Context Dependent Auditory Thresholds Determined by Brainstem Audiometry and Prepulse Inhibition in Mongolian Gerbils

Markus Walter, Konstantin Tziridis, Sonke Ahlf, Holger Schulze

Experimental Otolaryngology, University of Erlangen-Nuremberg, Erlangen, Germany.

DOI: 10.4236/oja.2012.21004                

Abstract

Information on hearing thresholds is not always reliable as differences in these thresholds have been described even for the same species. This may partially be due to different methods used by different labs. A frequently used approach to obtain an estimate of hearing threshold is the electrophysiological recording of auditory brainstem responses (ABR). They are usually recorded under deep anesthesia and represent the auditory evoked far-field potentials at various levels in the central auditory pathway. Alternatively, several behavioral approaches are employed. These commonly use operant or classical conditioning to determine hearing thresholds. A potential disadvantage of these methods is that any sound conditioning may in principle alter auditory perception and therefore auditory thresholds. To exclude this type of methodological bias a prepulse inhibition (PPI) paradigm can be used where an audiogram can be determined without any kind of pre-training. Here we compare the threshold estimates obtained by two different ABR and PPI measurements where stimuli are presented in different contexts, either randomly or non-randomly, to test for a possible effect of auditory sensitization. In addition we test the effect of a frequency specific acoustic trauma on the audiograms obtained with both methods. In general we find behaviorally determined audiograms to be significantly lower in absolute thresh- old compared to ABR measurements. Furthermore non-randomized presentation context of the stimuli generally results in audiograms with 10 to 15 dB lower thresholds than pseudo-randomized presentation. Finally, the amount of threshold loss induced by acoustic trauma is similar for all methods tested.

Keywords

Acoustic Trauma; Hearing Thresholds; Auditory Processing; Startle Response

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	H. Markl and G. Ehret, “Auditory Threshold of the Mouse (Mus musculus). A Critical Evaluation of Methods for Measuring Auditory Threshold in a Mammal,” Zeitschrift für Tierpsychologie, Vol. 33, No. 3-4, 1973, pp. 274-286. doi:j.1439-0310.1973.tb02096.x
[2]	M. A. Ramsier and N. J. Dominy, “A Comparison of Auditory Brainstem Responses and Behavioral Estimates of Hearing Sensitivity in Lemur catta and Nycticebus coucang,” American Journal of Primatology, Vol. 72, No. 3, 2010, pp. 217-233. doi:ajp.20780
[3]	H. E. Heffner, G. Koay and R. S. Heffner, “Comparison of Behavioral and Auditory Brainstem Response Measures of Threshold Shift in Rats Exposed to Loud Sound,” Journal of the Acoustical Society of America, Vol. 124, No. 2, 2008, pp. 1093-1104. doi:10.1121/1.2949518
[4]	K. R. Henry, “Differential Changes of Auditory Nerve and Brain Stem Short Latency Evoked Potentials in the Laboratory Mouse,” Electroencephalography and Clinical Neurophysiology, Vol. 46, No. 4, 1979, pp. 452-459. doi:0013-4694(79)90146-9
[5]	S. L. McFadden, E. J. Walsh and J. McGee, “Onset and Development of Auditory Brainstem Responses in the Mongolian Gerbil (Meriones unguiculatus),” Hearing Research, Vol. 100, No. 1-2, 1996, pp. 68-79. doi:0378-5955(96)00108-6
[6]	R. E. Lasky, M. M. Maier, E. B. Snodgrass, N. K. Laughlin and K. E. Hecox, “Auditory Evoked Brainstem and Middle Latency Responses in Macaca mulatta and Humans,” Hearing Research, Vol. 89, No. 1-2, 1995, pp. 212- 225. doi:0378-5955(95)00140-7
[7]	A. C. Coats and J. L. Martin, “Human Auditory Nerve Action Potentials and Brain Stem Evoked Responses: Effects of Audiogram Shape and Lesion Location,” Archives of Otolaryngology, Vol. 103, No. 10, 1977, pp. 605- 622.
[8]	H. Davis, S. K. Hirsh, L. L. Turpin and M. E. Peacock, “Threshold Sensitivity and Frequency Specificity in Auditory Brainstem Response Audiometry,” Audiology, Vol. 24, No. 1, 1985, pp. 54-70.
[9]	B. L. Lonsbury-Martin, F. P. Harris, B. B. Stagner, M. D. Hawkins and G. K. Martin, “Distortion Product Emissions in Humans. I. Basic Properties in Normally Hearing Subjects,” The Annals of Otology, Rhinology & Laryngology: Supplement, Vol. 147, 1990, pp. 3-14.
[10]	S. H. Sha, et al., “Age-Related Auditory Pathology in the CBA/J Mouse,” Hearing Research, Vol. 243, No. 1-2, 2008, pp. 87-94. doi:j.heares.2008.06.001
[11]	H. Winter, et al., “Deafness in TRbeta Mutants Is Caused by Malformation of the Tectorial Membrane,” Journal of Neuroscience, Vol. 29, No. 8, 2009, pp. 2581-2587. doi:JNEUROSCI.3557-08.2009
[12]	X. Zhou, P. H. Jen, K. L. Seburn, W. N. Frankel and Q. Y. Zheng, “Auditory Brainstem Responses in 10 Inbred Strains of Mice,” Brain Research, Vol. 1091, No. 1, 2006, pp. 16-26.
[13]	J. W. Hall and D. W. Swanepoel, “Objective Assessment of Hearing,” Plural Publishing, Inc., San Diego, 2010.
[14]	K. R. Henry, “Auditory Brainstem Volume-Conducted Responses: Origins in the Laboratory Mouse,” Journal of the American Auditory Society, Vol. 4, No. 5, 1979, pp. 173-178.
[15]	B. L. Lonsbury-Martin, G. K. Martin and M. T. Hannley, “Physiology of the Auditory and Vestibular System,” In: J. B. Snow and P. A. Wackym, Eds., Ballenger’s Otorhinolaryngology: Head and Neck Surgery, 2009.
[16]	H. Heffner and B. Masterton, “Hearing in Primitive Primates: Slow Loris (Nycticebus coucang) and Potto (Pero- dicticus potto),” Journal of Comparative and Physiologi- cal Psychology, Vol. 71, No. 2, 1970, pp. 175-182. doi:h0029138
[17]	R. S. Heffner and H. E. Heffner, “Behavioral Hearing Range of the Chinchilla,” Hearing Research, Vol. 52, No. 1, 1991, pp. 13-16. doi:0378-5955(91)90183-A
[18]	L. L. Jackson, R. S. Heffner and H. E. Heffner, “Free-Field Audiogram of the Japanese Macaque (Macaca fuscata),” Journal of the Acoustical Society of America, Vol. 106, No. 5, 1999, pp. 3017-3023. doi:1.428121
[19]	R. E. Lasky, A. A. Soto, M. L. Luck and N. K. Laughlin, “Otoacoustic Emission, Evoked Potential, and Behavioral Auditory Thresholds in the Rhesus Monkey (Macaca mulatta),” Hearing Research, Vol. 136, No. 1-2, 1999, pp. 35-43. doi:S0378-5955(99)00100-8
[20]	A. Ryan, “Hearing Sensitivity of the Mongolian Gerbil, Meriones unguiculatis,” Journal of the Acoustical Society of America, Vol. 59, No. 5, 1976, pp. 1222-1226. doi:1.380961
[21]	M. D. Szymanski, et al., “Killer Whale (Orcinus orca) Hearing: Auditory Brainstem Response and Behavioral Audiograms,” Journal of the Acoustical Society of America, Vol. 106, No. 2, 1999, pp. 1134-1141. doi:1.427121
[22]	M. M. Yuen, P. E. Nachtigall, M. Breese and A. Y. Supin, “Behavioral and Auditory Evoked Potential Audiograms of a False Killer Whale (Pseudorca crassidens),” Journal of the Acoustical Society of America, Vol. 118, No. 4, 2005, pp. 2688-2695. doi:1.2010350
[23]	E. Borg and B. Engstrom, “Hearing Thresholds in the Rabbit. A Behavioral and Electrophysiological Study,” Acta Otolaryngologica, Vol. 95, No. 1-2, 1983, pp. 19-26.
[24]	J. R. Ison, P. Agrawal, J. Pak and W. J. Vaughn, “Changes in Temporal Acuity with Age and with Hearing Impairment in the Mouse: A Study of the Acoustic Startle Reflex and Its Inhibition by Brief Decrements in Noise Level,” Journal of the Acoustical Society of America, Vol. 104, No. 3, 1998, pp. 1696-1704. doi:1.424382
[25]	G. Yang, et al., “Salicylate Induced Tinnitus: Behavioral Measures and Neural Activity in Auditory Cortex of Awake Rats,” Hearing Research, Vol. 226, No. 1-2, 2007, pp. 244-253. doi:j.heares.2006.06.013
[26]	M. Brown, D. R. Irvine and V. N. Park, “Perceptual Learning on an Auditory Frequency Discrimination Task by Cats: Association with Changes in Primary Auditory Cortex,” Cerebral Cortex, Vol. 14, No. 9, 2004, pp. 952-965. doi:bhh056
[27]	F. W. Ohl and H. Scheich, “Learning-Induced Plasticity in Animal and Human Auditory Cortex,” Current Opinion in Neurobiology, Vol. 15, No. 4, 2005, pp. 470-477. doi:j.conb.2005.07.002
[28]	N. M. Weinberger, “Auditory Associative Memory and Representational Plasticity in the Primary Auditory Cortex,” Hearing Research, Vol. 229, No. 1-2, 2007, pp. 54- 68. doi:j.heares.2007.01.004
[29]	M. Koch, “The Neurobiology of Startle,” Progress in Neurobiology, Vol. 59, No. 2, 1999, pp. 107-128. doi:S0301-0082(98)00098-7
[30]	J. Larrauri and N. Schmajuk, “Prepulse Inhibition Mechanisms and Cognitive Processes: A Review and Model,” Neurotransmitter Interactions and Cognitive Function, EXS, Vol. 98, 2006, pp. 245-278. doi:978-3-7643-7772-4_12
[31]	K. M. Crofton and X. Zhao, “Mid-Frequency Hearing Loss in Rats Following Inhalation Exposure to Trichloroethylene: Evidence from Reflex Modification Audiometry,” Neurotoxicology and Teratology, Vol. 15, No. 6, 1993, pp. 413-423. doi:0892-0362(93)90059-W
[32]	L. D. Fechter, L. Sheppard, J. S. Young and S. Zeger, “Sensory Threshold Estimation from a Continuously Graded Response Produced by Reflex Modification Audiometry,” Journal of the Acoustical Society of America, Vol. 84, No. 1, 1988, pp. 179-185. doi:1.396962
[33]	J. S. Young and L. D. Fechter, “Reflex Inhibition Procedures for Animal Audiometry: A Technique for Assessing Ototoxicity,” Journal of the Acoustical Society of America, Vol. 73, No. 5, 1983, pp. 1686-1693. doi:1.389391
[34]	N. Ulanovsky, L. Las, D. Farkas and I. Nelken, “Multiple Time Scales of Adaptation in Auditory Cortex Neurons,” The Journal of Neuroscience, Vol. 24, No. 46, 2004, pp. 10440-10453. doi:JNEUROSCI.1905-04.2004
[35]	I. Dean, N. S. Harper and D. McAlpine, “Neural Population Coding of Sound Level Adapts to Stimulus Statistics,” Nature Neuroscience, Vol. 8, No. 12, 2005, pp. 1684-1689.
[36]	I. Dean, B. L. Robinson, N. S. Harper and D. McAlpine, “Rapid Neural Adaptation to Sound Level Statistics,” Journal of Neuroscience, Vol. 28, No. 25, 2008, pp. 6430- 6438. doi:JNEUROSCI.0470-08.2008
[37]	G. S. Donaldson and E. W. Rubel, “Effects of Stimulus Repetition Rate on ABR Threshold, Amplitude and Latency in Neonatal and Adult Mongolian Gerbils,” Electroencephalography and Clinical Neurophysiology, Vol. 77, No. 6, 1990, pp. 458-470. doi:0168-5597(90)90006-Y
[38]	S. Carlson and J. F. Willott, “The Behavioral Salience of Tones as Indicated by Prepulse Inhibition of the Startle Response: Relationship to Hearing Loss and Central Neural Plasticity in C57BL/6J Mice,” Hearing Research, Vol. 99, No. 1-2, 1996, pp. 168-175. doi:S0378-5955(96)00098-6
[39]	J. F. Willott, S. Carlson and H. Chen, “Prepulse Inhibition of the Startle Response in Mice: Relationship to Hearing Loss and Auditory System Plasticity,” Behavioral Neuroscience, Vol. 108, No. 4, 1994, pp. 703-713. doi:0735-7044.108.4.703
[40]	M. Grassi and A. Soranzo, “MLP: A MATLAB Toolbox for Rapid and Reliable Auditory Threshold Estimation,” Behavioral Research Methods, Vol. 41, No. 1, 2009, pp. 20-28. doi:BRM.41.1.20
[41]	F. A. Boettcher, “Susceptibility to Acoustic Trauma in Young and Aged Gerbils,” Journal of the Acoustical Society of America, Vol. 112, No. 6, 2002, pp. 2948-2955. doi:1.1513364
[42]	A. F. Ryan, T. M. Bennett, N. K. Woolf and A. Axelsson, “Protection from Noise-Induced Hearing Loss by Prior Exposure to a Nontraumatic Stimulus: Role of the Middle Ear Muscles,” Hearing Research, Vol. 72, No. 1-2, 1994, pp. 23-28. doi:0378-5955(94)90201-1
[43]	K. R. Henry, “Cochlear Damage Resulting from Exposure to Four Different Octave Bands of Noise at Three Ages,” Behavioral Neuroscience, Vol. 98, No. 1, 1984, pp. 107- 117. doi:0735-7044.98.1.107
[44]	J. F. Willott and K. R. Henry, “Auditory Evoked Potentials: Developmental Changes of Threshold and Amplitude Following Early Acoustic Trauma,” Journal of Comparative and Physiological Psychology, Vol. 86, No. 1, 1974, pp. 1- 7. doi:h0035922
[45]	R. P. Hamernik, W. A. Ahroon and J. A. Patterson Jr., “Threshold Recovery Functions Following Impulse Noise Trauma,” Journal of the Acoustical Society of America, Vol. 84, No. 3, 1988, pp. 941-950. doi:1.396663
[46]	D. Yamashita, S. B. Minami, S. Kanzaki, K. Ogawa and J. M. Miller, “Bcl-2 Genes Regulate Noise-Induced Hearing Loss,” Journal of Neuroscience Research, Vol. 86, No. 4, 2008, pp. 920-928. doi:jnr.21533
[47]	S. Kurt, C. K. Moeller, M. Jeschke and H. Schulze, “Differential Effects of Iontophoretic Application of the GABAA-Antagonists Bicuculline and Gabazine on Tone- Evoked Local Field Potentials in Primary Auditory Cortex: Interaction with Ketamine Anesthesia,” Brain Re- search, Vol. 1220, 2008, pp. 58-69. doi:j.brainres.2007.10.023
[48]	R. P. Bobbin, J. G. May and R. L. Lemoine, “Effects of Pentobarbital and Ketamine on Brain Stem Auditory Potentials. Latency and Amplitude Intensity Functions after Intraperitoneal Administration,” Archives of Otolaryngology, Vol. 105, No. 8, 1979, pp. 467-470.
[49]	F. Dodd and R. R. Capranica, “A Comparison of Anesthetic Agents and Their Effects on the Response Properties of the Peripheral Auditory System,” Hearing Research, Vol. 62, No. 2, 1992, pp. 173-180. doi:0378-5955(92)90183-N
[50]	S. Kurt, M. Groszer, S. E. Fisher and G. Ehret, “Modified Sound-Evoked Brainstem Potentials in Foxp2 Mutant Mice,” Brain Research, Vol. 1289, 2009, pp. 30-36. doi:j.brainres.2009.06.092
[51]	M. P. Gorga, D. W. Worthington, J. K. Reiland, K. A. Beauchaine and D. E. Goldgar, “Some Comparisons between Auditory Brain Stem Response Thresholds, Latencies, and the Pure-Tone Audiogram,” Ear and Hearing, Vol. 6, No. 2, 1985, pp. 105-112.
[52]	T. W. Picton, A. Durieux-Smith and L. M. Moran, “Recording Auditory Brainstem Responses from Infants,” International Journal of Pediatric Otorhinolaryngology, Vol. 28, No. 2-3, 1994, pp. 93-110. doi:0165-5876(94)90001-9
[53]	F. A. Boettcher, J. H. Mills, J. R. Dubno and R. A. Schmiedt, “Masking of Auditory Brainstem Responses in Young and Aged Gerbils,” Hearing Research, Vol. 89, No. 1-2, 1995, pp. 1-13. doi:0378-5955(95)00116-X
[54]	N. J. Ingham, S. K. Thornton, S. D. Comis and D. J. Withington, “The Auditory Brainstem Response of Aged Guinea Pigs,” Acta Otolaryngologica, Vol. 118, No. 5, 1998, pp. 673-680.
[55]	T. Fowler, B. Canlon, D. Dolan and J. M. Miller, “The Effect of Noise Trauma Following Training Exposures in the Mouse,” Hearing Research, Vol. 88, No. 1-2, 1995, pp. 1-13. doi:0378-5955(95)00062-9
[56]	J. Popelar, J. Grecova, N. Rybalko and J. Syka, “Comparison of Noise-Induced Changes of Auditory Brainstem and Middle Latency Response Amplitudes in Rats,” Hearing Research, Vol. 245, No. 1-2, 2008, pp. 82-91. doi:j.heares.2008.09.002
[57]	Q. Y. Zheng, K. R. Johnson and L. C. Erway, “Assessment of Hearing in 80 Inbred Strains of Mice by ABR Threshold Analyses,” Hearing Research, Vol. 130, No. 1- 2, 1999, pp. 94-107. doi:S0378-5955(99)00003-9
[58]	L. O. Trussell, “Synaptic Mechanisms for Coding Timing in Auditory Neurons,” Annual Review of Physiology, Vol. 61, 1999, pp. 477-496. doi:annurev.physiol.61.1.477
[59]	R. G. Turcott, et al., “A Nonstationary Poisson Point Process Describes the Sequence of Action Potentials over Long Time Scales in Lateral-Superior-Olive Auditory Neurons,” Biological Cybernetics, Vol. 70, No. 3, 1994, pp. 209-217. doi:BF00197601
[60]	J. R. Melcher and N. Y. Kiang, “Generators of the Brainstem Auditory Evoked Potential in Cat. III: Identified Cell Populations,” Hearing Research, Vol. 93, No. 1-2, 1996, pp. 52-71. doi:0378-5955(95)00200-6
[61]	B. J. Malone, B. H. Scott and M. N. Semple, “Context-Dependent Adaptive Coding of Interaural Phase Disparity in the Auditory Cortex of Awake Macaques,” Journal of Neuroscience, Vol. 22, No. 11, 2002, pp. 4625- 4638.
[62]	J. A. Hobin, K. A. Goosens and S. Maren, “Context-Dependent Neuronal Activity in the Lateral Amygdala Represents Fear Memories after Extinction,” Journal of Neuroscience, Vol. 23, No. 23, 2003, pp. 8410- 8416.
[63]	J. R. Melcher, J. J. Guinan Jr., I. M. Knudson and N. Y. Kiang, “Generators of the Brainstem Auditory Evoked Potential in Cat. II. Correlating Lesion Sites with Waveform Changes,” Hearing Research, Vol. 93, No. 1-2, 1996, pp. 28-51. doi:0378-5955(95)00179-4
[64]	R. E. Lasky, “Rate and Adaptation Effects on the Auditory Evoked Brainstem Response in Human Newborns and Adults,” Hearing Research, Vol. 111, No. 1-2, 1997, pp. 165-176. doi:S0378-5955(97)00106-8
[65]	Q. C. Chen and P. H. Jen, “Pulse Repetition Rate Increases the Minimum Threshold and Latency of Auditory Neurons,” Brain Research, Vol. 654, No. 1, 1994, pp. 155-158. doi:0006-8993(94)91582-2
[66]	L. Ruttiger, et al., “BDNF mRNA Expression and Protein Localization are Changed in Age-Related Hearing Loss,” Neurobiology of Aging, Vol. 28, No. 4, 2007, pp. 586-601. doi:j.neurobiolaging.2006.02.008
[67]	M. D. Szymanski, K. R. Henry and F. O. Buchting, “Albino and Pigmented Gerbil Auditory Function: Influence of Genotype and Gentamicin,” Audiology, Vol. 33, No. 2, 1994, pp. 63-72.
[68]	R. H. Fitch, S. W. Threlkeld, M. M. McClure and A. M. Peiffer, “Use of a Modified Prepulse Inhibition Paradigm to Assess Complex Auditory Discrimination in Rodents,” Brain Research Bulletin, Vol. 76, No. 1-2, 2008, pp. 1-7. doi:j.brainresbull.2007.07.013
[69]	J. T. Friedman, A. M. Peiffer, M. G. Clark, A. A. Benasich and R. H. Fitch, “Age and Experience-Related Improvements in Gap Detection in the Rat,” Developmental Brain Research, Vol. 152, No. 2, 2004, pp. 83-91. doi:j.devbrainres.2004.06.007
[70]	J. R. Ison and E. E. Krauter, “Acoustic Startle Reflexes in the Rat During Consummatory Behavior,” Journal of Comparative and Physiological Psychology, Vol. 89, No. 1, 1975, pp. 39-49. doi:h0076387
[71]	P. K. Pilz and H. U. Schnitzler, “Habituation and Sensitization of the Acoustic Startle Response in Rats: Amplitude, Threshold, and Latency Measures,” Neurobiology of Learning and Memory, Vol. 66, No. 1, 1996, pp. 67-79. doi:nlme.1996.0044
[72]	H. Schulze and H. Scheich, “Discrimination Learning of Amplitude Modulated Tones in Mongolian Gerbils,” Neuroscience Letters, Vol. 261, No. 1-2, 1999, pp. 13-16. doi:S0304-3940(98)00991-4
[73]	E. A. Blakeslee, K. Hynson, R. P. Hamernik and D. Henderson, “Asymptotic Threshold Shift in Chinchillas Exposed to Impulse Noise,” Journal of the Acoustical Society of America, Vol. 63, No. 3, 1978, pp. 876-882. doi:1.381767
[74]	M. Brosch and C. E. Schreiner, “Time Course of Forward Masking Tuning Curves in Cat Primary Auditory Cortex,” Journal of Neurophysiology, Vol. 77, No. 2, 1997, pp. 923-943.
[75]	M. B. Calford and M. N. Semple, “Monaural Inhibition in Cat Auditory Cortex,” Journal of Neurophysiology, Vol. 73, No. 5, 1995, pp. 1876-1891.
[76]	S. L. Sally and J. B. Kelly, “Organization of Auditory Cortex in the Albino Rat: Sound Frequency,” Journal of Neurophysiology, Vol. 59, No. 5, 1988, pp. 1627-1638.
[77]	G. Ehret, “Psychoacoustics,” In: J. F. Willott, Ed. The Auditory Psychobiology of the Mouse, Charles C. Thomas, Springfield, 1983, pp. 13-56.
[78]	I. Hamann, et al., “Behavioral and Evoked-Potential Thresholds in Young and Old Mongolian Gerbils (Meriones unguiculatus),” Hearing Research, Vol. 171, No. 1-2, 2002, pp. 82-95. doi:S0378-5955(02)00454-9
[79]	O. Bar-Yosef, Y. Rotman and I. Nelken, “Responses of Neurons in Cat Primary Auditory Cortex to Bird Chirps: Effects of Temporal and Spectral Context,” Journal of Neuroscience, Vol. 22, No. 19, 2002, pp. 8619-8632.
[80]	N. Schmajuk, “Brain-Behaviour Relationships in Latent Inhibition: A Computational Model,” Neuroscience & Bio- behavioral Reviews, Vol. 29, No. 6, 2005, pp. 1001-1020. doi:j.neubiorev.2005.02.005
[81]	P. K. Pilz, J. Ostwald, A. Kreiter and H. U. Schnitzler, “Effect of the Middle Ear Reflex on Sound Transmission to the Inner Ear of Rat,” Hearing Research, Vol. 105, No. 1-2, 1997, pp. 171-182. doi:S0378-5955(96)00206-7
[82]	L. G. Reijmers and B. W. Peeters, “Effects of Acoustic Prepulses on the Startle Reflex in Rats: A Parametric Analysis,” Brain Research, Vol. 667, No. 1, 1994, pp. 144-150. doi:0006-8993(94)91727-2
[83]	G. S. Borszcz, J. Cranney and R. N. Leaton, “Influence of Long-Term Sensitization on Long-Term Habituation of the Acoustic Startle Response in Rats: Central Gray Lesions, Preexposure, and Extinction,” Journal of Experimental Psychology: Animal Behavior Processes, Vol. 15, No. 1, 1989, pp. 54-64.
[84]	C. C. Chabot and D. H. Taylor, “Circadian Modulation of the Rat Acoustic Startle Response,” Behavioral Neuroscience, Vol. 106, No. 5, 1992, pp. 846-852. doi:0735-7044.106.5.846
[85]	B. H. Gaese, M. Nowotny and P. K. Pilz, “Acoustic Startle and Prepulse Inhibition in the Mongolian Gerbil,” Physiology & Behavior, Vol. 98, No. 4, 2009, pp. 460- 466. doi:j.physbeh.2009.07.014