Longterm-habituation of the startle response in mice is stimulus modality, but not context specific

Frontiers in Integrative Neuroscience

Volumn 7, Issue JAN, 2014, Pages

  Pliz, Peter K D ^a   Arnold, Stephan W ^a   Rischawy, Anja T ^a   Plappert, Claudia F ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Acoustic startle; Auditory pathways; Context; Generalization; Long term habituation; Specificity; Tactile startle

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; CONTROLLED STUDY; FEMALE; HABITUATION; LONG TERM HABITUATION; MALE; MOUSE; NONHUMAN; SENSORY STIMULATION; SHORT TERM HABITUATION; STARTLE REFLEX; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; TACTILE STIMULATION;

EID: 84892583558     PISSN: 16625145     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnint.2013.00103     Document Type: Article

References (51)

1. Azzopardi, E., Typlt, M., Jenkins, B., and Schmid, S. (2013). Sensorimotor gating and spatial learning in α7-nicotinic receptor knockout mice. Genes Brain Behav. 12, 414-423. doi: 10.1111/gbb.12038
2. Borszcz, G. S., Cranney, J., and Leaton, R. N. (1989). Influence of long-term sensitization on long-term habituation of the acoustic startle response in rats: central gray lesions, preexposure, and extinction. J. Exp. Psychol. Anim. Behav. Process.15, 54-64. doi: 10.1037/0097-7403.15.1.54
3. Caeser, M., Ostwald, J., and Pilz, P. K. (1989). Startle responses measured in muscles innervated by facial and trigeminal nerves show common modulation. Behav. Neurosci. 103, 1075-1081. doi: 10.1037/0735-7044.103.5.1075
4. Cressant, A., Besson, M., Suarez, S., Cormier, A., and Granon, S. (2007). Spatial learning in Long-Evans Hooded rats and C57BL/6J mice: different strategies for different performance. Behav. Brain Res. 177, 22-29. doi: 10.1016/j.bbr.2006.11.010
5. Davis, M., Gendelman, D. S., Tischler, M. D., and Gendelman, P. M. (1982). A primary acoustic startle circuit: lesion and stimulation studies. J. Neurosci. 2, 791-805.
6. Ehret, G. (1974). Age-dependent hearing loss in normal hearing mice. Naturwissenschaften 61, 506-507. doi: 10.1007/BF00622976
7. Ehret, G. (1983). "Psychoacoustics," in The Auditory Psychobiology of the Mouse, ed J. F. Willott (Thomas, IL: Springfield), 13-56.
8. Frick, K. M., Stillner, E. T., and Berger-Sweeney, J. (2000). Mice are not little rats: species differences in a one-day water maze task. Neuroreport. 11, 3461-3465. doi: 10.1097/00001756-200011090-00013
9. Frings, M., Awad, N., Jentzen, W., Dimitrova, A., Kolb, F. P., Diener, H. C., et al. (2006). Involvement of the human cerebellum in short-term and longterm habituation of the acoustic startle response: a serial PET study. Clin. Neurophysiol. 117, 1290-1300. doi: 10.1016/j.clinph.2006.02.025
10. Groves, P. M., Wilson, C. J., and Boyle, R. D. (1974). Brain stem pathways, cortical modulation, and habituation of the acoustic startle response. Behav. Biol. 10, 391-418. doi: 10.1016/S0091-6773(74)91975-0
11. Jordan, W. P. (1989). Mesencephalic reticular formation lesions made after habituation training abolish long-term habituation of the acoustic startle response in rats. Behav. Neurosci. 103, 805-815. doi: 10.1037/0735-7044.103.4.805
12. Jordan, W. P., and Leaton, R. N. (1982). Effects of mesencephalic reticular formation lesions on habituation of startle and lick suppression responses in the rat. J. Comp. Physiol. Psychol. 96, 170-183. doi: 10.1037/h0077880
13. Jordan, W. P., and Leaton, R. N. (1983). Habituation of the acoustic startle response in rats after lesions in the mesencephalic reticular formation or in the inferior colliculus. Behav. Neurosci. 97, 710-724. doi: 10.1037/0735-7044.97.5.710
14. Jordan, W. P., Nelson, C. J., and Bodie, T. B. (1993). Long-term habituation of the EMG startle response following lesions to the mesencephalic reticular formation in rats. Soc. Neurosci. Abstr. 19, 1230.
15. Jordan, W. P., and Poore, L. H. (1998). Longand short-term habituation of acoustic startle is not frequency specific in the rat. Physiol. Behav. 63, 643-649. doi: 10.1016/S0031-9384(97)00512-X
16. Jordan, W. P., Strasser, H. C., and McHale, L. (2000). Contextual control of longterm habituation in rats. J. Exp. Psychol. Anim. Behav. Process. 26, 323-339. doi: 10.1037/0097-7403.26.3.323
17. Koch, M. (1999). The neurobiology of startle. Prog. Neurobiol. 59, 107-128. doi: 10.1016/S0301-0082(98)00098-7
18. Koch, M., Lingenhöhl, K., and Pilz, P. K. (1992). Loss of the acoustic startle response following neurotoxic lesions of the caudal pontine reticular formation: possible role of giant neurons. Neuroscience 49, 617-625. doi: 10.1016/0306-4522(92)90231-P
19. Lall, G. S., Revell, V. L., Momiji, H., Al Enezi, J., Altimus, C. M., Güler, A. D., et al. (2010). Distinct contributions of rod, cone, and melanopsin photoreceptors to encoding irradiance. Neuron 66, 417-428. doi: 10.1016/j.neuron.2010.04.037
20. Leaton, R. N. (1976). Long-term retention of the habituation of lick suppression and startle response produced by a single auditory stimulus. J. Exp. Psychol. Anim. Behav. Process. 2, 248-259. doi: 10.1037/0097-7403.2.3.248
21. Leaton, R. N., Cassella, J. V., and Borszcz, G. S. (1985). Short-term and long-term habituation of the acoustic startle response in chronic decerebrate rats. Behav. Neurosci. 99, 901-912. doi: 10.1037/0735-7044.99.5.901
22. Leaton, R., and Supple, W. (1986). Cerebellar vermis: essential for long-term habituation of the acoustic startle response. Science 232, 513-515. doi: 10.1126/science.3961494
23. Leaton, R. N., and Supple, W. F. Jr. (1991). Medial cerebellum and long-term habituation of acoustic startle in rats. Behav. Neurosci. 105, 804-816. doi: 10.1037/0735-7044.105.6.804
24. Lee, Y., López, D. E., Meloni, E. G., and Davis, M. (1996). A primary acoustic startle pathway: obligatory role of cochlear root neurons and the nucleus reticularis pontis caudalis. J. Neurosci. 16, 3775-3789.
25. Li, L., Steidl, S., and Yeomans, J. S. (2001). Contributions of the vestibular nucleus and vestibulospinal tract to the startle reflex. Neuroscience 106, 811-821. doi: 10.1016/S0306-4522(01)00324-4
26. Li, L., and Yeomans, J. S. (1999). Summation between acoustic and trigeminal stimuli evoking startle. Neuroscience 90, 139-152. doi: 10.1016/S0306-4522(98)00436-9
27. Lingenhöhl, K., and Friauf, E. (1992). Giant neurons in the caudal pontine reticular formation receive short latency acoustic input: an intracellular recording and HRP-study in the rat. J. Comp. Neurol. 325, 473-492. doi: 10.1002/cne.903250403
28. Lingenhöhl, K., and Friauf, E. (1994). Giant neurons in the rat reticular formation: a sensorimotor interface in the elementary acoustic startle circuit? J. Neurosci. 14, 1176-1194.
29. Lopiano, L., de'Sperati, C., and Montarolo, P. G. (1990). Long-term habituation of the acoustic startle response: role of the cerebellar vermis. Neuroscience 35, 79-84. doi: 10.1016/0306-4522(90)90122-K
30. Marlin, N. A., and Miller, R. R. (1981). Associations to contextual stimuli as a determinant of long-term habituation. J. Exp. Psychol. Anim. Behav. Process. 7, 313-333. doi: 10.1037/0097-7403.7.4.313
31. Maschke, M., Drepper, J., Kindsvater, K., Kolb, F. P., Diener, H. C., and Timmann, D. (2000). Involvement of the human medial cerebellum in long-term habituation of the acoustic startle response. Exp Brain Res. 133, 359-367. doi: 10.1007/s002210000417
32. Meloni, E. G., and Davis, M. (1998). The dorsal cochlear nucleus contributes to a high intensity component of the acoustic startle reflex in rats. Hear. Res. 119, 69-80. doi: 10.1016/S0378-5955(98)00040-9
33. Pilz, P. K., Carl, T. D., and Plappert, C. F. (2004). Habituation of the acoustic and the tactile startle responses in mice: two independent sensory processes. Behav. Neurosci. 118, 975-983. doi: 10.1037/0735-7044.118.5.975
34. Pilz, P. K. D., and Leaton, R. N. (1999). Short-term and long-term habituation of the acoustic startle response as a function of stimulus rise time in rats. Psychobiology 27, 402-414.
35. Pissiota, A., Frans, O., Fredrikson, M., Långström, B., and Flaten, M. A. (2002). The human startle reflex and pons activation: a regional cerebral blood flow study. Eur. J. Neurosci. 15, 395-398. doi: 10.1046/j.0953-816x.2001.01870.x
36. Plappert, C. F., Kuhn, S., Schnitzler, H. U., and Pilz, P. K. (2006). Experience increases the prepulse inhibition of the acoustic startle response in mice. Behav. Neurosci. 120, 16-23. doi: 10.1037/0735-7044.120.1.16
37. Plappert, C. F., and Pilz, P. K. (2005). Long-term habituation of the startle response in mice evoked by acoustic and tactile stimuli. Behav. Brain Res. 162, 307-310. doi: 10.1016/j.bbr.2005.03.022
38. Plappert, C. F., and Pilz, P. K. (2013). "Startle behavior and prepulse inhibition," in Behavioral Genetics of the Mouse, Vol. 1, eds W. E. Cursio, F. Sluyter, R. T. Gerlai, and S. Pietropaolo (Cambridge University Press), 171-178. doi: 10.1017/CBO9781139541022.019
39. Ponce, F. P., Quintana, G. R., Philominraj, A. S., and Vogel, E. H. (2011). Habituation of the eyeblink response in humans with stimuli presented in a sequence of incremental intensity. Biol. Res. 44, 295-299. doi: 10.4067/S0716-97602011000300011
40. Poore, L. H., and Jordan, W. P. (1992). Modulation of the acoustic startle response: EMG activity in the spinotrapezius muscle of the rat. Soc. Neursci. Abstr. 18, 1065.
41. Rankin, C. H., Abrams, T., Barry, R. J., Bhatnagar, S., Clayton, D. F., Colombo, J., et al. (2009). Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiol. Learn. Mem. 92, 135-138. doi: 10.1016/j.nlm.2008.09.012
42. Schmid, S., Azzopardi, E., De Jaeger, X., Prado, M. A., and Prado, V. F. (2011). VAChT knock-down mice show normal prepulse inhibition but disrupted long-term habituation. Genes Brain Behav. 10, 457-464. doi: 10.1111/j.1601-183X.2011.00686.x
43. Scott, B. W., Frankland, P. W., Li, L., and Yeomans, J. S. (1999). Cochlear and trigeminal systems contributing to the startle reflex in rats. Neuroscience 91, 1565-1574. doi: 10.1016/S0306-4522(98)00708-8
44. Simons-Weidenmaier, N., Weber, M., Plappert, C., Pilz, P. K., and Schmid, S. (2006). Synaptic depression and short-term habituation are located in the sensory part of the mammalian startle pathway. BMC Neurosci. 7:38. doi: 10.1186/1471-2202-7-38
45. Snyder, J. S., Choe, J. S., Clifford, M. A., Jeurling, S. I., Hurley, P., Brown, A., et al. (2009). Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J. Neurosci. 29, 14484-14495. doi: 10.1523/JNEUROSCI.1768-09.2009
46. Stranahan, A. M. (2011). Similarities and differences in spatial learning and object recognition between young male C57Bl/6J mice and Sprague-Dawley rats. Behav. Neurosci. 125, 791-795. doi: 10.1037/a0025133
47. Thompson, R. F., and Spencer, W. A. (1966). Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol. Rev. 73, 16-43. doi: 10.1037/h0022681
48. Timmann, D., Musso, C., Kolb, F. P., Rijntjes, M., Jüptner, M., Müller, S. P., et al. (1998). Involvement of the human cerebellum during habituation of the acoustic startle response: a PET study. J. Neurol. Neurosurg. Psychiatry 65, 771-773. doi: 10.1136/jnnp.65.5.771
49. Typlt, M., Mirkowski, M., Azzopardi, E., Ruth, P., Pilz, P. K. D., and Schmid, S. (2013). Habituation of reflexive and motivated behaviour in mice with a deficiency of the α-subunit of the BK channel. Front. Integr. Neurosci. 7:79. doi: 10.3389/fnint.2013.00079
50. Vogel, E. H., and Wagner, A. R. (2005). Stimulus specificity in the habituation of the startle response in the rat. Physiol. Behav. 86, 516-525. doi: 10.1016/j.physbeh.2005.08.042
51. Yeomans, J. S., and Frankland, P. W. (1996). The acoustic startle reflex: neurons and connections. Brain Res. Rev. 21, 301-314. doi: 10.1016/0165-0173.(96)00004-5