Advertisement

The extraordinary partnership of Geoff Burnstock and Mollie Holman

  • Nick J. Spencer
    Correspondence
    Corresponding author at: College of Medicine and Public Health, Department of Human Physiology, Flinders University, GPO Box 2100, Adelaide, South Australia, Australia.
    Affiliations
    College of Medicine and Public Health, Department of Human Physiology, Flinders University, Bedford Park, South Australia 5042, Australia
    Search for articles by this author
  • Marcello Costa
    Affiliations
    College of Medicine and Public Health, Department of Human Physiology, Flinders University, Bedford Park, South Australia 5042, Australia
    Search for articles by this author

      Abstract

      Here, we recognise some of the extraordinary accomplishments of the partnership between Geoff Burnstock and Mollie Holman, and the everlasting impact they both made in autonomic neuroscience in Australia. Much of strength today in autonomic neuroscience can be traced back to a time when Geoff and Mollie commenced their seminal studies on autonomic neuroscience, initially at Oxford, then at The University of Melbourne in the mid 1960's. Mollie and Geoff published their first paper together, at Oxford, with their then mentor, and doyenne of smooth muscle, Professor Edith Bülbring. They did not always agree on the interpretation of their own scientific findings. Geoff was convinced early on that Adenosine triphosphate (ATP), or a related purine, was an excitatory neurotransmitter at peripheral sympathetic neuroeffector junctions. Mollie was reticent for decades. However, she began to take the notion seriously that ATP maybe a neurotransmitter, when receptors for purines were identified in the 1990's. What the partnership between Mollie and Geoff taught us in Australia was to not fear respectful criticism, but rather to be receptive to and embrace objective, collegial and constructive scientific peer-review. One of the many great legacies of Geoff and Mollie was the large number of researchers, who were fortunate disciples of their supervision, and who have now themselves gone on to make significant discoveries in autonomic and visceral neuroscience. This review summarizes some of their major legacies and represents a very personal historical perspective of the two authors, pupils respectively of Mollie and Geoff.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Autonomic Neuroscience: Basic and Clinical
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Bayliss W.M.
        • Starling E.H.
        The movements and innervation of the small intestine.
        J. Physiol. 1899; 24: 99-143
        • Benard T.
        • Bouchoucha M.
        • Dupres M.
        • Cugnenc P.H.
        In vitro analysis of rat intestinal wall movements at rest and during propagated contraction: a new method.
        Am. J. Phys. 1997; 273: G776-G784
        • Bercik P.
        • Bouley L.
        • Dutoit P.
        • Blum A.L.
        • Kucera P.
        Quantitative analysis of intestinal motor patterns: spatiotemporal organization of nonneural pacemaker sites in the rat ileum.
        Gastroenterology. 2000; 119: 386-394
        • Blessing W.W.
        • Costa M.
        • Geffen L.B.
        • Rush R.A.
        Immune lesions of central noradrenergic nerves in the rat produced by antibodies to dopamine-beta-hydroxylase.
        Clin. Exp. Neurol. 1978; 15: 307-308
        • Blessing W.W.
        • Furness J.B.
        • Costa M.
        • West M.J.
        • Chalmers J.P.
        Projection of ventrolateral medullary (A1) catecholamine neurons toward nucleus tractus solitarii.
        Cell Tissue Res. 1981; 220: 27-40
        • Bornstein J.F.J.
        Enteric neural regulation of mucosal secretion.
        in: Elsevier E. H. M. S. Physiology of the gastrointestinal tract. 2018
        • Bornstein J.C.
        • North R.A.
        • Costa M.
        • Furness J.B.
        Excitatory synaptic potentials due to activation of neurons with short projections in the myenteric plexus.
        Neuroscience. 1984; 11: 723-731
        • Brookes S.J.
        • Steele P.A.
        • Costa M.
        Identification and immunohistochemistry of cholinergic and non-cholinergic circular muscle motor neurons in the guinea-pig small intestine.
        Neuroscience. 1991; 42: 863-878
        • Brookes S.J.H.
        • Spencer N.J.
        • Costa M.
        • Zagorodnyuk V.P.
        Extrinsic primary afferent signalling in the gut.
        Nat. Rev. Gastroenterol. Hepatol. 2013; 10: 286-296https://doi.org/10.1038/nrgastro.2013.29
        • Burnstock G.
        Do some nerve cells release more than one transmitter?.
        Neuroscience. 1976; 1: 239-248
        • Burnstock G.
        • Holman M.E.
        Effect of denervation and of reserpine treatment on transmission at sympathetic nerve endings.
        J. Physiol. 1962; 160: 461-469
        • Burnstock G.
        • Holman M.E.
        Smooth muscle: autonomic nerve transmission.
        Annu. Rev. Physiol. 1963; 25: 61-90
        • Burnstock G.
        • Campbell G.
        • Bennett M.
        • Holman M.E.
        Inhibition of the smooth muscle on the taenia coli.
        Nature. 1963; 200: 581-582
        • Burnstock G.
        • Holman M.E.
        • Prosser C.L.
        Electrophysiology of smooth muscle.
        Physiol. Rev. 1963; 43: 482-527
        • Burnstock G.
        • Campbell G.
        • Bennett M.
        • Holman M.E.
        Innervation of the guinea-pig taenia coli: are there intrinsic inhibitory nerves which are distinct from sympathetic nerves?.
        Int. J. Neuropharmacol. 1964; 3: 163-166
        • Burnstock G.
        • Campbell G.
        • Satchell D.
        • Smythe A.
        Evidence that adenosine triphosphate or a related nucleotide is the transmitter substance released by non-adrenergic inhibitory nerves in the gut.
        Br. J. Pharmacol. 1970; 40: 668-688
        • Bywater R.A.
        • Small R.C.
        • Taylor G.S.
        Neurogenic slow depolarizations and rapid oscillations in the membrane potential of circular muscle of mouse colon.
        J. Physiol. 1989; 413: 505-519
        • Costa M.
        • Furness J.B.
        The peristaltic reflex: an analysis of the nerve pathways and their pharmacology.
        Naunyn Schmiedeberg’s Arch. Pharmacol. 1976; 294: 47-60
        • Costa M.
        • Furness J.B.
        • Gabella G.
        Catecholamine containing nerve cells in the mammalian myenteric plexus.
        Histochemie. 1971; 25: 103-106
        • Costa M.
        • Furness J.B.
        • Smith I.J.
        • Davies B.
        • Oliver J.
        An immunohistochemical study of the projections of somatostatin-containing neurons in the guinea-pig intestine.
        Neuroscience. 1980; 5: 841-852
        • Costa M.
        • Furness J.B.
        • Cuello A.C.
        • Verhofstad A.A.
        • Steinbusch H.W.
        • Elde R.P.
        Neurons with 5-hydroxytryptamine-like immunoreactivity in the enteric nervous system: their visualization and reactions to drug treatment.
        Neuroscience. 1982; 7: 351-363
        • Costa M.
        • Furness J.B.
        • Pullin C.O.
        • Bornstein J.
        Substance P enteric neurons mediate non-cholinergic transmission to the circular muscle of the guinea-pig intestine.
        Naunyn Schmiedeberg’s Arch. Pharmacol. 1985; 328: 446-453
        • Costa M.
        • Furness J.B.
        • Gibbins I.L.
        Chemical coding of enteric neurons.
        Prog. Brain Res. 1986; 68: 217-239
        • Costa M.
        • Furness J.B.
        • Humphreys C.M.
        Apamin distinguishes two types of relaxation mediated by enteric nerves in the guinea-pig gastrointestinal tract.
        Naunyn Schmiedeberg’s Arch. Pharmacol. 1986; 332: 79-88
        • Costa M.
        • Brookes S.J.
        • Steele P.A.
        • Gibbins I.
        • Burcher E.
        • Kandiah C.J.
        Neurochemical classification of myenteric neurons in the Guinea-pig ileum.
        Neuroscience. 1996; 75: 949-967
        • Costa M.
        • Sanders K.M.
        • Schemann M.
        • Smith T.K.
        • Cook I.J.
        • De Giorgio R.
        • Dent J.
        • Grundy D.
        • Shea-Donohue T.
        • Tonini M.
        • Brookes S.J.
        • Varenna G.
        A teaching module on cellular control of small intestinal motility.
        Neurogastroenterol. Motil. 2005; 17: 4-19
        • Costa M.
        • Keightley L.J.
        • Wiklendt L.
        • Hibberd T.J.
        • Arkwright J.W.
        • Omari T.
        • Wattchow D.A.
        • Brookes S.J.H.
        • Dinning P.G.
        • Spencer N.J.
        Identification of multiple distinct neurogenic motor patterns that can occur simultaneously in the guinea pig distal colon.
        Am. J. Physiol. Gastrointest. Liver Physiol. 2019; 316: G32-G44
        • Costa M.
        • Keightley L.J.
        • Wiklendt L.
        • Hibberd T.J.
        • Arkwright J.W.
        • Omari T.
        • Wattchow D.A.
        • Zagorodnyuk V.
        • Brookes S.J.H.
        • Dinning P.G.
        • Spencer N.J.
        Roles of three distinct neurogenic motor patterns during pellet propulsion in guinea pig distal colon.
        J. Physiol. 2019; 597: 5125-5140
        • Furness J.B.
        An examination of nerve-mediated, hyoscine-resistant excitation of the guinea-pig colon.
        J. Physiol. 1970; 207: 803-821
        • Furness J.B.
        The origin and distribution of adrenergic nerve fibres in the guinea-pig colon.
        Histochemie. 1970; 21: 295-306
        • Furness J.B.
        The Enteric Nervous System.
        Blackwell Publishing, Oxford, U.K2006
        • Furness J.B.
        • Costa M.
        The nervous release and the action of substances which affect intestinal muscle through neither adrenoreceptors nor cholinoreceptors.
        Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 1973; 265: 123-133
        • Furness J.B.
        • Costa M.
        Types of nerves in the enteric nervous system.
        Neuroscience. 1980; 5: 1-20https://doi.org/10.1016/0306-4522(80)90067-6
        • Furness J.B.
        • Costa M.
        The Enteric Nervous System.
        Churchill Livingston, Edinburgh, U.K1987
        • Furness J.B.
        • Morris J.L.
        • Gibbins I.L.
        • Costa M.
        Chemical coding of neurons and plurichemical transmission.
        Annu. Rev. Pharmacol. Toxicol. 1989; 29: 289-306
        • Gabella G.
        • Costa M.
        Le fibre adrenergiche del canale alimentare. Giorn. Acc. Med. Torino.
        130. 1967: 1-12
        • Hennig G.W.
        • Costa M.
        • Chen B.N.
        • Brookes S.J.
        Quantitative analysis of peristalsis in the guinea-pig small intestine using spatio-temporal maps.
        J. Physiol. 1999; 517: 575-590
        • Hirst G.D.
        • Edwards F.R.
        Role of interstitial cells of Cajal in the control of gastric motility.
        J. Pharmacol. Sci. 2004; 96: 1-10
        • Hirst G.D.
        • Holman M.E.
        • Spence I.
        Two types of neurones in the myenteric plexus of duodenum in the guinea-pig.
        J. Physiol. 1974; 236: 303-326
        • McLachlan E.M.
        Diversity of sympathetic vasoconstrictor pathways and their plasticity after spinal cord injury.
        Clin. Auton. Res. 2007; 17: 6-12
        • Nishi S.
        • North R.A.
        Intracellular recording from the myenteric plexus of the guinea-pig ileum.
        J. Physiol. 1973; 231: 471-491
        • Porter A.J.
        • Wattchow D.A.
        • Hunter A.
        • Costa M.
        Abnormalities of nerve fibers in the circular muscle of patients with slow transit constipation.
        Int. J. Color. Dis. 1998; 13: 208-216
        • Song Z.M.
        • Brookes S.J.
        • Costa M.
        All calbindin-immunoreactive myenteric neurons project to the mucosa of the guinea-pig small intestine.
        Neurosci. Lett. 1994; 180: 219-222
        • Song Z.M.
        • Brookes S.J.
        • Costa M.
        Characterization of alkaline phosphatase-reactive neurons in the guinea-pig small intestine.
        Neuroscience. 1994; 63: 1153-1167
        • Song Z.M.
        • Brookes S.J.
        • Ramsay G.A.
        • Costa M.
        Characterization of myenteric interneurons with somatostatin immunoreactivity in the guinea-pig small intestine.
        Neuroscience. 1997; 80: 907-923
        • Spencer N.J.
        • Hu H.
        Enteric nervous system: sensory transduction, neural circuits and gastrointestinal motility.
        Nat. Rev. Gastroenterol. Hepatol. 2020; 17: 338-351
        • Spencer N.J.
        • Dinning P.G.
        • Brookes S.J.
        • Costa M.
        Insights into the mechanisms underlying colonic motor patterns.
        J. Physiol. 2016; 594: 4099-4116
        • Spencer N.J.
        • Hibberd T.J.
        • Travis L.
        • Wiklendt L.
        • Costa M.
        • Hu H.
        • Brookes S.J.
        • Wattchow D.A.
        • Dinning P.G.
        • Keating D.J.
        • Sorensen J.
        Identification of a rhythmic firing pattern in the enteric nervous system that generates rhythmic electrical activity in smooth muscle.
        J. Neurosci. 2018; 38: 5507-5522
        • Spencer N.J.
        • Costa M.
        • Hibberd T.J.
        • Wood J.D.
        Advances in colonic motor complexes in mice.
        Am. J. Physiol. Gastrointest. Liver Physiol. 2021; 320: G12-G29
        • The Royal Society
        • Tonini M.
        • Costa M.
        A pharmacological analysis of the neuronal circuitry involved in distension-evoked enteric excitatory reflex.
        Neuroscience. 1990; 38: 787-795
        • Tonini M.
        • Waterman S.A.
        • Candura S.M.
        • Coccini T.
        • Costa M.
        Sites of action of morphine on the ascending excitatory reflex in the guinea-pig small intestine.
        Neurosci. Lett. 1992; 144: 195-198
        • Vickers J.C.
        • Costa M.
        The neurofilament triplet is present in distinct subpopulations of neurons in the central nervous system of the guinea-pig.
        Neuroscience. 1992; 49: 73-100
        • Vickers J.C.
        • Dickson T.C.
        • Adlard P.A.
        • Saunders H.L.
        • King C.E.
        • McCormack G.
        The cause of neuronal degeneration in Alzheimer's disease.
        Prog. Neurobiol. 2000; 60: 139-1396
        • Waterman S.A.
        • Costa M.
        • Tonini M.
        Accommodation mediated by enteric inhibitory reflexes in the isolated guinea-pig small intestine.
        J. Physiol. 1994; 474: 539-546
        • Wattchow D.A.
        • Porter A.J.
        • Brookes S.J.
        • Costa M.
        The polarity of neurochemically defined myenteric neurons in the human colon.
        Gastroenterology. 1997; 113: 497-506
        • Wood J.D.
        Electrical activity of the intestine of mice with hereditary megacolon and absence of enteric ganglion cells.
        Am J Dig Dis. 1973; 18: 477-488