دورية أكاديمية

Hippocampal neurogenesis promotes effortful responding but does not regulate effort-based choice.

التفاصيل البيبلوغرافية
العنوان: Hippocampal neurogenesis promotes effortful responding but does not regulate effort-based choice.
المؤلفون: Seib DR; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia, Canada., Princz-Lebel O; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia, Canada., Chahley ER; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia, Canada., Floresco SB; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia, Canada., Snyder JS; Department of Psychology, Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia, Canada.
المصدر: Hippocampus [Hippocampus] 2022 Nov; Vol. 32 (11-12), pp. 818-827. Date of Electronic Publication: 2022 Sep 30.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Wiley Country of Publication: United States NLM ID: 9108167 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1098-1063 (Electronic) Linking ISSN: 10509631 NLM ISO Abbreviation: Hippocampus Subsets: MEDLINE
أسماء مطبوعة: Publication: New York, NY : Wiley
Original Publication: New York, NY : Churchill Livingstone, c1991-
مواضيع طبية MeSH: Neurogenesis* , Reward*, Humans ; Rats ; Animals ; Hippocampus ; Motivation ; Sugars ; Choice Behavior/physiology
مستخلص: A fundamental trait of depression is low motivation. Hippocampal neurogenesis has been associated with motivational deficits but detailed evidence on how it regulates human-relevant behavioral traits is still missing. We used the hGFAP-TK rat model to deplete actively dividing neural stem cells in the rat hippocampus. Use of the effort-discounting operant task allowed us to identify specific and detailed deficits in motivation behavior. In this task, rats are given a choice between small and large food rewards, where 2-20 lever presses are required to obtain the large reward (four sugar pellets) versus one press to receive the smaller reward (two sugar pellets). We found that depleting adult neurogenesis did not affect effort-based choice or general motivation to complete the task. However, lack of adult neurogenesis reduced the pressing rate and thus increased time to complete the required presses to obtain a reward. In summary, the present study finds that adult hippocampal neurogenesis specifically reduces response vigor to obtain rewards and thus deepens our understanding in how neurogenesis shapes depression.
(© 2022 Wiley Periodicals LLC.)
References: Abela, A. R., Duan, Y., & Chudasama, Y. (2015). Hippocampal interplay with the nucleus accumbens is critical for decisions about time. The European Journal of Neuroscience, 42, 2224-2233.
Avchalumov, Y., & Mandyam, C. D. (2021). Plasticity in the hippocampus, neurogenesis and drugs of abuse. Brain Sciences, 11, 404.
Bagot, R. C., Parise, E. M., Peña, C. J., Zhang, H.-X., Maze, I., Chaudhury, D., Persaud, B., Cachope, R., Bolaños-Guzmán, C. A., Cheer, J. F., Deisseroth, K., Han, M.-H., & Nestler, E. J. (2015). Ventral hippocampal afferents to the nucleus accumbens regulate susceptibility to depression. Nature Communications, 6, 7062.
Bayer, R., Franke, H., Ficker, C., Richter, M., Lessig, R., Büttner, A., & Weber, M. (2015). Alterations of neuronal precursor cells in stages of human adult neurogenesis in heroin addicts. Drug and Alcohol Dependence, 156, 139-149.
Belleau, E. L., Treadway, M. T., & Pizzagalli, D. A. (2019). The impact of stress and major depressive disorder on hippocampal and medial prefrontal cortex morphology. Biological Psychiatry, 85, 443-453.
Belujon, P., & Grace, A. A. (2008). Critical role of the prefrontal cortex in the regulation of hippocampus-Accumbens information flow. Journal of Neuroscience, 28, 9797-9805.
Boldrini, M., Fulmore, C. A., Tartt, A. N., Simeon, L. R., Pavlova, I., Poposka, V., Rosoklija, G. B., Stankov, A., Arango, V., Dwork, A. J., Hen, R., & Mann, J. J. (2018). Human hippocampal neurogenesis persists throughout aging. Cell Stem Cell, 22, 589-599.e5.
Boldrini, M., Santiago, A. N., Hen, R., Dwork, A. J., Rosoklija, G. B., Tamir, H., Arango, V., & John, M. J. (2013). Hippocampal granule neuron number and dentate gyrus volume in antidepressant-treated and untreated major depression. Neuropsychopharmacology, 38, 1068-1077.
Boldrini, M., Underwood, M. D., Hen, R., Rosoklija, G. B., Dwork, A. J., John Mann, J., & Arango, V. (2009). Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology, 34, 2376-2389.
Botvinick, M. M., Huffstetler, S., & McGuire, J. T. (2009). Effort discounting in human nucleus accumbens. Cognitive, Affective, & Behavioral Neuroscience, 9, 16-27.
Britt, J. P., Benaliouad, F., McDevitt, R. A., Stuber, G. D., Wise, R. A., & Bonci, A. (2012). Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus Accumbens. Neuron, 76, 790-803.
Bryce, C. A., & Floresco, S. B. (2016). Perturbations in effort-related decision-making driven by acute stress and Corticotropin-releasing factor. Neuropsychopharmacology, 41, 2147-2159.
Bryce, C. A., & Floresco, S. B. (2019). Alterations in effort-related decision-making induced by stimulation of dopamine D1, D2, D3, and corticotropin-releasing factor receptors in nucleus accumbens subregions. Psychopharmacology, 236, 2699-2712.
Bulin, S. E., Mendoza, M. L., Richardson, D. R., Song, K. H., Solberg, T. D., Yun, S., & Eisch, A. J. (2018). Dentate gyrus neurogenesis ablation via cranial irradiation enhances morphine self-administration and locomotor sensitization: Ablation of neurogenesis and morphine addiction. Addiction Biology, 23, 665-675.
Cléry-Melin, M.-L., Schmidt, L., Lafargue, G., Baup, N., Fossati, P., & Pessiglione, M. (2011). Why Don't you try harder? An investigation of effort production in major depression. PLoS One, 6, e23178.
David, D. J., Samuels, B. A., Rainer, Q., Wang, J.-W., Marsteller, D., Mendez, I., Drew, M., Craig, D. A., Guiard, B. P., Guilloux, J.-P., Artymyshyn, R. P., Gardier, A. M., Gerald, C., Antonijevic, I. A., Leonardo, E. D., & Hen, R. (2009). Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron, 62, 479-493.
Delaney, C. L., Brenner, M., & Messing, A. (1996). Conditional ablation of cerebellar astrocytes in postnatal transgenic mice. The Journal of Neuroscience, 16, 6908-6918.
Deroche-Gamonet, V., Revest, J.-M., Fiancette, J.-F., Balado, E., Koehl, M., Grosjean, N., Abrous, D. N., & Piazza, P.-V. (2019). Depleting adult dentate gyrus neurogenesis increases cocaine-seeking behavior. Molecular Psychiatry, 24, 312-320.
Dombrovski, A. Y., Clark, L., Siegle, G. J., Butters, M. A., Ichikawa, N., Sahakian, B. J., & Szanto, K. (2010). Reward/punishment reversal learning in older suicide attempters. AJP, 167, 699-707.
Eisch, A. J., & Petrik, D. (2012). Depression and hippocampal neurogenesis: A road to remission? Science, 338, 72-75.
Eliwa, H., Brizard, B., le Guisquet, A.-M., Hen, R., Belzung, C., & Surget, A. (2021). Adult neurogenesis augmentation attenuates anhedonia and HPA axis dysregulation in a mouse model of chronic stress and depression. Psychoneuroendocrinology, 124, 105097.
Farrar, A. M., Segovia, K. N., Randall, P. A., Nunes, E. J., Collins, L. E., Stopper, C. M., Port, R. G., Hockemeyer, J., Müller, C. E., Correa, M., & Salamone, J. D. (2010). Nucleus accumbens and effort-related functions: Behavioral and neural markers of the interactions between adenosine A2A and dopamine D2 receptors. Neuroscience, 166, 1056-1067.
Floresco, S. B., & Ghods-Sharifi, S. (2006). Amygdala-prefrontal cortical circuitry regulates effort-based decision making. Cerebral Cortex, 17, 251-260.
Floresco, S. B., Todd, C. L., & Grace, A. A. (2001). Glutamatergic afferents from the hippocampus to the nucleus Accumbens regulate activity of ventral tegmental area dopamine neurons. The Journal of Neuroscience, 21, 4915-4922.
Gamble, B., Moreau, D., Tippett, L. J., & Addis, D. R. (2019). Specificity of future thinking in depression: A meta-analysis. Perspectives on Psychological Science, 14, 816-834.
Garthe, A., Behr, J., & Kempermann, G. (2009). Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS One, 4, e5464.
Ghods-Sharifi, S., & Floresco, S. B. (2010). Differential effects on effort discounting induced by inactivations of the nucleus accumbens core or shell. Behavioral Neuroscience, 124, 179-191.
Grace, A. A., Floresco, S. B., Goto, Y., & Lodge, D. J. (2007). Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends in Neurosciences, 30, 220-227.
Grahek, I., Shenhav, A., Musslick, S., Krebs, R. M., & Koster, E. H. W. (2019). Motivation and cognitive control in depression. Neuroscience & Biobehavioral Reviews, 102, 371-381.
Halahakoon, D. C., Kieslich, K., O'Driscoll, C., Nair, A., Lewis, G., & Roiser, J. P. (2020). Reward-processing behavior in depressed participants relative to healthy volunteers: A systematic review and meta-analysis. JAMA Psychiatry, 77, 1286-1295.
Henriques, J. B., & Davidson, R. J. (2000). Decreased responsiveness to reward in depression. Cognition & Emotion, 14, 711-724.
Henriques JB, Glowacki JM, Davidson RJ. 1994. Reward Fails to Alter Response Bias in Depression 103:460-466.
Hill, A. S., Sahay, A., & Hen, R. (2015). Increasing adult hippocampal neurogenesis is sufficient to reduce anxiety and depression-like behaviors. Neuropsychopharmacology, 40, 2368-2378.
Hosking, J. G., Floresco, S. B., & Winstanley, C. A. (2015). Dopamine antagonism decreases willingness to expend physical, but not cognitive, effort: A comparison of two rodent cost/benefit decision-making tasks. Neuropsychopharmacology, 40, 1005-1015.
Karlsson, R.-M., Wang, A. S., Sonti, A. N., & Cameron, H. A. (2018). Adult neurogenesis affects motivation to obtain weak, but not strong, reward in operant tasks. Hippocampus, 28, 512-522.
Kheramin, S., Body, S., Herrera, F. M., Bradshaw, C. M., Szabadi, E., Deakin, J. F. W., & Anderson, I. M. (2005). The effect of orbital prefrontal cortex lesions on performance on a progressive ratio schedule: Implications for models of inter-temporal choice. Behavioural Brain Research, 156, 145-152.
Li, Z., Chen, Z., Fan, G., Li, A., Yuan, J., & Xu, T. (2018). Cell-type-specific afferent innervation of the nucleus Accumbens Core and Shell. Frontiers in Neuroanatomy, 12, 84-100.
Lodge, D. J., & Grace, A. A. (2007). Aberrant hippocampal activity underlies the dopamine dysregulation in an animal model of schizophrenia. Journal of Neuroscience, 27, 11424-11430.
Lothmann, K., Deitersen, J., Zilles, K., Amunts, K., & Herold, C. (2021). New boundaries and dissociation of the mouse hippocampus along the dorsal-ventral axis based on glutamatergic, GABAergic and catecholaminergic receptor densities. Hippocampus, 31, 56-78.
Luo, O. D., Kwiecien-Delaney, B., Martin, P., Foster, J. A., & Sidor, M. M. (2021). The effect of early life immune challenge on adult forced swim test performance and hippocampal neurogenesis. Journal of Neuroimmunology, 354, 577530.
McGregor, A., Baker, G., & Roberts, D. (1996). Effect of 6-hydroxydopamine lesions of the medial prefrontal cortex on intravenous cocaine self-administration under a progressive ratio schedule of reinforcement. Pharmacology Biochemistry and Behavior, 53, 5-9.
Miller, B. R., & Hen, R. (2015). The current state of the neurogenic theory of depression and anxiety. Current Opinion in Neurobiology, 30, 51-58.
Murphy, F. C., Michael, A., Robbins, T. W., & Sahakian, B. J. (2003). Neuropsychological impairment in patients with major depressive disorder: The effects of feedback on task performance. Psychological Medicine, 33, 455-467.
Noonan, M. A., Bulin, S. E., Fuller, D. C., & Eisch, A. J. (2010). Reduction of adult hippocampal neurogenesis confers vulnerability in an animal model of cocaine addiction. Journal of Neuroscience, 30, 304-315.
Nunes, E. J., Randall, P. A., Podurgiel, S., Correa, M., & Salamone, J. D. (2013). Nucleus accumbens neurotransmission and effort-related choice behavior in food motivation: Effects of drugs acting on dopamine, adenosine, and muscarinic acetylcholine receptors. Neuroscience & Biobehavioral Reviews, 37, 2015-2025.
Pizzagalli, D. A., Iosifescu, D., Hallett, L. A., Ratner, K. G., & Fava, M. (2009). Reduced hedonic capacity in major depressive disorder: Evidence from a probabilistic reward task. Journal of Psychiatric Research, 43, 76-87.
Planchez, B., Lagunas, N., Le Guisquet, A.-M., Legrand, M., Surget, A., Hen, R., & Belzung, C. (2021). Increasing adult hippocampal neurogenesis promotes resilience in a mouse model of depression. Cell, 10, 972-990.
Pulcu, E., Trotter, P. D., Thomas, E. J., McFarquhar, M., Juhasz, G., Sahakian, B. J., Deakin, J. F. W., Zahn, R., Anderson, I. M., & Elliott, R. (2014). Temporal discounting in major depressive disorder. Psychological Medicine, 44, 1825-1834.
Randall, P. A., Pardo, M., Nunes, E. J., López Cruz, L., Vemuri, V. K., Makriyannis, A., Baqi, Y., Müller, C. E., Correa, M., & Salamone, J. D. (2012). Dopaminergic modulation of effort-related choice behavior as assessed by a progressive ratio chow feeding choice task: Pharmacological studies and the role of individual differences. PLoS One, 7, e47934.
Salamone, J. D., Correa, M., Farrar, A., & Mingote, S. M. (2007). Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology, 191, 461-482.
Salamone, J. D., Correa, M., Yang, J.-H., Rotolo, R., & Presby, R. (2018). Dopamine, effort-based choice, and behavioral economics: Basic and translational research. Frontiers in Behavioral Neuroscience, 12, 52.
Salamone, J. D., Correa, M., Yohn, S., Lopez Cruz, L., San Miguel, N., & Alatorre, L. (2016). The pharmacology of effort-related choice behavior: Dopamine, depression, and individual differences. Behavioural Processes, 127, 3-17.
Salamone, J. D., Cousins, M. S., McCullough, L. D., Carriero, D. L., & Berkowitz, R. J. (1994). Nucleus accumbens dopamine release increases during instrumental lever pressing for food but not free food consumption. Pharmacology Biochemistry and Behavior, 49, 25-31.
Santarelli, L. (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science, 301, 805-809.
Schmidt-Hieber, C., Jonas, P., & Bischofberger, J. (2004). Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature, 429, 184-187.
Schoenfeld, T. J., McCausland, H. C., Morris, H. D., Padmanaban, V., & Cameron, H. A. (2017). Stress and loss of adult neurogenesis differentially reduce hippocampal volume. Biological Psychiatry, 82, 914-923.
Seib D, Martin-Villalba A. 2013. In vivo Neurogenesis. BIO-PROTOCOL 3:e841.
Seib, D. R., Espinueva, D. F., Floresco, S. B., & Snyder, J. S. (2020). A role for neurogenesis in probabilistic reward learning. Behavioral Neuroscience, 134, 283-295.
Seib, D. R., Espinueva, D. F., Princz-Lebel, O., Chahley, E., Stevenson, J., O'Leary, T. P., Floresco, S. B., & Snyder, J. S. (2021). Hippocampal neurogenesis promotes preference for future rewards. Molecular Psychiatry, 26, 6317-6335.
Seib, D. R. M., Corsini, N. S., Ellwanger, K., Plaas, C., Mateos, A., Pitzer, C., Niehrs, C., Celikel, T., & Martin-Villalba, A. (2013). Loss of Dickkopf-1 restores neurogenesis in old age and counteracts cognitive decline. Cell Stem Cell, 12, 204-213.
Seok, J.-W., & Cheong, C. (2020). Functional dissociation of hippocampal subregions corresponding to memory types and stages. Journal of Physiological Anthropology, 39, 15.
Shafiei, N., Gray, M., Viau, V., & Floresco, S. B. (2012). Acute stress induces selective alterations in cost/benefit decision-making. Neuropsychopharmacology, 37, 2194-2209.
Sheline, Y. I., Liston, C., & McEwen, B. S. (2019). Parsing the hippocampus in depression: Chronic stress, hippocampal volume, and major depressive disorder. Biological Psychiatry, 85, 436-438.
Snyder, J. S., Grigereit, L., Russo, A., Seib, D. R., Brewer, M., Pickel, J., & Cameron, H. A. (2016). A transgenic rat for specifically inhibiting adult neurogenesis. eNeuro, 3(3), ENEURO.0064-16.2016.
Snyder, J. S., Kee, N., & Wojtowicz, J. M. (2001). Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. Journal of Neurophysiology, 85, 2423-2431.
Snyder, J. S., Soumier, A., Brewer, M., Pickel, J., & Cameron, H. A. (2011). Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature, 476, 458-461.
Taliaz, D., Stall, N., Dar, D. E., & Zangen, A. (2010). Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Molecular Psychiatry, 15, 80-92.
Tang, M., Lin, W., Pan, Y., Guan, X., & Li, Y. (2016). Hippocampal neurogenesis dysfunction linked to depressive-like behaviors in a neuroinflammation induced model of depression. Physiology & Behavior, 161, 166-173.
Treadway, M. T., Bossaller, N. A., Shelton, R. C., & Zald, D. H. (2012). Effort-based decision-making in major depressive disorder: A translational model of motivational anhedonia. Journal of Abnormal Psychology, 121, 553-558.
Treadway, M. T., Buckholtz, J. W., Schwartzman, A. N., Lambert, W. E., & Zald, D. H. (2009). Worth the ‘EEfRT’? The effort expenditure for rewards task as an objective measure of motivation and anhedonia. PLoS One, 4, e6598.
Trifilieff, P., Feng, B., Urizar, E., Winiger, V., Ward, R. D., Taylor, K. M., Martinez, D., Moore, H., Balsam, P. D., Simpson, E. H., & Javitch, J. A. (2013). Increasing dopamine D2 receptor expression in the adult nucleus accumbens enhances motivation. Molecular Psychiatry, 18, 1025-1033.
Uribe, K. P., Correa, V. L., Pinales, B. E., Flores, R. J., Cruz, B., Shan, Z., Bruijnzeel, A. W., Khan, A. M., & O'Dell, L. E. (2020). Overexpression of corticotropin-releasing factor in the nucleus accumbens enhances the reinforcing effects of nicotine in intact female versus male and ovariectomized female rats. Neuropsychopharmacology, 45, 394-403.
Videbech, P. (2004). Hippocampal volume and depression: A meta-analysis of MRI studies. American Journal of Psychiatry, 161, 1957-1966.
Wang, Y., Cui, X.-L., Liu, Y.-F., Gao, F., Wei, D., Li, X.-W., Wang, H.-N., Tan, Q.-R., & Jiang, W. (2011). LPS inhibits the effects of fluoxetine on depression-like behavior and hippocampal neurogenesis in rats. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 35, 1831-1835.
Williams, R. G., Li, K. H., & Phillips, P. E. M. (2022). The influence of stress on decision-making: Effects of CRF and dopamine antagonism in the nucleus Accumbens. Frontiers in Psychiatry, 12, 814218.
معلومات مُعتمدة: Canada CIHR
فهرسة مساهمة: Keywords: adult neurogenesis; depression; hippocampus; motivation; reward
المشرفين على المادة: 0 (Sugars)
تواريخ الأحداث: Date Created: 20220930 Date Completed: 20221121 Latest Revision: 20230105
رمز التحديث: 20240628
DOI: 10.1002/hipo.23472
PMID: 36177887
قاعدة البيانات: MEDLINE
الوصف
تدمد:1098-1063
DOI:10.1002/hipo.23472