Alan Watts

Summary Statement of Research Interests

Our work is directed towards understanding how the brain contributes to the development, manifestation, and complications of diabetes and obesity. We do this in two projects that focus on the neural control of energy metabolism.

The first project investigates how peripheral metabolism interacts with the brain to generate adrenocortical and sympathoadrenal hormonal responses. In particular, we are interested in the way that two critical metabolic signals—glucocorticoid hormones and hypoglycemia—are sensed by the brain, and then generate appropriate counter-regulatory responses. We are interested in how glucocorticoids and neurotransmitters interact with neurons in the hypothalamic paraventricular nucleus, which is a major integrative cell group for metabolic control. A major focus is on sets of hindbrain catecholaminergic neurons that project to the forebrain. These neurons are crucial for detecting and encoding information about blood glucose levels. We investigate the way that catecholaminergic neurons and glucocorticoids affect signal transduction and gene regulatory mechanisms in sets of forebrain neurons.

The second project investigates the neural basis of anorexia using dehydration as a physiological challenge. The goal here is to understand the structure and functional interactions between the neural systems that inhibit and stimulate feeding, particularly between the cortex, hypothalamus, and hindbrain.

The techniques we use include: whole animal physiology, in situ hybridization, immunocytochemistry (with confocal and conventional immunofluorescence), tract-tracing, behavioral analysis, and neuroinfomatics.

Book Chapters

• Watts, A. G. (2011). Neuroendocrine Regulation of Food Intake. The Handbook of Neuroendocrinology pp. 331-354. San Diego, CA: Academic Press.
• Schneider, J. E., Watts, A. G. (2009). Energy Partitioning, Ingestive Behavior and Reproductive Success. In “Hormones, Brain, and Behavior, Vol 1.”. 2nd Edtn (Vol. 1) pp. 205-258. San Diego: Academic Press.
• Watts, A., Salter, D. S. (2004). Neural Mechanisms of Anorexia. 2 ‘The Handbook of Behavioral Neurobiology. Food and Fluid Intake’/Plenum Press..

Journal Article

• Chen, D., Rehfeld, J. F., Watts, A. G., Rorsman, P., Gundlach, A. L. (2023). History of key regulatory peptide systems and perspectives for future research. Journal of neuroendocrinology. Vol. 35 (11), pp. e13251. PubMed Web Address
• Langhans, W., Watts, A. G., Spector, A. C. (2023). The elusive cephalic phase insulin response: triggers, mechanisms, and functions. Physiological reviews. Vol. 103 (2), pp. 1423-1485. PubMed Web Address
• Watts, A. G., Kanoski, S. E., Sanchez-Watts, G., Langhans, W. (2022). The physiological control of eating: signals, neurons, and networks. Physiological reviews. Vol. 102 (2), pp. 689-813. PubMed Web Address
• Garcia-Luna, C., Sanchez-Watts, G., Arnold, M., de, G., DeWalt, N., Langhans, W., Watts, A. G. (2021). The Medullary Targets of Neurally Conveyed Sensory Information from the Rat Hepatic Portal and Superior Mesenteric Veins. eNeuro. Vol. 8 (1) PubMed Web Address
• Hahn, J. D., Sporns, O., Watts, A. G., Swanson, L. W. (2019). Macroscale intrinsic network architecture of the hypothalamus. Proceedings of the National Academy of Sciences of the United States of America. Vol. 116 (16), pp. 8018-8027. PubMed Web Address
• Krieger, J. P., Santos, E. P., Sanchez-Watts, G., Arnold, M., Pettersen, K. G., Mohammed, M., Modica, S., Lossel, P., Morrison, S. F., Madden, C. J., Watts, A. G., Langhans, W., Lee, S. J. (2018). Glucagon-like peptide-1 regulates brown adipose tissue thermogenesis via the gut-brain axis in rats. American journal of physiology. Regulatory, integrative and comparative physiology. Vol. 315 (4), pp. R708-R720. PubMed Web Address
• Langhans, W., Adan, R., Arnold, M., Banks, W. A., Card, J. P., Dailey, M. J., Daniels, D., de, A. D., de, G., Dickson, S., Fedele, S., Grill, H. J., Jansson, J. O., Kaufman, S., Kolar, G., Krause, E., Lee, S. J., Le, C., Levin, B. E., Lutz, T. A., Mansouri, A., Moran, T. H., Pacheco-López, G., Ramachandran, D., Raybould, H., Rinaman, L., Samson, W. K., Sanchez-Watts, G., Seeley, R. J., Skibicka, K. P., Small, D., Spector, A. C., Tamashiro, K. L., Templeton, B., Trapp, S., Tso, P., Watts, A. G., Weissfeld, N., Williams, D., Wolfrum, C., Yosten, G., Woods, S. C. (2018). New horizons for future research – Critical issues to consider for maximizing research excellence and impact. Molecular metabolism. Vol. 14, pp. 53-59. PubMed Web Address
• Johnson, C. S., Bains, J. S., Watts, A. G. (2018). Neurotransmitter diversity in pre-synaptic terminals located in the parvicellular neuroendocrine paraventricular nucleus of the rat and mouse hypothalamus. The Journal of comparative neurology. Vol. 526 (8), pp. 1287-1306. PubMed Web Address
• Lee, S. J., Jokiaho, A. J., Sanchez-Watts, G., Watts, A. G. (2018). Catecholaminergic projections into an interconnected forebrain network control the sensitivity of male rats to diet-induced obesity. American journal of physiology. Regulatory, integrative and comparative physiology. Vol. 314 (6), pp. R811-R823. PubMed Web Address
• Lee, S. J., Sanchez-Watts, G., Krieger, J. P., Pignalosa, A., Norell, P. N., Cortella, A., Pettersen, K. G., Vrdoljak, D., Hayes, M. R., Kanoski, S. E., Langhans, W., Watts, A. G. (2018). Loss of dorsomedial hypothalamic GLP-1 signaling reduces BAT thermogenesis and increases adiposity. Molecular metabolism. Vol. 11, pp. 33-46. PubMed Web Address
• Ryu, V., Watts, A. G., Xue, B., Bartness, T. J. (2017). Bidirectional crosstalk between the sensory and sympathetic motor systems innervating brown and white adipose tissue in male Siberian hamsters. American journal of physiology. Regulatory, integrative and comparative physiology. Vol. 312 (3), pp. R324-R337. PubMed Web Address
• Watts, A. G. (2017). Great Expectations: Anticipatory Control of Magnocellular Vasopressin Neurons. Neuron. Vol. 93 (1), pp. 1-2. PubMed Web Address
• Lee, S. J., Diener, K., Kaufman, S., Krieger, J. P., Pettersen, K. G., Jejelava, N., Arnold, M., Watts, A. G., Langhans, W. (2016). Limiting glucocorticoid secretion increases the anorexigenic property of Exendin-4. Molecular metabolism. Vol. 5 (7), pp. 552-565. PubMed Web Address
• Foster, N. N., Azam, S., Watts, A. G. (2016). Rapid-onset hypoglycemia suppresses Fos expression in discrete parts of the ventromedial nucleus of the hypothalamus. American journal of physiology. Regulatory, integrative and comparative physiology. Vol. 310 (11), pp. R1177-85. PubMed Web Address
• Watts, A. G., Grill, H. J. (2016). Tim Bartness (1953-2015). American journal of physiology. Regulatory, integrative and comparative physiology. Vol. 310 (5), pp. R385-7. PubMed Web Address
• Watts, A. G. (2015). 60 YEARS OF NEUROENDOCRINOLOGY: The structure of the neuroendocrine hypothalamus: the neuroanatomical legacy of Geoffrey Harris. The Journal of endocrinology. Vol. 226 (2), pp. T25-39. PubMed Web Address
• Donovan, C. M., Watts, A. G. (2014). Peripheral and central glucose sensing in hypoglycemic detection. Physiology (Bethesda, Md.). Vol. 29 (5), pp. 314-24. PubMed Web Address
• Jokiaho, A. J., Donovan, C. M., Watts, A. G. (2014). The rate of fall of blood glucose determines the necessity of forebrain-projecting catecholaminergic neurons for male rat sympathoadrenal responses. Diabetes. Vol. 63 (8), pp. 2854-65. PubMed Web Address
• Bohland, M., Matveyenko, A. V., Saberi, M., Khan, A. M., Watts, A. G., Donovan, C. M. (2014). Activation of hindbrain neurons is mediated by portal-mesenteric vein glucosensors during slow-onset hypoglycemia. Diabetes. Vol. 63 (8), pp. 2866-75. PubMed Web Address
• Watts, A. G. (2014). How do we know if the brain is wired for type 2 diabetes?. Current diabetes reports. Vol. 14 (3), pp. 465. PubMed Web Address
• Khan, A. M., Walker, E. M., Dominguez, N., Watts, A. G. (2014). Neural input is critical for arcuate hypothalamic neurons to mount intracellular signaling responses to systemic insulin and deoxyglucose challenges in male rats: implications for communication within feeding and metabolic control networks. Endocrinology. Vol. 155 (2), pp. 405-16. PubMed Web Address
• McCoy, D. D., Zhou, L., Nguyen, A. K., Watts, A. G., Donovan, C. M., McKemy, D. D. (2013). Enhanced insulin clearance in mice lacking TRPM8 channels. American journal of physiology. Endocrinology and metabolism. Vol. 305 (1), pp. E78-88. PubMed Web Address
• Watts, A. G., Khan, A. M. (2013). Identifying links in the chain: the dynamic coupling of catecholamines, peptide synthesis, and peptide release in hypothalamic neuroendocrine neurons. Advances in pharmacology (San Diego, Calif.). Vol. 68, pp. 421-44. PubMed Web Address
• Wamsteeker, J. I., Füzesi, T., Watts, A. G., Bains, J. S. (2013). Characterization of corticotropin-releasing hormone neurons in the paraventricular nucleus of the hypothalamus of Crh-IRES-Cre mutant mice. PloS one. Vol. 8 (5), pp. e64943. PubMed Web Address
• Khan, A. M., Kaminski, K. L., Sanchez-Watts, G., Ponzio, T. A., Kuzmiski, J. B., Bains, J. S., Watts, A. G. (2011). MAP kinases couple hindbrain-derived catecholamine signals to hypothalamic adrenocortical control mechanisms during glycemia-related challenges. J. Neuroscience. Vol. 31, pp. 18479-18491.
• Lui, Y., Poon, V., Sanchez-Watts, G., Watts, A. G., Takemori, H., Aguilera, G. (2011). Salt-inducible kinase is involved in the regulation of corticotropin-releasing hormone transcription in hypothalamic neurons in rats. Endocrinology.. Vol. 153 (1), pp. 223-233.
• Watts, A. G., Sanchez-Watts, G., Liu, Y., Aguilera, G. (2011). The distribution of messenger RNAs encoding the three isoforms of the Transducer Of Regulated CREB Activity (TORC) in the rat forebrain. J. Neuroendocrinology. Vol. 23, pp. 754-766.
• Boyle, C. N., Lorenzen, S. M., Compton, D., Watts, A. G. (2011). Dehydration-anorexia derives from a reduction in meal size, but not meal number. Physiology & Behavior. Vol. 105, pp. 305-314.
• Watts, A. G., Sanchez-Watts, G., Liu, Y., Aguilera, G. (2011). The distribution of messenger RNAs encoding the three isoforms of the transducer of regulated cAMP responsive element binding protein activity in the rat forebrain. Journal of neuroendocrinology. Vol. 23 (8), pp. 754-66. PubMed Web Address
• Watts, A. G. (2010). Structure and function in the conceptual development of mammalian neuroendocrinology between 1920 and 1965. Brain Research Reviews. Vol. 65 (2), pp. 174-204.
• Watts, A. G., Boyle, C. N. (2010). The functional architecture of dehydration-anorexia. Physiology & Behavior. Vol. 100, pp. 422-427.
• Watts, A. G., Donovan, C. D. (2010). Sweet Talk In The Brain: Glucosensing, Neural Networks, and Hypoglycemic Counterregulation. Frontiers in Neuroendocrinology. Frontiers in Neuroendocrinology.
• Watts, A. G., Donovan, C. M. (2010). Sweet talk in the brain: glucosensing, neural networks, and hypoglycemic counterregulation. Frontiers in neuroendocrinology. Vol. 31 (1), pp. 32-43. PubMed Web Address
• Salter-Venzon, D., Watts, A. G. (2009). Site-specific attenuation of feeding response after hypothalamic injections of neuropeptide Y in anorexia. Am. J. Physiol. Reg, and Comp Physiol.. Vol. 297 (6), pp. R1813-1821.
• Salter-Venzon, D., Watts, A. G. (2009). Site-specific attenuation of food intake but not the latency to eat after hypothalamic injections of neuropeptide Y in dehydrated-anorexic rats. American journal of physiology. Regulatory, integrative and comparative physiology. Vol. 297 (6), pp. R1813-21. PubMed Web Address
• Salter-Venzon, D., Watts, A. G. (2008). The role of hypothalamic ingestive behavior controllers in generating dehydration anorexia: a FOS mapping study. Am. J. Physiol. Reg, and Comp Physiol.. Vol. 295, pp. R1009-1019.
• Gorton, L. M., Khan, A. M., Bohland, M., Sanchez-Watts, G., Donovan, C. M., Watts, A. G. (2007). A role for the forebrain in mediating time-of-day differences in glucocorticoid counterregulatory responses to hypoglycemia in rats. Endocrinology. Vol. 148 (12), pp. 6026-39. PubMed Web Address
• Khan, A. M., Ponzio, T. A., Sanchez-Watts, G., Stanley, B. G., Hatton, G. I., Watts, A. G. (2007). Catecholaminergic control of mitogen-activated protein kinase signaling in paraventricular neuroendocrine neurons in vivo and in vitro: a proposed role during glycemic challenges. The Journal of neuroscience : the official journal of the Society for Neuroscience. Vol. 27 (27), pp. 7344-60. PubMed Web Address
• Watts, A., Sanchez-Watts, G. (2007). Rapid and preferential activation of Fos protein in hypocretin/orexin neurons following the reversal of dehydration-anorexia. J. Comp.Neurol.. Vol. 502, pp. 768-782.
• Watts, A., Salter, D. S., Neuner, C. M. (2007). Neural network interactions and ingestive behavior control during anorexia. Pysiology & Behavior. Vol. 91, pp. 389-396.
• Khan, A. M., Ponzio, T. A., Sanchez-Watts, G., Stanley, B. G., Hatton, G. I., Watts, A. (2007). Catecholaminergic control of MAP kinase signaling in paraventricular neuroendocrine neurons in vivo and in vitro: A proposed role during glycemic challenges. J.Neuroscience. Vol. 27, pp. 7344-7360.
• Gorton, L. M., Khan, A. M., Bohland, M. A., Sanchez-Watts, G., Donovan, C. M., Watts, A. (2007). A role for the forebrain in mediating time-of-day differences in glucocorticoid counterregulatory responses to hypoglycemia. Endocrinology.. Vol. 148, pp. 6026-6039.
• Watts, A. G., Khan, A. M., Sanchez-Watts, G., Salter, D., Neuner, C. M. (2006). Activation in neural networks controlling ingestive behaviors: what does it mean, and how do we map and measure it?. Physiology & behavior. Vol. 89 (4), pp. 501-10. PubMed Web Address
• Watts, A., Sanchez-Watts, G., Salter, G., Neuner, C. M. (2006). Activation in neural networks controlling ingestive behaviors: what does it mean and how do we map and measure it?. Physiology & Behavior. Vol. 89, pp. 501-520.
• Khan, A. M., Hahn, J. D., Cheng, W. C., Watts, A. G., Burns, G. A. (2006). NeuroScholar’s electronic laboratory notebook and its application to neuroendocrinology. Neuroinformatics. Vol. 4 (2), pp. 139-62. PubMed Web Address
• Swanson, L. W., Sanchez-Watts, G., Watts, A. G. (2005). Comparison of melanin-concentrating hormone and hypocretin/orexin mRNA expression patterns in a new parceling scheme of the lateral hypothalamic zone. Neuroscience letters. Vol. 387 (2), pp. 80-4. PubMed Web Address
• Swanson, L. W., Sanchez-Watts, G., Watts, A. (2005). Comparison of melanin-concentrating hormone and hypocretin/orexin mRNA expression patterns in a new parcelating scheme of the lateral hypothalamic zone. Neuroscience Letters. Vol. 387, pp. 80-84.
• Watts, A. (2005). Glucocorticoid regulation of peptide genes in neuroendocrine CRH neurons: a complexity beyond negative feedback. Frontiers in Neuroendocrinology. Vol. 26, pp. 109-130.
• Watts, A. G., Tanimura, S., Sanchez-Watts, G. (2004). Corticotropin-releasing hormone and arginine vasopressin gene transcription in the hypothalamic paraventricular nucleus of unstressed rats: daily rhythms and their interactions with corticosterone. Endocrinology. Vol. 145 (2), pp. 529-40. PubMed Web Address
• Khan, A. M., Watts, A. G. (2004). Intravenous 2-deoxy-D-glucose injection rapidly elevates levels of the phosphorylated forms of p44/42 mitogen-activated protein kinases (extracellularly regulated kinases 1/2) in rat hypothalamic parvicellular paraventricular neurons. Endocrinology. Vol. 145 (1), pp. 351-9. PubMed Web Address
• Khan, A. M., Watts, A. (2004). Intravenous 2-deoxy-D-glucose Injection Rapidly Elevates Levels of the Phosphorylated Forms of p44/42 Mitogen Activated Protein Kinases (Erk 1/2) in Rat Hypothalamic Parvocellular Paraventricular Neurons. Endocrinology.. Vol. 145, pp. 351-359.
• Watts, A., Tanimura, S. M., Sanchez-Watts, G. (2004). Crh and Avp gene transcription in the hypothalamic paraventricular nucleus of unstressed rats: daily rhythms and their corticosterone dependence. Endocrinology.. Vol. 145, pp. 529-540.
• Ritter, S., Watts, A. G., Dinh, T. T., Sanchez-Watts, G., Pedrow, C. (2003). Immunotoxin lesion of hypothalamically projecting norepinephrine and epinephrine neurons differentially affects circadian and stressor-stimulated corticosterone secretion. Endocrinology. Vol. 144 (4), pp. 1357-67. PubMed Web Address
• Salter, D., Watts, A. G. (2003). Differential suppression of hyperglycemic, feeding, and neuroendocrine responses in anorexia. American journal of physiology. Regulatory, integrative and comparative physiology. Vol. 284 (1), pp. R174-82. PubMed Web Address
• Watts, A. G., Sanchez-Watts, G. (2002). Interactions between heterotypic stressors and corticosterone reveal integrative mechanisms for controlling corticotropin-releasing hormone gene expression in the rat paraventricular nucleus. The Journal of neuroscience : the official journal of the Society for Neuroscience. Vol. 22 (14), pp. 6282-9. PubMed Web Address

• USC Raubenheimer Outstanding Senior Faculty Award, 2024-2025
• American Association for the Advancement of Science Fellow, Fellow, 2012
• Morton Jones Memorial Medal, International Congress of Neuroendocrinology, 2002
• NIH/NSF Career Development Award, 1996 – 2000

Administrative Appointments

• Director, Neuroscience Research Institute, 08/16/2006 – 08/15/2007
• Chair, USC Neuroscience Executive Committee, 07/01/2006 – 08/15/2007
• Head, Neurobiology Section, Dept. of Biological Sciences, 2003 – 2006
• Director, NIBS Neuroscience Program, 12/01/2004 – 08/16/2006

Committees

• Chair, Program Committee, Society for the Study of Ingestive Behaviors., 2010 – 2012

Editorships and Editorial Boards

• Senior Editor, Journal of Neuroendocrinology, 2012 – 2024
• Editorial board member, J. Neuroendocrinology, 2003 – 2012
• Associate Editor, Obesity, 2007 – 2011
• Editorial board member, Endocrinology, 2005 – 2009
• Editorial board member, Am. J. Physiol (Reg & Comp. Physiol.), 2007 – 2008

Professional Offices

• President, Society for the Study of Ingestive Behaviors, 2014 – 2015

Review Panels

• Center for Scientific Review, NIH, Various, 2003 – 2024
• The Obesity Society, Program Committee, 2012 – 2015
• Juvenile Diabetes Research Foundation, Hypoglycemia complications, 2009 – 2011