popov VI, Dallérac G, Davies HA, Laroche S, Kraev IV, Rodriguez Arellano JJ, Doyère V & Stewart MG. (2010) Neuroscience, 171(2):390-7.
• Asymmetries in long-term and short-term plasticity at thalamic and cortical inputs to the amygdala in vivo. Siguròsson T, Cain CK, Doyère V & LeDoux JE (2010) European Journal of Neuroscience, 31(2):250-62.