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Thomas Heinbockel

TitleDr.
InstitutionHoward University
DepartmentAnatomy
AddressHoward University College of Medicine
Dept. of Anatomy
1105 Adams Bldg.
Washington DC 20059
Phone202-806-9873
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    Research in Cellular & Systems Neuroscience:

    Neurobiology of Olfactory and Limbic Systems
    Research in my lab is aimed at elucidating organizational principles of neural systems in the brain using electrophysiological, pharmacological and anatomical methods. In particular, I am interested in the functional organization of the olfactory and limbic system. How do intrinsic and synaptic neuronal properties relate to information coding and neural network function of these systems? My research on both systems has been directed at understanding mechanisms of information processing that form the basis of persistent functional changes in these systems and their relation to neuropsychiatric and neurological disorders including epilepsy. To that end, I have started to work on translational projects, specifically, the development of novel anti-epileptic drugs and new pharmacological approaches for drug abuse treatment.

    Synaptic plasticity and neuromodulation
    In the limbic system, my research activities have been centered on a subcortical structure of the vertebrate brain, the amygdala. This structure is a component of the limbic system and a key brain site for emotion, fear, learning and memory. The amygdala is essential for developing an inner view of the outside sensory world and is thought to be one of the key structures for the interpretation of sensory information associated with motivation and emotion. Functional impairment of amygdaloid structures and related brain areas forms the pathophysiological basis of some common neuropsychiatric and neurological disorders including forms of epilepsy. The main goal of this line of work is to reveal functions of the amygdala at the cellular and network level and to integrate this knowledge into the functioning of higher order brain systems. I have studied properties of identified neuronal cell types at the level of local neuronal networks using acutely isolated slice preparations. This allows me to focus on intra-amygdaloidal synaptic networks that form the basis of the integrative functions of the amygdala. This helps us to better understand the cellular mechanisms that may underlie enduring changes in amygdala function associated with amygdala-dependent neuropsychiatric disorders. My research on the amygdala includes topics such synaptic transmission, neuromodulation, synaptic plasticity as well as mechanisms for generating rhythmic and epileptiform activity.

    Intrinsic and synaptic properties of olfactory bulb neurons
    In an olfactory bulb slice preparation I am using patch clamp and imaging techniques to characterize biophysical, cellular and synaptic properties of mitral and granule cells to gain insights into neuronal processing and odor coding in the vertebrate brain. Mitral and granule cells are two key cell types in the olfactory bulb. Mitral cells receive afferent input from olfactory receptor neurons and communicate with regions of the cerebral cortex. Granule cells provide inhibitory input to mitral cell dendrites in local neuronal circuits within the olfactory bulb. In particular, I am pursuing projects related to the presence and functional role of ionotropic and metabotropic receptors and associated neurotransmitter systems in shaping responses to olfactory nerve input and synaptic output to higher brain centers.

    Laboratory Techniques:
    • recording neural activity:
    - patch clamp technique, current clamp and voltage clamp
    - intracellular (sharp microelectrode) and extracellular electrophysiology
    - intracellular calcium measurements
    - voltage-sensitive dye imaging
    • photolysis of caged compounds
    • microstimulation, microinjection
    • intracellular staining
    • histochemistry
    • immunocytochemistry
    • neuronal tracing & neuroanatomical techniques (histochemistry, immunocytochemistry)
    • light and laser scanning confocal microscopy
    • differential interference contrast visualization of cells in living slices
    • acute tissue slices and organotypic slice cultures from wild-type and gene-targeted mice


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    Collapse selected publications
    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Faculty can login to make corrections and additions.
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    PMC Citations indicate the number of times the publication was cited by articles in PubMed Central, and the Altmetric score represents citations in news articles and social media. (Note that publications are often cited in additional ways that are not shown here.) Fields are based on how the National Library of Medicine (NLM) classifies the publication's journal and might not represent the specific topic of the publication. Translation tags are based on the publication type and the MeSH terms NLM assigns to the publication. Some publications (especially newer ones and publications not in PubMed) might not yet be assigned Field or Translation tags.) Click a Field or Translation tag to filter the publications.
    1. Gerkin RC, Ohla K, Veldhuizen MG, Joseph PV, Kelly CE, Bakke AJ, Steele KE, Farruggia MC, Pellegrino R, Pepino MY, Bouysset C, Soler GM, Pereda-Loth V, Dibattista M, Cooper KW, Croijmans I, Di Pizio A, Ozdener MH, Fjaeldstad AW, Lin C, Sandell MA, Singh PB, Brindha VE, Olsson SB, Saraiva LR, Ahuja G, Alwashahi MK, Bhutani S, D'Errico A, Fornazieri MA, Golebiowski J, Hwang LD, Öztürk L, Roura E, Spinelli S, Whitcroft KL, Faraji F, Fischmeister FPS, Heinbockel T, Hsieh JW, Huart C, Konstantinidis I, Menini A, Morini G, Olofsson JK, Philpott CM, Pierron D, Shields VDC, Voznessenskaya VV, Albayay J, Altundag A, Bensafi M, Bock MA, Calcinoni O, Fredborg W, Laudamiel C, Lim J, Lundström JN, Macchi A, Meyer P, Moein ST, Santamaría E, Sengupta D, Domínguez PP, Yanik H, Boesveldt S, de Groot JHB, Dinnella C, Freiherr J, Laktionova T, Mariño S, Monteleone E, Nunez-Parra A, Abdulrahman O, Ritchie M, Thomas-Danguin T, Walsh-Messinger J, Al Abri R, Alizadeh R, Bignon E, Cantone E, Cecchini MP, Chen J, Guàrdia MD, Hoover KC, Karni N, Navarro M, Nolden AA, Mazal PP, Rowan NR, Sarabi-Jamab A, Archer NS, Chen B, Di Valerio EA, Feeney EL, Frasnelli J, Hannum M, Hopkins C, Klein H, Mignot C, Mucignat C, Ning Y, Ozturk EE, Peng M, Saatci O, Sell EA, Yan CH, Alfaro R, Cecchetto C, Coureaud G, Herriman RD, Justice JM, Kaushik PK, Koyama S, Overdevest JB, Pirastu N, Ramirez VA, Roberts SC, Smith BC, Cao H, Wang H, Balungwe P, Baguma M, Hummel T, Hayes JE, Reed DR, Niv MY, Munger SD, Parma V. Recent smell loss is the best predictor of COVID-19: a preregistered, cross-sectional study. medRxiv. 2020 Jul 26. PMID: 32743605.
      Citations:    
    2. Parma V, Ohla K, Veldhuizen MG, Niv MY, Kelly CE, Bakke AJ, Cooper KW, Bouysset C, Pirastu N, Dibattista M, Kaur R, Liuzza MT, Pepino MY, Schöpf V, Pereda-Loth V, Olsson SB, Gerkin RC, Rohlfs Domínguez P, Albayay J, Farruggia MC, Bhutani S, Fjaeldstad AW, Kumar R, Menini A, Bensafi M, Sandell M, Konstantinidis I, Di Pizio A, Genovese F, Öztürk L, Thomas-Danguin T, Frasnelli J, Boesveldt S, Saatci Ö, Saraiva LR, Lin C, Golebiowski J, Dar Hwang L, Ozdener MH, Guàrdia MD, Laudamiel C, Ritchie M, Havlícek J, Pierron D, Roura E, Navarro M, Nolden AA, Lim J, Whitcroft KL, Colquitt LR, Ferdenzi C, Brindha EV, Altundag A, Macchi A, Nunez-Parra A, Patel ZM, Fiorucci S, Philpott CM, Smith BC, Lundström JN, Mucignat C, Parker JK, van den Brink M, Schmuker M, Fischmeister FPS, Heinbockel T, Shields VDC, Faraji F, Santamaría E, Fredborg WEA, Morini G, Olofsson JK, Jalessi M, Karni N, D'Errico A, Alizadeh R, Pellegrino R, Meyer P, Huart C, Chen B, Soler GM, Alwashahi MK, Welge-Lüssen A, Freiherr J, de Groot JHB, Klein H, Okamoto M, Singh PB, Hsieh JW, Reed DR, Hummel T, Munger SD, Hayes JE. More than smell - COVID-19 is associated with severe impairment of smell, taste, and chemesthesis. Chem Senses. 2020 Jun 20. PMID: 32564071.
      Citations: 3     Fields:    
    3. Bhatia-Dey N, Heinbockel T. Endocannabinoid-Mediated Neuromodulation in the Olfactory Bulb: Functional and Therapeutic Significance. Int J Mol Sci. 2020 Apr 19; 21(8). PMID: 32325875.
      Citations: 1     Fields:    
    4. Koyama S, Heinbockel T. The Effects of Essential Oils and Terpenes in Relation to Their Routes of Intake and Application. Int J Mol Sci. 2020 Feb 25; 21(5). PMID: 32106479.
      Citations:    Fields:    
    5. Craighead DH, Heinbockel TC, Hamilton MN, Bailey EF, MacDonald MJ, Gibala MJ, Seals DR. Time-efficient physical training for enhancing cardiovascular function in midlife and older adults: promise and current research gaps. J Appl Physiol (1985). 2019 11 01; 127(5):1427-1440. PMID: 31556835.
      Citations:    Fields:    
    6. Wang ZJ, Hu SS, Bradshaw HB, Sun L, Mackie K, Straiker A, Heinbockel T. Cannabinoid receptor-mediated modulation of inhibitory inputs to mitral cells in the main olfactory bulb. J Neurophysiol. 2019 08 01; 122(2):749-759. PMID: 31215302.
      Citations: 2     Fields:    Translation:AnimalsCells
    7. Harvey JD, Heinbockel T. Neuromodulation of Synaptic Transmission in the Main Olfactory Bulb. Int J Environ Res Public Health. 2018 10 08; 15(10). PMID: 30297631.
      Citations: 5     Fields:    Translation:HumansCells
    8. Heinbockel T, Csoka AB. Epigenetic Effects of Drugs of Abuse. Int J Environ Res Public Health. 2018 09 25; 15(10). PMID: 30257440.
      Citations:    Fields:    Translation:HumansAnimals
    9. Amaye IJ, Heinbockel T, Woods J, Wang Z, Martin-Caraballo M, Jackson-Ayotunde P. 6 Hz Active Anticonvulsant Fluorinated N-Benzamide Enaminones and Their Inhibitory Neuronal Activity. Int J Environ Res Public Health. 2018 08 20; 15(8). PMID: 30127263.
      Citations: 1     Fields:    Translation:AnimalsCells
    10. Kanherkar RR, Getachew B, Ben-Sheetrit J, Varma S, Heinbockel T, Tizabi Y, Csoka AB. The Effect of Citalopram on Genome-Wide DNA Methylation of Human Cells. Int J Genomics. 2018; 2018:8929057. PMID: 30148158.
      Citations:    
    11. Getachew B, Hudson T, Heinbockel T, Csoka AB, Tizabi Y. Protective Effects of Donepezil Against Alcohol-Induced Toxicity in Cell Culture: Role of Caspase-3. Neurotox Res. 2018 Oct; 34(3):757-762. PMID: 29804239.
      Citations: 1     Fields:    Translation:HumansCells
    12. Wang ZJ, Heinbockel T. Essential Oils and Their Constituents Targeting the GABAergic System and Sodium Channels as Treatment of Neurological Diseases. Molecules. 2018 May 02; 23(5). PMID: 29724056.
      Citations: 2     Fields:    Translation:HumansAnimals
    13. Zou L, Xue Y, Jones M, Heinbockel T, Ying M, Zhan X. The Effects of Quinine on Neurophysiological Properties of Dopaminergic Neurons. Neurotox Res. 2018 07; 34(1):62-73. PMID: 29285614.
      Citations:    Fields:    Translation:HumansAnimalsCells
    14. Heinbockel T, Wang ZJ, Brown EA, Austin PT. Endocannabinoid signaling in neural circuits of the olfactory and limbic system. In: Cannabinoids in Health and Disease. Rosaria Meccariello and Rosanna Chianese (ed.). 2016; chapter 2:11-37. View Publication.
    15. Wang ZJ, Heinbockel T. Ginsenosides as brain signaling molecules and potential cures for neurological and neurodegenerative diseases. Horizons in Neuroscience Research (Costa A, Villalba E). 2016; 24:83-100.
    16. Heinbockel T, Wang ZJ. Cellular Mechanisms of Action of Drug Abuse on Olfactory Neurons. Int J Environ Res Public Health. 2015 Dec 22; 13(1):ijerph13010005. PMID: 26703658.
      Citations: 3     Fields:    Translation:HumansAnimalsCells
    17. Wang ZJ, Tabakoff B, Levinson SR, Heinbockel T. Inhibition of Nav1.7 channels by methyl eugenol as a mechanism underlying its antinociceptive and anesthetic actions. Acta Pharmacol Sin. 2015 Jul; 36(7):791-9. PMID: 26051112.
      Citations: 5     Fields:    Translation:HumansAnimalsCells
    18. Heinbockel T. Anandamide is a fast retrograde signaling molecule in neural circuits. In: Endocannabinoids: Chemical Structure, Role in Physiological Processes and Therapeutic Effects. Garza T (ed), Series: Neuroscience Research Progress. 2015; 25-42.
    19. Heinbockel T, Wang ZJ, Jackson-Ayotunde PL. Allosteric Modulation of GABAA Receptors by an Anilino Enaminone in an Olfactory Center of the Mouse Brain. Pharmaceuticals (Basel). 2014 Dec 17; 7(12):1069-90. PMID: 25525715.
      Citations:    
    20. Wang ZJ, Sun L, Heinbockel T. Resibufogenin and cinobufagin activate central neurons through an ouabain-like action. PLoS One. 2014; 9(11):e113272. PMID: 25420080.
      Citations: 3     Fields:    Translation:AnimalsCells
    21. Heinbockel T. Neurochemical communication: The case of endocannabinoids. In: Neurochemistry; Thomas Heinbockel (ed). 2014; chapter 6:179-198. View Publication.
    22. Heinbockel T. Neurochemistry. 2014; 414 pages. View Publication.
    23. Wang ZJ, Levinson SR, Sun L, Heinbockel T. Identification of both GABAA receptors and voltage-activated Na(+) channels as molecular targets of anticonvulsant a-asarone. Front Pharmacol. 2014; 5:40. PMID: 24653701.
      Citations:    
    24. Heinbockel T, Wang ZJ. Cannabinoid receptor- and metabotropic glutamate receptor-mediated signaling in neural circuits of the main olfactory bulb. Horizons in Neuroscience Research. Costa A, Villalba E (eds). 2014; 13:37-62.
    25. Young JK, Heinbockel T, Gondré-Lewis MC. Astrocyte fatty acid binding protein-7 is a marker for neurogenic niches in the rat hippocampus. Hippocampus. 2013 Dec; 23(12):1476-83. PMID: 23996503.
      Citations: 5     Fields:    Translation:AnimalsCells
    26. Zhan X, Yin P, Heinbockel T. The basal forebrain modulates spontaneous activity of principal cells in the main olfactory bulb of anesthetized mice. Front Neural Circuits. 2013; 7:148. PMID: 24065892.
      Citations: 8     Fields:    Translation:AnimalsCells
    27. Heinbockel T, Shields VD, Reisenman CE. Glomerular interactions in olfactory processing channels of the antennal lobes. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2013 Nov; 199(11):929-46. PMID: 23893248.
      Citations: 2     Fields:    Translation:AnimalsCells
    28. Wang ZJ, Sun L, Heinbockel T. Cannabinoid receptor-mediated regulation of neuronal activity and signaling in glomeruli of the main olfactory bulb. J Neurosci. 2012 Jun 20; 32(25):8475-9. PMID: 22723687.
      Citations: 13     Fields:    Translation:AnimalsCells
    29. Heinbockel T. Neuroscience. 2012; 138 pages. View Publication.
    30. Heinbockel T. Electrophysiological recording and imaging of neuronal signals in brain slices. In: Neuroscience; Thomas Heinbockel (ed.). 2012; chapter 2:19-48. View Publication.
    31. Shields VDC, Heinbockel T . Neurophysiological recording techniques applied to insect chemosensory systems. In: Zoology; Maria-Dolores Garcia (ed.). 2012; chapter 7:123-162. View Publication.
    32. Wang ZJ, Sun L, Peng W, Ma S, Zhu C, Fu F, Heinbockel T. Ginseng derivative ocotillol enhances neuronal activity through increased glutamate release: a possible mechanism underlying increased spontaneous locomotor activity of mice. Neuroscience. 2011 Nov 10; 195:1-8. PMID: 21864652.
      Citations: 6     Fields:    Translation:AnimalsCells
    33. Wang ZJ, Sun L, Jackson PL, Scott KR, Heinbockel T. A substituted anilino enaminone acts as a novel positive allosteric modulator of GABA(A) receptors in the mouse brain. J Pharmacol Exp Ther. 2011 Mar; 336(3):916-24. PMID: 21163867.
      Citations: 5     Fields:    Translation:AnimalsCells
    34. Dong HW, Heinbockel T, Hamilton KA, Hayar A, Ennis M. Metabotropic glutamate receptors and dendrodendritic synapses in the main olfactory bulb. Ann N Y Acad Sci. 2009 Jul; 1170:224-38. PMID: 19686141.
      Citations: 5     Fields:    Translation:HumansAnimalsCells
    35. Heinbockel T, Heyward PM. Glutamate synapses in olfactory neural circuits. In: Amino Acid Receptor Research; Paley BF, Warfield TE (eds). 2009; chapter 16:379-414.
    36. Reisenman CE, Heinbockel T, Hildebrand JG. Inhibitory interactions among olfactory glomeruli do not necessarily reflect spatial proximity. J Neurophysiol. 2008 Aug; 100(2):554-64. PMID: 18417626.
      Citations: 13     Fields:    Translation:AnimalsCells
    37. Heinbockel T, Ennis M. Metabotropic glutamate receptors and neural processing in the olfactory system. In: Neural Pathways Research; Pichler FL (ed). 2008; chapter 1:1-30.
    38. Heinbockel T, Hamilton KA, Ennis M. Group I metabotropic glutamate receptors are differentially expressed by two populations of olfactory bulb granule cells. J Neurophysiol. 2007 Apr; 97(4):3136-41. PMID: 17215500.
      Citations: 9     Fields:    Translation:AnimalsCells
    39. Heinbockel T, Laaris N, Ennis M. Metabotropic glutamate receptors in the main olfactory bulb drive granule cell-mediated inhibition. J Neurophysiol. 2007 Jan; 97(1):858-70. PMID: 17093122.
      Citations: 18     Fields:    Translation:AnimalsCells
    40. Ennis M, Zhu M, Heinbockel T, Hayar A. Olfactory nerve-evoked, metabotropic glutamate receptor-mediated synaptic responses in rat olfactory bulb mitral cells. J Neurophysiol. 2006 Apr; 95(4):2233-41. PMID: 16394070.
      Citations: 12     Fields:    Translation:AnimalsCells
    41. Heinbockel T, Brager DH, Reich CG, Zhao J, Muralidharan S, Alger BE, Kao JP. Endocannabinoid signaling dynamics probed with optical tools. J Neurosci. 2005 Oct 12; 25(41):9449-59. PMID: 16221855.
      Citations: 18     Fields:    Translation:AnimalsCells
    42. Hamilton KA, Heinbockel T, Ennis M, Szabó G, Erdélyi F, Hayar A. Properties of external plexiform layer interneurons in mouse olfactory bulb slices. Neuroscience. 2005; 133(3):819-29. PMID: 15896912.
      Citations: 17     Fields:    Translation:AnimalsCells
    43. Heinbockel T, Christensen TA, Hildebrand JG. Representation of binary pheromone blends by glomerulus-specific olfactory projection neurons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2004 Dec; 190(12):1023-37. PMID: 15378331.
      Citations: 14     Fields:    Translation:AnimalsCells
    44. Heinbockel T, Heyward P, Conquet F, Ennis M. Regulation of main olfactory bulb mitral cell excitability by metabotropic glutamate receptor mGluR1. J Neurophysiol. 2004 Nov; 92(5):3085-96. PMID: 15212418.
      Citations: 24     Fields:    Translation:AnimalsCells
    45. Hayar A, Heyward PM, Heinbockel T, Shipley MT, Ennis M. Direct excitation of mitral cells via activation of alpha1-noradrenergic receptors in rat olfactory bulb slices. J Neurophysiol. 2001 Nov; 86(5):2173-82. PMID: 11698509.
      Citations: 33     Fields:    Translation:AnimalsCells
    46. Pape HC, Driesang RB, Heinbockel T, Laxmi TR, Meis S, Seidenbecher T, Szinyei C, Frey U, Stork O. Cellular processes in the amygdala: gates to emotional memory? Zoology (Jena). 2001; 104(3-4):232-40. PMID: 16351838.
      Citations: 2     Fields:    
    47. Szinyei C, Heinbockel T, Montagne J, Pape HC. Putative cortical and thalamic inputs elicit convergent excitation in a population of GABAergic interneurons of the lateral amygdala. J Neurosci. 2000 Dec 01; 20(23):8909-15. PMID: 11102501.
      Citations: 33     Fields:    Translation:AnimalsCells
    48. Danober L, Heinbockel T, Driesang RB, Pape HC. Synaptic mechanisms of NMDA-mediated hyperpolarization in lateral amygdaloid projection neurons. Neuroreport. 2000 Aug 03; 11(11):2501-6. PMID: 10943711.
      Citations: 2     Fields:    Translation:AnimalsCells
    49. Kloppenburg P, Heinbockel T. 5-Hydroxy-tryptamine modulates pheromone-evoked local field potentials in the macroglomerular complex of the sphinx moth Manduca sexta. J Exp Biol. 2000 Jun; 203(Pt 11):1701-9. PMID: 10804160.
      Citations: 5     Fields:    Translation:AnimalsCells
    50. Heinbockel T, Pape HC. Input-specific long-term depression in the lateral amygdala evoked by theta frequency stimulation. J Neurosci. 2000 Apr 01; 20(7):RC68. PMID: 10729357.
      Citations: 13     Fields:    Translation:AnimalsCells
    51. Heinbockel T, Pape HC. Modulatory effects of adenosine on inhibitory postsynaptic potentials in the lateral amygdala of the rat. Br J Pharmacol. 1999 Sep; 128(1):190-6. PMID: 10498851.
      Citations: 3     Fields:    Translation:AnimalsCells
    52. Heinbockel T, Christensen TA, Hildebrand JG. Temporal tuning of odor responses in pheromone-responsive projection neurons in the brain of the sphinx moth Manduca sexta. J Comp Neurol. 1999 Jun 21; 409(1):1-12. PMID: 10363707.
      Citations: 25     Fields:    Translation:AnimalsCells
    53. Heinbockel T, Hildebrand JG. Antennal receptive fields of pheromone-responsive projection neurons in the antennal lobes of the male sphinx moth Manduca sexta. J Comp Physiol A. 1998 Aug; 183(2):121-33. PMID: 9693989.
      Citations: 3     Fields:    Translation:AnimalsCells
    54. Heinbockel T, Kloppenburg P, Hildebrand JG. Pheromone-evoked potentials and oscillations in the antennal lobes of the sphinx moth Manduca sexta. J Comp Physiol A. 1998 Jun; 182(6):703-14. PMID: 9631552.
      Citations: 14     Fields:    Translation:AnimalsCells
    55. Christensen TA, Heinbockel T, Hildebrand JG. Olfactory information processing in the brain: encoding chemical and temporal features of odors. J Neurobiol. 1996 May; 30(1):82-91. PMID: 8727985.
      Citations: 10     Fields:    Translation:Animals
    56. Hildebrand JG, Christensen TA, Heinbockel T, Roche King J, Mechaber W, Rössler W, Shields VDC. The olfactory neurobiology of host- and mate-attraction in moths. In: From Molecular Neurobiology to Clinical Neuroscience; Elsner N, Eysel U (eds). 1996; 1:56-67.
    57. Heinbockel T, Kaissling K-E . Variability of olfactory receptor neuron responses of female silkmoths (Bombyx mori L.) to benzoic acid and (+)-linalool. J Insect Physiol. 1996; 42:565-578.
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