Avoidance Behavior: A Free‐Operant Lever‐Press Avoidance Task for the Assessment of the Effects of Safety Signals

Anushka B.P. Fernando1, Adam C. Mar1, Gonzalo P. Urcelay1, Anthony Dickinson1, Trevor W. Robbins1

1 Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge
Publication Name:  Current Protocols in Neuroscience
Unit Number:  Unit 8.32
DOI:  10.1002/0471142301.ns0832s70
Online Posting Date:  January, 2015
GO TO THE FULL TEXT: PDF or HTML at Wiley Online Library


This protocol details a free‐operant avoidance paradigm that has been developed to evaluate the relative contribution of different sources of reinforcement of avoidance behavior that may play an important role in the development and maintenance of human anxiety disorders. The task enables the assessment of the effects of safety cues that signal a period free from danger on lever‐press avoidance behavior. Avoidance behavior trained using this protocol has been shown to be sensitive to both behavioral and pharmacological manipulations and has been optimized so that it takes approximately 1 month for rats to perform at high levels of stable avoidance responding. © 2015 by John Wiley & Sons, Inc.

Keywords: avoidance; rodents; habits; revaluation

PDF or HTML at Wiley Online Library

Table of Contents

  • Commentary
  • Literature Cited
  • Figures
  • Tables
PDF or HTML at Wiley Online Library


Basic Protocol 1:

  • Rats (see Strategic Planning)
  • 70% ethanol (dissolved in distilled water; for cleaning and keeping the shock grids free from moisture)
  • Animal housing (see Strategic Planning)
  • Rat lever‐press operant chambers (Coulborn Instruments, Med Associates, or other commercial suppliers; or custom made lever‐press operant boxes)
  • Sound attenuating, fan ventilated cubicles (large enough to enclose each operant chamber)
  • Dedicated computer software (see Equipment Setup in Strategic Planning)
  • Hardware to interface the operant boxes (interfacing hardware is generally available from suppliers of the operant boxes)
  • Uninterruptible power supply (UPS)
  • Data handling software (e.g., Microsoft Access)
  • Data analysis software (e.g., SPSS)
  • Medical gloves (e.g., nitrile gloves)
  • Appropriate personal protection equipment (e.g., scrubs and FFP2D‐type mask)
  • Camera above chamber, connected to closed circuit monitor and digital video recording device (to monitor and record animals’ behavior; optional but recommended)
  • Controlling devices (see Equipment Setup in Strategic Planning)
  • Shelf to support rat chamber (for some tasks, see Equipment Setup in Strategic Planning)
  • Auditory stimuli (e.g., white noise or tone generators; with adjustable intensity and frequency)
  • Shock generators that produce scrambled shock delivered for up to 2 sec (see Equipment Setup in Strategic Planning)
PDF or HTML at Wiley Online Library



Literature Cited

Literature Cited
  Baum, M. 1970. Extinction of avoidance responding through response prevention (flooding). Psychol. Bull. 74:276‐284.
  Baum, M. and Poser, E.G. 1971. Comparison of flooding procedures in animals and man. Behav. Res. Ther. 9:249‐254.
  Beck, K.D., Jiao, X., Cominski, T.P., and Servatius, R.J. 2008. Estrus cycle stage modifies the presentation of stress‐induced startle suppression in female Sprague‐Dawley rats. Physiol. Behav. 93:1019‐1023.
  Beck, K.D., Jiao, X., Ricart, T.M., Myers, C.E., Minor, T.R., Pang, K.C., and Servatius, R.J. 2011. Vulnerability factors in anxiety: Strain and sex differences in the use of signals associated with non‐threat during the acquisition and extinction of active‐avoidance behavior. Progr. Neuropsychopharm. Biol. Psych. 35:1659‐1670.
  Cardinal, R.N. and Aitken, M.R.F. 2010. Whisker: A client‐server high‐performance multimedia research control system. Behav. Res. Methods 42:1059‐1071.
  Carter, M.M., Hollon, S.D., Carson, R., and Shelton, R.C. 1995. Effects of a safe person on induced distress following a biological challenge in panic disorder with agoraphobia. J. Abnorm. Psychol. 104:156‐163.
  Choi, J.S., Cain, C.K., and LeDoux, J.E. 2010. The role of amygdala nuclei in the expression of auditory signaled two‐way active avoidance in rats. Learn. Memory 17:139‐147.
  Dickinson, A. and Dearing, M.F. 1979. Appetitive‐aversive interactions and inhibitory processes. In Mechanisms of Learning and Motivation. (A. Dickinson and R.A. Boakes, eds.) pp. 203‐231. Lawrence Erlbaum Associates, Inc., Hillsdale, N.J.
  Dinsmoor, J.A. 2001. Stimuli inevitably generated by behavior that avoids electric shock are inherently reinforcing. J. Exp. Anal. Behav. 75:311‐333.
  Dinsmoor, J.A. and Sears, G.W. 1973. Control of avoidance by a response‐produced stimulus. Learn. Motiv. 4:284‐293.
  Fernando, A.B.P., Urcelay, G.P., Mar, A.C., Dickinson, A., and Robbins, T.W. 2014a. Safety signals as instrumental reinforcers during free‐operant avoidance. Learn. Mem. 21:488‐497.
  Fernando, A., Urcelay, G., Mar, A., Dickinson, A., and Robbins, T.W. 2014b. Free‐operant avoidance behavior by rats after reinforcer revaluation using opioid agonists and D‐amphetamine. J. Neurosci. 34:6286‐6293.
  Fernando, A.B.P., Urcelay, G.P., Mar, A.C., Dickinson, A., and Robbins, T.W. 2014c. The role of the nucleus accumbens shell in the mediation of the reinforcing properties of a safety signal in free‐operant avoidance: Dopamine‐dependent inhibitory effects of D‐amphetamine. Neuropsychopharmacology 39:1420‐1430.
  Franklin, M.E. and Foa, E.B. 2011. Treatment of obsessive compulsive disorder. Annu. Rev. Clin. Psychol. 7:229‐243.
  Frost, R.O., Hartl, T.L., Christian, R., and Williams, N. 1995. The value of possessions in compulsive hoarding: Patterns of use and attachment. Behav. Res. Ther. 33:897‐902.
  Gillan, C.M., Morein‐Zamir, S., Urcelay, G.P., Sule, A., Voon, V., Apergis‐Schoute, A., Fineberg, N.A., Sahakian, B.J., and Robbins, T.W. 2014. Enhanced avoidance habits in obsessive‐compulsive disorder. Biol. Psychiatr. 75:631‐638.
  Goldsmith, T.B., Shapira, N.A., and Keck, P.E. Jr. 1999. Rapid remission of OCD with tramadol hydrochloride. Am. J. Psychiatr. 156:660‐661.
  Gray, J.A. 1987. The Psychology of Fear and Stress, 2nd Edition. University of Cambridge, Cambridge, U.K.
  Graybiel, A.M. and Rauch, S.L. 2000. Toward a neurobiology of obsessive‐compulsive disorder. Neuron 28:343‐347.
  Khazaal, Y., Krenz, S., Benmebarek, M., and Zullino, D.F. 2006. Worsening of obsessive‐compulsive symptoms under methadone tapering. Progr. Neuropsychopharmacol. Biol. Psychiatr. 30:1350‐1352.
  Konorski, J. 1948. Conditioned Reflex and Neuron Organisation. Cambridge University Press, Cambridge, U.K.
  Konorski, J. 1967. Integrative Activity of the Brain. University of Chicago Press, Chicago.
  Konorski, J. and Miller, S. 1937. On two types of conditioned reflex. J. Gen. Psychol. 16:264‐272.
  Koran, L.M., Aboujaoude, E., Bullock, K.D., Franz, B., Gamel, N., and Elliott, M. 2005. Double‐blind treatment with oral morphine in treatment‐resistant obsessive‐compulsive disorder. J. Clin. Psychiatr. 66:353‐359.
  Lysle, D.T. and Fowler, H. 1985. Inhibition as a ‘slave’ process: deactivation of conditioned inhibition through extinction of conditioned excitation. J. Exp. Psychol. Animal Behav. Proc. 11:71‐94.
  Mackintosh, N.J. 1983. Conditioning and Associative Learning. Oxford University Press, Oxford.
  McCullough, L.D., Sokolowski, J.D., and Salamone, J.D. 1993. A neurochemical and behavioral investigation of the involvement of nucleus accumbens dopamine in instrumental avoidance. Neuroscience 52:919‐925.
  McKay, D., Taylor, S., and Abramowitz, J.S. 2010. Obsessive‐compulsive disorder. In Cognitive‐Behavioral Therapy for Refractory Cases: Turning Failure into Success (D. McKay, S. Abramowitz, and S. Taylor, eds.) pp. 89‐109. American Psychological Association, Washington, D.C.
  Morris, R.G.M. 1975. Preconditioning of reinforcing properties to an exteroceptive feedback stimulus. Learn. Motiv. 6:289‐298.
  Rachman, S. 1984. Agoraphobia—a safety‐signal perspective. Behav. Res. Ther. 22:59‐70.
  Sidman, M. 1953. Avoidance conditioning with brief shock and no exteroceptive warning signal. Science 118:157‐158.
  Solomon, R.L., Kamin, L.J., and Wynne, L.C. 1953. Traumatic avoidance learning: The outcomes of several extinction procedures with dogs. J. Abnorm. Psychol. 48:291‐302.
  Weisman, R.G. and Litner, J.S. 1969. Positive conditioned reinforcement of Sidman avoidance behavior in rats. J. Comp. Physiol. Psychol. 68:597‐603.
  Woody, S. and Rachman, S. 1994. Generalized anxiety disorder (GAD) as an unsuccessful search for safety. Clin. Psychol. Rev. 14:743‐753.
PDF or HTML at Wiley Online Library