Disinhibition of the midbrain colliculi unmasks coordinated autonomic, Respiratory, And somatomotor responses to auditory and visual stimuli

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 307, Issue 8, 2014, Pages R1025-R1035

  Müller Ribeiro, Flávia C F ^a,b   Dampney, Roger A L ^c   McMullan, Simon ^a   Fontes, Marco A P ^b   Goodchild, Ann K ^a  

^a MACQUARIE UNIVERSITY   (Australia)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Arterial pressure; Command neuron; Defensive behavior; Phrenic nerve activity; Sympathetic activity

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BICUCULLINE; PICROTOXIN;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTERIAL PRESSURE; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; AUTONOMIC NERVOUS SYSTEM FUNCTION; BRAIN FUNCTION; BRAIN STEM; DECEREBRATION; EVOKED AUDITORY RESPONSE; EVOKED RESPONSE; FOREBRAIN; HEART RATE; HYPOTHALAMUS; INFERIOR COLLICULUS; LATERAL HYPOTHALAMUS; MALE; MICROINJECTION; NERVE CELL; NEUROMUSCULAR BLOCKING; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PREFRONTAL CORTEX; RAT; RESPIRATORY FUNCTION; SOMATOSENSORY STIMULATION; SUPERIOR COLLICULUS; VISUAL STIMULATION; ANIMAL; ANIMAL MODEL; AUTONOMIC NERVOUS SYSTEM; DRUG EFFECTS; EVOKED VISUAL RESPONSE; MOTOR CORTEX; PATHOPHYSIOLOGY; PHOTOSTIMULATION; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TIME;

ACOUSTIC STIMULATION; ANIMALS; AUTONOMIC NERVOUS SYSTEM; DECEREBRATE STATE; EVOKED POTENTIALS, AUDITORY; EVOKED POTENTIALS, VISUAL; INFERIOR COLLICULI; MALE; MICROINJECTIONS; MODELS, ANIMAL; MOTOR CORTEX; PHOTIC STIMULATION; PICROTOXIN; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY PHYSIOLOGICAL PHENOMENA; SUPERIOR COLLICULI; TIME FACTORS;

EID: 84908056335     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00165.2014     Document Type: Article

References (50)

1. Belekhova MG, Kenigfest-Rio NB, Vesselkin NP, Rio JP, Reperant J, Ward R. Evolutionary significance of different neurochemical organisation of the internal and external regions of auditory centres in the reptilian brain: an immunocytochemical and reduced NADPH-diaphorase histochemical study in turtles. Brain Res 925: 100-106, 2002.
2. Brandao ML, Tomaz C, Leao Borges PC, Coimbra NC, Bagri A. Defense reaction induced by microinjections of bicuculline into the inferior colliculus. Physiol Behav 44: 361-365, 1988.
3. Casseday JH, Covey E. A neuroethological theory of the operation of the superior colliculus. Brain Behav Evol 47: 311-336, 1996.
4. Castellan-Baldan L, da Costa Kawasaki M., Ribeiro SJ, Calvo F, Correa VM, Coimbra NC. Topographic and functional neuroanatomical study of GABAergic disinhibitory striatum-nigral inputs and inhibitory nigrocollicular pathways: Neural hodology recruiting the substantia nigra, pars reticulata, for the modulation of the neural activity in the inferior colliculus involved with panic-like emotions. J Chem Neuroanat 32: 1-27, 2006.
5. Cohen JD, Castro-Alamancos MA. Early sensory pathways for detection of fearful conditioned stimuli: tectal and thalamic relays. J Neurosci 27: 7762-7776, 2007.
6. Cohen JD, Castro-Alamancos MA. Neural correlates of active avoidance behavior in superior colliculus. J Neurosci 30: 8502-8511, 2010.
7. Coimbra NC, Brandao ML. GABAergic nigro-collicular pathways modulate the defensive behaviour elicited by midbrain tectum stimulation. Behav Brain Res 59: 131-139, 1993.
8. Dean P, Redgrave P, Westby GW. Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci 12: 137-147, 1989.
9. Duque D, Perez-Gonzalez D, Ayala YA, Palmer AR, Malmierca MS. Topographic distribution, frequency, and intensity dependence of stimulus-specific adaptation in the inferior colliculus of the rat. J Neurosci 32: 17762-17774, 2012.
10. Gandhi NJ, Katnani HA. Motor functions of the superior colliculus. Ann Rev Neurosci 34: 205-231, 2011.
11. Garcia Del Cano G, Gerrikagoitia I, Alonso-Cabria A, Martinez-Millan L. Organization and origin of the connection from the inferior to the superior colliculi in the rat. J Comp Neurol 499: 716-731, 2006.
12. Goodchild AK, van Deurzen BTM, Hildreth CM, Pilowsky PM. Control of sympathetic, respiratory and somatomotor outflow by an intraspinal pattern generator. Clin Exp Pharmacol Physiol 35: 447-453, 2008.
13. Hagbarth RG, Hallin A, Hongell HE, Torebjörk HE, Wallin BG. General characteristics of sympathetic activity in human skin nerves. Acta Physiol Scand 84: 164-176, 1972.
14. Heffner HE, Heffner RS, Contos C, Ott T. Audiogram of the hooded Norway rat. Hear Res 73: 244-247, 1994.
15. Hirokawa J, Sadakane O, Sakata S, Bosch M, Sakurai Y, Yamamori T. Multisensory information facilitates reaction speed by enlarging activity difference between superior colliculus hemispheres in rats. PLoS One 6: e25283, 2011.
16. Huffman RF, Henson OW. The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus. Brain Res Rev 15: 295-323, 1990.
17. Iigaya K, Muller-Ribeiro FC, Horiuchi J, McDowall LM, Nalivaiko E, Fontes MAP, Dampney RAL. Synchronized activation of sympathetic vasomotor, cardiac, and respiratory outputs by neurons in the midbrain colliculi. Am J Physiol Regul Integr Comp Physiol 303: R599-R610, 2012.
18. Jääskeläinen IP, Ahveninen J, Belliveau JW, Raij T, Sams M. Shortterm plasticity in auditory cognition. Trends Neurosci 30: 653-661, 2007.
19. Jänig W. Preand postganglionic vasoconstrictor neurons: differentiation, types, and discharge properties. Annu Rev Physiol 50: 525-539, 1988.
20. Jen LS, Au C. Intercollicular fibers terminating in the superficial layers of the superior colliculus: a WHA-HRP study in the rat. Brain Res 379: 385-389, 1986.
21. Jiang ZD, Moore DR, King AJ. Sources of subcortical projections to the superior colliculus in the ferret. Brain Res 755: 279-292, 1997.
22. Johnson SW, Seutin V. Bicuculline methiodide potentiates NMDAdependent burst firing in rat dopamine neurons by blocking apaminsensitive Ca2-activated K currents. Neurosci Lett 231: 13-16, 1997.
23. Keay KA, Dean P, Redgrave P. N-methyl D-aspartate (NMDA) evoked changes in blood pressure and heart rate from the rat superior colliculus. Exp Brain Res 80: 148-156, 1990.
24. Keay KA, Redgrave P, Dean P. Cardiovascular and respiratory changes elicited by stimulation of rat superior colliculus. Brain Res Bull 20: 13-26, 1998.
25. Kenney MJ, Weiss ML, Patel KP, Wang Y, Fels RJ. Paraventricular nucleus bicuculline alters frequency components of sympathetic nerve discharge bursts. Am J Physiol Heart Circ Physiol 281: H1233-H1241, 2001.
26. Kenney MJ, Weiss ML, Mendes T, Wang Y, Fels RJ. Role of paraventricular nucleus in regulation of sympathetic nerve frequency components. Am J Physiol Heart Circ Physiol 284: H1710-H1720, 2003.
27. King AJ, Palmer AR. Integration of visual and auditory information in bimodal neurones in the guinea-pig superior colliculus. Exp Brain Res 60: 492-500, 1985.
28. Kleiman-Weiner M, Beenhakker MP, Segal WA, Huguenard JR. Synergistic roles of GABAA receptors and SK channels in regulating thalamocortical oscillations. J Neurophysiol 102: 203-213, 2009.
29. LeDoux JE. Brain mechanisms of emotion and emotional learning. Curr Opinion Neurobiol 2: 191-197, 1992.
30. Malmierca MS, Cristaudo S, Peérez-Gonzaález D, Covey E. Stimulusspecific adaptation in the inferior colliculus of the anesthetized rat. J Neurosci 29: 5483-5493, 2009.
31. May PJ. The mammalian superior colliculus: laminar structure and connections. Prog Brain Res 151: 321-378, 2006.
32. McDowall LM, Horiuchi J, Dampney RA. Effects of disinhibition of neurons in the dorsomedial hypothalamus on central respiratory drive. Am J Physiol Regul Integr Comp Physiol 293: R1728-R1735, 2007.
33. Meredith MA, Stein BE. Spatial factors determine the activity of multisensory neurons in cat superior colliculus. Brain Res 365: 350-354, 1986.
34. Meredith MA, Stein BE. Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. J Neurophysiol 356: 640-662, 1986.
35. Mize RR. The organization of GABAergic neurons in the mammalian superior colliculus. Prog Brain Res 90: 219-248, 1992.
36. Nobre MJ, Lopes MG, Brandao ML. Defense reaction mediated by NMDA mechanisms in the inferior colliculus is modulated by GABAergic nigro-collicular pathways. Brain Res 999: 124-131, 2004.
37. Padley JR, Li Q, Pilowsky PM, Goodchild AK. Cannabinoid receptor activation in the rostral ventrolateral medulla oblongata evokes cardiorespiratory effects in anaesthetised rats. Br J Pharmacol 140: 384-394, 2003.
38. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. New York: Academic, 2004.
39. Pellet J. Neural organization in the brainstem circuit mediating the primary acoustic head startle: an electrophysiological study in the rat. Physiol Behav 48: 727-739, 1990.
40. Pickering M, Jones JF. Comparison of the motor discharge to the crural and costal diaphragm in the rat. Respir Physiol Neurobiol 159: 21-27, 2007.
41. Redgrave P, Marrow L, Dean P. Topographical organization of the nigrotetal projection in rat: evidence for segregated channels. Neuroscience 50: 571-595, 1992.
42. Redgrave P, Mitchell IJ, Dean P. Descending projections from the superior colliculus in rat: a study using orthograde transport of wheatgermagglutinin conjugated horseradish peroxidase. Exp Brain Res 68: 47-167, 1987.
43. Schmalbruch H. Fiber composition of the rat sciatic nerve. Anat Rec 215: 71-81, 1986.
44. Semyanox A, Walker MC, Kullmann DM, Silver RA. Tonically active GABAA receptors: modulating gain and maintaining the tone. Trends Neurosci 27: 71-81, 1986.
45. Soltis RP, DiMicco JA. Interaction of hypothalamic GABAA and excitatory amino acid receptors controlling heart rate in rats. Am J Physiol Regul Integr Comp Physiol 261: R427-R433, 1991.
46. Stein BE. Neural mechanisms for synthesizing sensory information and producing adaptive behaviors. Exp Brain Res 123: 124-135, 1998.
47. Stein BE, Gaither NS. Sensory representation in reptilian optic tectum: some comparisons with mammals. J Comp Neurol 202: 69-87, 1981.
48. Thomas PK, Jefferys JGR, Sharma AK, Bajada S. Nerve conduction velocity in experimental diabetes in the rat and rabbit. J Neurol Neurosurg Psychiatry 44: 233-238, 1981.
49. Ulanovsky N, Las L, Nelken I. Processing of low-probability sounds by cortical neurons. Nat Neurosci 6: 391-398, 2003.
50. Wiberg M, Westman J, Blomqvist A. Somatosensory projection to the mesencephalon: an anatomical study in the monkey. J Comp Neurol 264: 92-117, 1987.