Neural substrates underlying fear-evoked freezing: The periaqueductal grey-cerebellar link

Journal of Physiology

Volumn 592, Issue 10, 2014, Pages 2197-2213

  Koutsikou, Stella ^a   Crook, Jonathan J ^a   Earl, Emma V ^a   Leith, J Lianne ^a   Watson, Thomas C ^a   Lumb, Bridget M ^a   Apps, Richard ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ALPHA NERVE FIBER; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CEREBELLUM; CEREBELLUM CORTEX; CLIMBING FIBER; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; EMOTIONALITY; EVOKED MUSCLE RESPONSE; FREEZING; MALE; MEDULLARY PYRAMID; MUSCLE TONE; NERVE CELL NETWORK; NONHUMAN; OPEN FIELD TEST; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAT; SENSORY NERVE; SURVIVAL; ANIMAL; CATALEPSY; FEAR; MOVEMENT (PHYSIOLOGY); NERVE TRACT; PHYSIOLOGY; REFLEX; WISTAR RAT;

ANIMALS; CEREBELLUM; FEAR; FREEZING REACTION, CATALEPTIC; MALE; MOVEMENT; NERVE NET; NEURAL PATHWAYS; PERIAQUEDUCTAL GRAY; RATS; RATS, WISTAR; REFLEX;

EID: 84900521994     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.268714     Document Type: Article

References (78)

1. Apps R (1990). Columnar organisation of the inferior olive projection to the posterior lobe of the rat cerebellum. J Comp Neurol 302, 236-254.
2. Bastian AJ (2011). Moving, sensing and learning with cerebellar damage. Curr Opin Neurobiol 21, 596-601.
3. Berntson GG, Potolicchio SJ Jr & Miller NE (1973). Evidence for higher functions of the cerebellum: eating and grooming elicited by cerebellar stimulation in cats. Proc Natl Acad Sci U S A 70, 2497-2499.
4. Berntson GG & Schumacher KM (1980). Effects of cerebellar lesions on activity, social interactions, and other motivated behaviors in the rat. J Comp Physiol Psychol 94, 706-717.
5. Berntson GG & Torello MW (1982). The paleocerebellum and the integration of behavioral function. Physiol Psychol 10, 2-12.
6. Blanchard RJ & Blanchard DC (1969). Crouching as an index of fear. J Comp Physiol Psychol 67, 370-375.
7. Blanchard RJ, Blanchard DC, Weiss SM & Meyer S (1990). The effects of ethanol and diazepam on reactions to predatory odors. Pharmacol Biochem Behav 35, 775-780.
8. Blenkinsop TA & Lang EJ (2011). Synaptic action of the olivocerebellar system on cerebellar nuclear spike activity. J Neurosci 31, 14708-14720.
9. Boorman GI, Hoffer JA, Kallesoe K, Viberg D & Mah C (1996). A measure of peripheral nerve stimulation efficacy applicable to H-reflex studies. Can J Neurol Sci 23, 264-270.
10. Carrive P, Leung P, Harris J & Paxinos G (1997). Conditioned fear to context is associated with increased Fos expression in the caudal ventrolateral region of the midbrain periaqueductal gray. Neuroscience 78, 165-177.
11. Cerminara NL, Koutsikou S, Lumb BM & Apps R (2009). The periaqueductal grey modulates sensory input to the cerebellum: a role in coping behaviour? Eur J Neurosci 29, 2197-2206.
12. Cerminara NL & Rawson JA (2004). Evidence that climbing fibers control an intrinsic spike generator in cerebellar Purkinje cells. J Neurosci 24, 4510-4517.
13. Cryan JF & Sweeney FF (2011). The age of anxiety: role of animal models of anxiolytic action in drug discovery. Br J Pharmacol 164, 1129-1161.
14. Davies HE & Edgley SA (1994). Inputs to group II-activated midlumbar interneurones from descending motor pathways in the cat. J Physiol 479, 463-473.
15. Dielenberg RA & McGregor IS (2001). Defensive behavior in rats towards predatory odors: a review. Neurosci Biobehav Rev 25, 597-609.
16. Dietrichs E (1983). Cerebellar cortical afferents from the periaqueductal grey in the cat. Neurosci Lett 41, 21-26.
17. Goodchild AK, Dampney RA & Bandler R (1982). A method for evoking physiological responses by stimulation of cell bodies, but not axons of passage, within localized regions of the central nervous system. J Neurosci Methods 6, 351-363.
18. Gordon M, Rubia FJ & Strata P (1973). The effect of pentothal on the activity evoked in the cerebellar cortex. Exp Brain Res 17, 50-62.
19. Gozariu M, Roth V, Keime F, Le Bars D & Willer JC (1998). An electrophysiological investigation into the monosynaptic H-reflex in the rat. Brain Res 782, 343-347.
20. Gross CT & Canteras NS (2012). The many paths to fear. Nat Rev Neurosci 13, 651-658.
21. Hopyan T, Laughlin S & Dennis M (2010). Emotions and their cognitive control in children with cerebellar tumors. J Int Neuropsychol Soc 16, 1027-1038.
22. Huang CM & Liu GL (1991). Auditory responses in the posterior vermis of the cat: the buried cerebellar cortex. Brain Res 553, 201-205.
23. Johansen JP, Cain CK, Ostroff LE & LeDoux JE (2011). Molecular mechanisms of fear learning and memory. Cell 147, 509-524.
24. Joyal CC, Strazielle C & Lalonde R (2001). Effects of dentate nucleus lesions on spatial and postural sensorimotor learning in rats. Behav Brain Res 122, 131-137.
25. Keay KA & Bandler R (2001). Parallel circuits mediating distinct emotional coping reactions to different types of stress. Neurosci Biobehav Rev 25, 669-678.
26. Kennedy PR, Ross HG & Brooks VB (1982). Participation of the principal olivary nucleus in neocerebellar motor control. Exp Brain Res 47, 95-104.
27. King RB (1948). The olivo-cerebella system; the effect of interolivary lesions on muscle tone in the trunk and limb girdles. J Comp Neurol 89, 207-223.
28. Koutsikou S, Parry DM, MacMillan FM & Lumb BM (2007). Laminar organization of spinal dorsal horn neurones activated by C- vs. A-heat nociceptors and their descending control from the periaqueductal grey in the rat. Eur J Neurosci 26, 943-952.
29. Lance JW (1980). The control of muscle tone, reflexes, and movement: Robert Wartenberg Lecture. Neurology 30, 1303-1313.
30. Larsell O (1952). The morphogenesis and adult pattern of the lobules and fissures of the cerebellum of the white rat. J Comp Neurol 97, 281-356.
31. LeDoux J (2012). Rethinking the emotional brain. Neuron 73, 653-676.
32. LeDoux JE, Iwata J, Cicchetti P & Reis DJ (1988). Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 8, 2517-2529.
33. Leith JL, Koutsikou S, Lumb BM & Apps R (2010). Spinal processing of noxious and innocuous cold information: differential modulation by the periaqueductal gray. J Neurosci 30, 4933-4942.
34. Leman S, Dielenberg RA & Carrive P (2003). Effect of dorsal periaqueductal gray lesion on cardiovascular and behavioural responses to contextual conditioned fear in rats. Behav Brain Res 143, 169-176.
35. Lipski J, Bellingham MC, West MJ & Pilowsky P (1988). Limitations of the technique of pressure microinjection of excitatory amino acids for evoking responses from localized regions of the CNS. J Neurosci Methods 26, 169-179.
36. Llewellyn-Smith IJ, Martin CL, Arnolda LF & Minson JB (2000). Tracer-toxins: cholera toxin B-saporin as a model. J Neurosci Methods 103, 83-90.
37. Lovick TA & Bandler R (2005). The organisation of the midbrain periaqueductal grey and the integration of pain behaviours. In The Neurobiology of Pain, ed. Hunt SP & Koltzenburg M, pp. 267-287. Oxford UP, Oxford.
38. McDevitt CJ, Ebner TJ & Bloedel JR (1982). The changes in Purkinje cell simple spike activity following spontaneous climbing fiber inputs. Brain Res 237, 484-491.
39. McMullan S & Lumb BM (2006). Midbrain control of spinal nociception discriminates between responses evoked by myelinated and unmyelinated heat nociceptors in the rat. Pain 124, 59-68.
40. Mantyh PW (1983). Connections of midbrain periaqueductal gray in the monkey. II. Descending efferent projections. J Neurophysiol 49, 582-594.
41. Mattsson JL, Albee RR & Brandt LM (1984). H-reflex waveform and latency variability in rats. Fundam Appl Toxicol 4, 944-948.
42. Merrill EG & Ainsworth A (1972). Glass-coated platinum-plated tungsten microelectrodes. Med Biol Eng 10, 662-672.
43. Misslin R (2003). The defense system of fear: behavior and neurocircuitry. Neurophysiol Clin 33, 55-66.
44. Monassi CR, Leite-Panissi CR & Menescal-de-Oliveira L (1999). Ventrolateral periaqueductal gray matter and the control of tonic immobility. Brain Res Bull 50, 201-208.
45. Morgan MM & Carrive P (2001). Activation of the ventrolateral periaqueductal gray reduces locomotion but not mean arterial pressure in awake, freely moving rats. Neuroscience 102, 905-910.
46. Mouton LJ & Holstege G (1994). The periaqueductal gray in the cat projects to lamina VIII and the medial part of lamina VII throughout the length of the spinal cord. Exp Brain Res 101, 253-264.
47. Pardoe J & Apps R (2002). Structure-function relations of two somatotopically corresponding regions of the rat cerebellar cortex: olivo-cortico-nuclear connections. Cerebellum 1, 165-184.
48. Parsons RG & Ressler KJ (2013). Implications of memory modulation for post-traumatic stress and fear disorders. Nat Neurosci 16, 146-153.
49. Paxinos G & Watson C (2005). The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego, CA USA.
50. Pellow S, Chopin P, File SE & Briley M (1985). Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14, 149-167.
51. Pijpers A, Winkelman BH, Bronsing R & Ruigrok TJ (2008). Selective impairment of the cerebellar C1 module involved in rat hind limb control reduces step-dependent modulation of cutaneous reflexes. J Neurosci 28, 2179-2189.
52. Reis DJ, Doba N & Nathan MA (1973). Predatory attack, grooming, and consummatory behaviors evoked by electrical stimulation of cat cerebellar nuclei. Science 182, 845-847.
53. Roste LS, Dietrichs E & Walberg F (1985). A projection from the periaqueductal grey to the lateral reticular nucleus in the cat. Anat Embryol (Berl) 172, 339-343.
54. Rutherford JG, Anderson WA & Gwyn DG (1984). A reevaluation of midbrain and diencephalic projections to the inferior olive in rat with particular reference to the rubro-olivary pathway. J Comp Neurol 229, 285-300.
55. Sacchetti B, Baldi E, Lorenzini CA & Bucherelli C (2002). Cerebellar role in fear-conditioning consolidation. Proc Natl Acad Sci U S A 99, 8406-8411.
56. Sacchetti B, Sacco T & Strata P (2007). Reversible inactivation of amygdala and cerebellum but not perirhinal cortex impairs reactivated fear memories. Eur J Neurosci 25, 2875-2884.
57. Sacchetti B, Scelfo B & Strata P (2009). Cerebellum and emotional behavior. Neuroscience 162, 756-762.
58. Sacchetti B, Scelfo B, Tempia F & Strata P (2004). Long-term synaptic changes induced in the cerebellar cortex by fear conditioning. Neuron 42, 973-982.
59. Schieppati M (1987). The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol 28, 345-376.
60. Schmahmann JD & Sherman JC (1998). The cerebellar cognitive affective syndrome. Brain 121, 561-579.
61. Seoane A, Apps R, Balbuena E, Herrero L & Llorens J (2005). Differential effects of trans-crotononitrile and 3-acetylpyridine on inferior olive integrity and behavioural performance in the rat. Eur J Neurosci 22, 880-894.
62. Sillery E, Bittar RG, Robson MD, Behrens TE, Stein J, Aziz TZ & Johansen-Berg H (2005). Connectivity of the human periventricular-periaqueductal gray region. J Neurosurg 103, 1030-1034.
63. Strata P, Scelfo B & Sacchetti B (2011). Involvement of cerebellum in emotional behavior. Physiol Res 60 (Suppl. 1), S39-48.
64. Sugihara I & Shinoda Y (2004). Molecular, topographic, and functional organization of the cerebellar cortex: a study with combined aldolase C and olivocerebellar labeling. J Neurosci 24, 8771-8785.
65. Supple WF Jr & Leaton RN (1990). Lesions of the cerebellar vermis and cerebellar hemispheres: effects on heart rate conditioning in rats. Behav Neurosci 104, 934-947.
66. Swenson RS & Castro AJ (1983a). The afferent connections of the inferior olivary complex in rats: a study using the retrograde transport of horseradish peroxidase. Am J Anat 166, 329-341.
67. Swenson RS & Castro AJ (1983b). The afferent connections of the inferior olivary complex in rats. An anterograde study using autoradiographic and axonal degeneration techniques. Neuroscience 8, 259-275.
68. Turner BM, Paradiso S, Marvel CL, Pierson R, Boles Ponto LL, Hichwa RD & Robinson RG (2007). The cerebellum and emotional experience. Neuropsychologia 45, 1331-1341.
69. Vianna DM, Graeff FG, Brandao ML & Landeira-Fernandez J (2001a). Defensive freezing evoked by electrical stimulation of the periaqueductal gray: comparison between dorsolateral and ventrolateral regions. Neuroreport 12, 4109-4112.
70. Vianna DM, Graeff FG, Landeira-Fernandez J & Brandão ML (2001b). Lesion of the ventral periaqueductal gray reduces conditioned fear but does not change freezing induced by stimulation of the dorsal periaqueductal gray. Learn Mem 8, 164-169.
71. Walker P & Carrive P (2003). Role of ventrolateral periaqueductal gray neurons in the behavioral and cardiovascular responses to contextual conditioned fear and poststress recovery. Neuroscience 116, 897-912.
72. Waters AJ & Lumb BM (2008). Descending control of spinal nociception from the periaqueductal grey distinguishes between neurons with and without C-fibre inputs. Pain 134, 32-40.
73. Watson TC, Koutsikou S, Cerminara NL, Flavell CR, Crook JJ, Lumb BM & Apps R (2013). The olivo-cerebellar system and its relationship to survival circuits. Front Neural Circuits 7, 72.
74. Welsh JP, Lang EJ, Suglhara I & Llinás R (1995). Dynamic organization of motor control within the olivocerebellar system. Nature 374, 453-457.
75. Welsh JP & Llinás R (1997). Some organizing principles for the control of movement based on olivocerebellar physiology. Prog Brain Res 114, 449-461.
76. Widdowson PS, Griffiths EC & Slater P (1986). The effects of opioids in the periaqueductal grey region of rat brain on hind-limb muscle tone. Neuropeptides 7, 251-258.
77. Wilson WC & Magoun HW (1945). The functional significance of the inferior olive in the cat. J Comp Neurol 83, 69-77.
78. Yeo CH & Hesslow G (1998). Cerebellum and conditioned reflexes. Trends Cogn Sci 2, 322-330.