Physical Address
304 North Cardinal St.
Dorchester Center, MA 02124
Schwabe, L. & Wolf, O. T. Stress prompts habit behavior in humans. J. Neurosci. 29, 7191–7198 (2009).
Google Scholar
Pool, E. R. et al. Determining the effects of training duration on the behavioral expression of habitual control in humans: a multilaboratory investigation. Learn. Mem. 29, 16–28 (2022).
Google Scholar
Friedel, E. et al. How accumulated real life stress experience and cognitive speed interact on decision-making processes. Front. Hum. Neurosci. 11, 302 (2017).
Google Scholar
Schwabe, L., Dalm, S., Schächinger, H. & Oitzl, M. S. Chronic stress modulates the use of spatial and stimulus-response learning strategies in mice and man. Neurobiol. Learn. Mem. 90, 495–503 (2008).
Google Scholar
Dias-Ferreira, E. et al. Chronic stress causes frontostriatal reorganization and affects decision-making. Science 325, 621–625 (2009).
Google Scholar
Balleine, B. W. The meaning of behavior: discriminating reflex and volition in the brain. Neuron 104, 47–62 (2019).
Google Scholar
Graybiel, A. M. Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 31, 359–387 (2008).
Google Scholar
Dickinson, A. Actions and habits: the development of behavioural autonomy. Phil. Trans. R. Soc.Lond. B 308, 67–78 (1985).
Google Scholar
Redish, A. D., Jensen, S. & Johnson, A. A unified framework for addiction: vulnerabilities in the decision process. Behav. Brain Sci. 31, 415–437; discussion 437–487 (2008).
Google Scholar
Vandaele, Y. & Ahmed, S. H. Habit, choice, and addiction. Neuropsychopharmacology 46, 689–698 (2021).
Google Scholar
Voon, V. et al. Disorders of compulsivity: a common bias towards learning habits. Mol. Psychiatry 20, 345–352 (2015).
Google Scholar
Belin, D., Belin-Rauscent, A., Murray, J. E. & Everitt, B. J. Addiction: failure of control over maladaptive incentive habits. Curr. Opin. Neurobiol. 23, 564–572 (2013).
Google Scholar
Hogarth, L., Balleine, B. W., Corbit, L. H. & Killcross, S. Associative learning mechanisms underpinning the transition from recreational drug use to addiction. Ann. N. Y. Acad. Sci. 1282, 12–24 (2013).
Google Scholar
Ray, L. A. et al. Capturing habitualness of drinking and smoking behavior in humans. Drug Alcohol Depend. 207, 107738 (2020).
Google Scholar
Gillan, C. M. et al. Disruption in the balance between goal-directed behavior and habit learning in obsessive-compulsive disorder. Am. J. Psychiatry 168, 718–726 (2011).
Google Scholar
Horstmann, A. et al. Slave to habit? Obesity is associated with decreased behavioural sensitivity to reward devaluation. Appetite 87, 175–183 (2015).
Google Scholar
Morris, R. W., Cyrzon, C., Green, M. J., Le Pelley, M. E. & Balleine, B. W. Impairments in action–outcome learning in schizophrenia. Transl. Psychiatry 8, 54 (2018).
Google Scholar
Griffiths, K. R., Morris, R. W. & Balleine, B. W. Translational studies of goal-directed action as a framework for classifying deficits across psychiatric disorders. Front. Syst. Neurosci. 8, 101 (2014).
Google Scholar
Byrne, K. A., Six, S. G. & Willis, H. C. Examining the effect of depressive symptoms on habit formation and habit-breaking. J. Behav. Ther. Exp. Psychiatry 73, 101676 (2021).
Google Scholar
Alvares, G. A., Balleine, B. W. & Guastella, A. J. Impairments in goal-directed actions predict treatment response to cognitive-behavioral therapy in social anxiety disorder. PLoS ONE 9, e94778 (2014).
Google Scholar
Alvares, G. A., Balleine, B. W., Whittle, L. & Guastella, A. J. Reduced goal-directed action control in autism spectrum disorder. Autism Res. 9, 1285–1293 (2016).
Google Scholar
Agid, O., Kohn, Y. & Lerer, B. Environmental stress and psychiatric illness. Biomed. Pharmacother. 54, 135–141 (2000).
Google Scholar
Baumeister, D., Lightman, S. L. & Pariante, C. M. The interface of stress and the HPA axis in behavioural phenotypes of mental illness. Curr. Top. Behav. Neurosci. 18, 13–24 (2014).
Google Scholar
Brady, K. T. & Sinha, R. Co-occurring mental and substance use disorders: the neurobiological effects of chronic stress. Am. J. Psychiatry 162, 1483–1493 (2005).
Google Scholar
Duffing, T. M., Greiner, S. G., Mathias, C. W. & Dougherty, D. M. Stress, substance abuse, and addiction. Curr. Top. Behav. Neurosci. 18, 237–263 (2014).
Google Scholar
Malvaez, M. & Wassum, K. Regulation of habit formation in the dorsal striatum. Curr. Opin. Behav. Sci. 20, 67–74 (2018).
Google Scholar
Balleine, B. W. & O’Doherty, J. P. Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 35, 48–69 (2010).
Google Scholar
Yin, H. H., Ostlund, S. B., Knowlton, B. J. & Balleine, B. W. The role of the dorsomedial striatum in instrumental conditioning. Eur. J. Neurosci. 22, 513–523 (2005).
Google Scholar
Balleine, B. W., Killcross, A. S. & Dickinson, A. The effect of lesions of the basolateral amygdala on instrumental conditioning. J. Neurosci. 23, 666–675 (2003).
Google Scholar
Pan, W. X., Mao, T. & Dudman, J. T. Inputs to the dorsal striatum of the mouse reflect the parallel circuit architecture of the forebrain. Front. Neuroanat. 4, 147 (2010).
Google Scholar
Gowrishankar, R. et al. Endogenous opioid dynamics in the dorsal striatum sculpt neural activity to control goal-directed action. Preprint at BioRxiv https://doi.org/10.1101/2024.05.20.595035 (2024).
Lingawi, N. W. & Balleine, B. W. Amygdala central nucleus interacts with dorsolateral striatum to regulate the acquisition of habits. J. Neurosci. 32, 1073–1081 (2012).
Google Scholar
Swanson, L. W. & Petrovich, G. D. What is the amygdala? Trends Neurosci. 21, 323–331 (1998).
Google Scholar
Wall, N. R., De La Parra, M., Callaway, E. M. & Kreitzer, A. C. Differential innervation of direct- and indirect-pathway striatal projection neurons. Neuron 79, 347–360 (2013).
Google Scholar
Heaton, E. C., Seo, E. H., Butkovich, L. M., Yount, S. T. & Gourley, S. L. Control of goal-directed and inflexible actions by dorsal striatal melanocortin systems, in coordination with the central nucleus of the amygdala. Prog. Neurobiol. 238, 102629 (2024).
Google Scholar
Moscarello, J. M. & Penzo, M. A. The central nucleus of the amygdala and the construction of defensive modes across the threat-imminence continuum. Nat. Neurosci. 25, 999–1008 (2022).
Google Scholar
Roozendaal, B., McEwen, B. S. & Chattarji, S. Stress, memory and the amygdala. Nat. Rev. Neurosci. 10, 423–433 (2009).
Google Scholar
Dickinson, A. D., Nicholas, J. & Adams, C. D. The effect of the instrumental training contingency on susceptibility to reinforcer devaluation. Q. J. Exp. Psychol. 35, 35–51 (1983).
Google Scholar
Adams, C. D. & Dickinson, A. Instrumental responding following reinforcer devaluation. Q. J. Exp. Psychol. 33, 109–121 (1981).
Google Scholar
Hammond, L. J. The effect of contingency upon the appetitive conditioning of free-operant behavior. J. Exp. Anal. Behav. 34, 297–304 (1980).
Google Scholar
Malvaez, M. et al. Habits are negatively regulated by histone deacetylase 3 in the dorsal striatum. Biol. Psychiatry 84, 383–392 (2018).
Google Scholar
Gremel, C. M. & Costa, R. M. Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions. Nat. Commun. 4, 2264 (2013).
Google Scholar
Alexander, G. M. et al. Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 63, 27–39 (2009).
Google Scholar
Zhu, H. et al. Cre-dependent DREADD (Designer Receptors Exclusively Activated by Designer Drugs) mice. Genesis 54, 439–446 (2016).
Google Scholar
Amaya, K. A. et al. Habit learning shapes activity dynamics in the central nucleus of the amygdala. Preprint at BioRxiv https://doi.org/10.1101/2024.02.20.580730 (2024).
Tipps, M., Marron Fernandez de Velasco, E., Schaeffer, A. & Wickman, K. Inhibition of pyramidal neurons in the basal amygdala promotes fear learning. eNeuro 5, ENEURO.0272-18.2018 (2018).
Tuscher, J. J., Taxier, L. R., Fortress, A. M. & Frick, K. M. Chemogenetic inactivation of the dorsal hippocampus and medial prefrontal cortex, individually and concurrently, impairs object recognition and spatial memory consolidation in female mice. Neurobiol. Learn. Mem. 156, 103–116 (2018).
Google Scholar
Corbit, L. H., Leung, B. K. & Balleine, B. W. The role of the amygdala-striatal pathway in the acquisition and performance of goal-directed instrumental actions. J. Neurosci. 33, 17682–17690 (2013).
Google Scholar
Ostlund, S. B. & Balleine, B. W. Differential involvement of the basolateral amygdala and mediodorsal thalamus in instrumental action selection. J. Neurosci. 28, 4398–4405 (2008).
Google Scholar
Fisher, S. D., Ferguson, L. A., Bertran-Gonzalez, J. & Balleine, B. W. Amygdala–cortical control of striatal plasticity drives the acquisition of goal-directed action. Curr. Biol. 30, 4541–4546.e5 (2020).
Google Scholar
Namburi, P. et al. A circuit mechanism for differentiating positive and negative associations. Nature 520, 675–678 (2015).
Google Scholar
Tye, K. M. Neural circuit motifs in valence processing. Neuron 100, 436–452 (2018).
Google Scholar
Balleine, B. W. & Killcross, S. Parallel incentive processing: an integrated view of amygdala function. Trends Neurosci. 29, 272–279 (2006).
Google Scholar
Ugolini, A., Sokal, D. M., Arban, R. & Large, C. H. CRF1 receptor activation increases the response of neurons in the basolateral nucleus of the amygdala to afferent stimulation. Front. Behav. Neurosci. 2, 2 (2008).
Google Scholar
Liu, Z. P. et al. Chronic stress impairs GABAergic control of amygdala through suppressing the tonic GABAA receptor currents. Mol. Brain 7, 32 (2014).
Google Scholar
Rosenkranz, J. A., Venheim, E. R. & Padival, M. Chronic stress causes amygdala hyperexcitability in rodents. Biol. Psychiatry 67, 1128–1136 (2010).
Google Scholar
Hetzel, A. & Rosenkranz, J. A. Distinct effects of repeated restraint stress on basolateral amygdala neuronal membrane properties in resilient adolescent and adult rats. Neuropsychopharmacology 39, 2114–2130 (2014).
Google Scholar
Rau, A. R., Chappell, A. M., Butler, T. R., Ariwodola, O. J. & Weiner, J. L. Increased basolateral amygdala pyramidal cell excitability may contribute to the anxiogenic phenotype induced by chronic early-life stress. J. Neurosci. 35, 9730–9740 (2015).
Google Scholar
Sharp, B. M. Basolateral amygdala and stress-induced hyperexcitability affect motivated behaviors and addiction. Transl. Psychiatry 7, e1194 (2017).
Google Scholar
Masneuf, S. et al. Glutamatergic mechanisms associated with stress-induced amygdala excitability and anxiety-related behavior. Neuropharmacology 85, 190–197 (2014).
Google Scholar
Lowery-Gionta, E. G. et al. Chronic stress dysregulates amygdalar output to the prefrontal cortex. Neuropharmacology 139, 68–75 (2018).
Google Scholar
Blume, S. R., Padival, M., Urban, J. H. & Rosenkranz, J. A. Disruptive effects of repeated stress on basolateral amygdala neurons and fear behavior across the estrous cycle in rats. Sci. Rep. 9, 12292 (2019).
Google Scholar
Partridge, J. G. et al. Stress increases GABAergic neurotransmission in CRF neurons of the central amygdala and bed nucleus stria terminalis. Neuropharmacology 107, 239–250 (2016).
Google Scholar
He, F., Ai, H., Wang, M., Wang, X. & Geng, X. Altered neuronal activity in the central nucleus of the amygdala induced by restraint water-immersion stress in rats. Neurosci. Bull. 34, 1067–1076 (2018).
Google Scholar
Giovanniello, J. et al. A central amygdala–globus pallidus circuit conveys unconditioned stimulus-related information and controls fear learning. J. Neurosci. 40, 9043–9054 (2020).
Google Scholar
Murray, J. E. et al. Basolateral and central amygdala differentially recruit and maintain dorsolateral striatum-dependent cocaine-seeking habits. Nat. Commun. 6, 10088 (2015).
Google Scholar
Liu, J. et al. Differential efferent projections of GABAergic neurons in the basolateral and central nucleus of amygdala in mice. Neurosci. Lett. 745, 135621 (2021).
Google Scholar
Sah, P., Faber, E. S., Lopez De Armentia, M. & Power, J. The amygdaloid complex: anatomy and physiology. Physiol. Rev. 83, 803–834 (2003).
Google Scholar
Limoges, A., Yarur, H. E. & Tejeda, H. A. Dynorphin/kappa opioid receptor system regulation on amygdaloid circuitry: implications for neuropsychiatric disorders. Front. Syst. Neurosci. 16, 963691 (2022).
Google Scholar
Daviu, N., Bruchas, M. R., Moghaddam, B., Sandi, C. & Beyeler, A. Neurobiological links between stress and anxiety. Neurobiol. Stress 11, 100191 (2019).
Google Scholar
McEwen, B. S., Nasca, C. & Gray, J. D. Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology 41, 3–23 (2016).
Google Scholar
Shan, Q., Ge, M., Christie, M. J. & Balleine, B. W. The acquisition of goal-directed actions generates opposing plasticity in direct and indirect pathways in dorsomedial striatum. J. Neurosci. 34, 9196–9201 (2014).
Google Scholar
Belin-Rauscent, A., Everitt, B. J. & Belin, D. Intrastriatal shifts mediate the transition from drug-seeking actions to habits. Biol. Psychiatry 72, 343–345 (2012).
Google Scholar
Corbit, L. H., Nie, H. & Janak, P. H. Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol. Psychiatry 72, 389–395 (2012).
Google Scholar
Wendler, E. et al. The roles of the nucleus accumbens core, dorsomedial striatum, and dorsolateral striatum in learning: performance and extinction of Pavlovian fear-conditioned responses and instrumental avoidance responses. Neurobiol. Learn. Mem. 109, 27–36 (2014).
Google Scholar
Weera, M. M., Schreiber, A. L., Avegno, E. M. & Gilpin, N. W. The role of central amygdala corticotropin-releasing factor in predator odor stress-induced avoidance behavior and escalated alcohol drinking in rats. Neuropharmacology 166, 107979 (2020).
Google Scholar
Franklin, K. B. J. & Paxinos, G. The Mouse Brain in Stereotaxic Coordinates 3rd edn (Elsevier, 2008).
Tye, K. M. et al. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493, 537–541 (2013).
Google Scholar
Cerniauskas, I. et al. Chronic stress induces activity, synaptic, and transcriptional remodeling of the lateral habenula associated with deficits in motivated behaviors. Neuron 104, 899–915.e898 (2019).
Google Scholar
Bavley, C. C., Fischer, D. K., Rizzo, B. K. & Rajadhyaksha, A. M. Cav1.2 channels mediate persistent chronic stress-induced behavioral deficits that are associated with prefrontal cortex activation of the p25/Cdk5-glucocorticoid receptor pathway. Neurobiol. Stress 7, 27–37 (2017).
Google Scholar
Freymann, J., Tsai, P. P., Stelzer, H. D., Mischke, R. & Hackbarth, H. Impact of bedding volume on physiological and behavioural parameters in laboratory mice. Lab. Anim. 51, 601–612 (2017).
Google Scholar
Pałucha-Poniewiera, A., Podkowa, K., Rafało-Ulińska, A., Brański, P. & Burnat, G. The influence of the duration of chronic unpredictable mild stress on the behavioural responses of C57BL/6J mice. Behav. Pharmacol. 31, 574–582 (2020).
Google Scholar
La-Vu, M. Q. et al. Sparse genetically defined neurons refine the canonical role of periaqueductal gray columnar organization. eLife 11, e77115 (2022).
Google Scholar
Reis, F. M. et al. Dorsal periaqueductal gray ensembles represent approach and avoidance states. eLife 10, e64934 (2021).
Google Scholar
Hilário, M. R., Clouse, E., Yin, H. H. & Costa, R. M. Endocannabinoid signaling is critical for habit formation. Front. Integr. Neurosci. 1, 6 (2007).
Google Scholar
Lichtenberg, N. T. et al. The medial orbitofrontal cortex–basolateral amygdala circuit regulates the influence of reward cues on adaptive behavior and choice. J. Neurosci. 41, 7267–7277 (2021).
Google Scholar
Sias, A. et al. A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories. eLife 10, e68617 (2021).
Google Scholar
Sherathiya, V. N., Schaid, M. D., Seiler, J. L., Lopez, G. C. & Lerner, T. N. GuPPy, a Python toolbox for the analysis of fiber photometry data. Sci. Rep. 11, 24212 (2021).
Google Scholar
Roth, B. L. DREADDs for neuroscientists. Neuron 89, 683–694 (2016).
Google Scholar
Vazey, E. M. & Aston-Jones, G. Designer receptor manipulations reveal a role of the locus coeruleus noradrenergic system in isoflurane general anesthesia. Proc. Natl Acad. Sci. USA 111, 3859–3864 (2014).
Google Scholar
Qiu, M. H., Chen, M. C., Fuller, P. M. & Lu, J. Stimulation of the pontine parabrachial nucleus promotes wakefulness via extra-thalamic forebrain circuit nodes. Curr. Biol. 26, 2301–2312 (2016).
Google Scholar
Pomrenze, M. B. et al. A corticotropin releasing factor network in the extended amygdala for anxiety. J. Neurosci. 39, 1030–1043 (2019).
Google Scholar
Malvaez, M., Shieh, C., Murphy, M. D., Greenfield, V. Y. & Wassum, K. M. Distinct cortical–amygdala projections drive reward value encoding and retrieval. Nat. Neurosci. 22, 762–769 (2019).
Google Scholar
Collins, A. L. et al. Nucleus accumbens cholinergic interneurons oppose cue-motivated behavior. Biol. Psychiatry 86, 388–396 (2019).
Google Scholar
Schmider, E., Ziegler, M., Danay, E., Beyer, L. & Bühner, M. Is it really robust? Reinvestigating the robustness of ANOVA against violations of the normal distribution assumption. Methodology (Gott.) 6, 147–151 (2010).
Google Scholar
Knief, U. & Forstmeier, W. Violating the normality assumption may be the lesser of two evils. Behav. Res. Methods 53, 2576–2590 (2021).
Google Scholar
Giovanniello, J. et al. A dual-pathway architecture for stress to disrupt agency and promote habit. Dryad https://doi.org/10.5061/dryad.2jm63xt00 (2024).
Monteiro, S. et al. An efficient chronic unpredictable stress protocol to induce stress-related responses in C57BL/6 mice. Front. Psychiatry 6, 6 (2015).
Google Scholar
Mineur, Y. S., Belzung, C. & Crusio, W. E. Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice. Behav. Brain Res. 175, 43–50 (2006).
Google Scholar
Fang, X. et al. Chronic unpredictable stress induces depression-related behaviors by suppressing AgRP neuron activity. Mol. Psychiatry 26, 2299–2315 (2021).
Google Scholar
Gong, S. et al. Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J. Neurosci. 27, 9817–9823 (2007).
Google Scholar
Valjent, E., Bertran-Gonzalez, J., Hervé, D., Fisone, G. & Girault, J. A. Looking BAC at striatal signaling: cell-specific analysis in new transgenic mice. Trends Neurosci. 32, 538–547 (2009).
Google Scholar
