A self-initiated cue-reward learning procedure for neural recording in rodents

Background Single-unit recording in Pavlovian conditioning tasks requires the use of within-subject designs as well as sampling a considerable number of trials per trial type and session, which increases the total trial count. Pavlovian conditioning, on the other hand, requires a long average intertrial interval (ITI) relative to cue duration for cue-specific learning to occur. These requirements combined can make the session duration unfeasibly long. New Method To circumvent this issue, we developed a self-initiated variant of the Pavlovian magazine-approach procedure in rodents. Unlike the standard procedure, where the animals passively receive the trials, the self-initiated procedure grants animals agency to self-administer and self-pace trials from a predetermined, pseudorandomized list. Critically, whereas in the standard procedure the typical ITI is in the order of minutes, our procedure uses a much shorter ITI (10 s). Results Despite such a short ITI, discrimination learning in the self-initiated procedure is comparable to that observed in the standard procedure with a typical ITI, and superior to that observed in the standard procedure with an equally short ITI. Comparison with Existing Method(s) The self-initiated procedure permits delivering 100 trials in a ∼1-h session, almost doubling the number of trials safely attainable over that period with the standard procedure. Conclusions The self-initiated procedure enhances the collection of neural correlates of cue-reward learning while producing good discrimination performance. Other advantages for neural recording studies include ensuring that at the start of each trial the animal is engaged, attentive and in the same location within the conditioning chamber.

[1]  Daniel A. Gottlieb Acquisition with partial and continuous reinforcement in rat magazine approach. , 2005, Journal of experimental psychology. Animal behavior processes.

[2]  JOHN W. Moore A Neuroscientist's Guide to Classical Conditioning , 2002 .

[3]  E. Kandel,et al.  A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. , 1983, Science.

[4]  W. R. Salafia,et al.  Conditioning of the nictitating membrane response of the rabbit (Oryctolagus cuniculus) as a function of length and degree of variation of intertrial interval , 1973 .

[5]  Daniel A. Gottlieb Is the number of trials a primary determinant of conditioned responding? , 2008, Journal of experimental psychology. Animal behavior processes.

[6]  W. Schultz,et al.  Dopamine responses comply with basic assumptions of formal learning theory , 2001, Nature.

[7]  K. Lattal,et al.  Trial and intertrial durations in Pavlovian conditioning: issues of learning and performance. , 1999, Journal of experimental psychology. Animal behavior processes.

[8]  P. Holland Brain mechanisms for changes in processing of conditioned stimuli in Pavlovian conditioning: Implications for behavior theory , 1997 .

[9]  R. F. Thompson,et al.  Inhibitory cerebello-olivary projections and blocking effect in classical conditioning. , 1998, Science.

[10]  J. Gibbon,et al.  Temporal factors influencing the acquisition and maintenance of an autoshaped keypeck , 1975 .

[11]  P. Holland Trial and intertrial durations in appetitive conditioning in rats , 2000 .

[12]  J. W. Rudy,et al.  Rehearsal in animal conditioning. , 1973, Journal of experimental psychology.

[13]  R. R. Miller,et al.  Trial spacing and trial distribution effects in Pavlovian conditioning: contributions of a comparator mechanism. , 1994, Journal of experimental psychology. Animal behavior processes.

[14]  Geoffrey Schoenbaum,et al.  Neural Estimates of Imagined Outcomes in the Orbitofrontal Cortex Drive Behavior and Learning , 2013, Neuron.

[15]  Hank Davis,et al.  Operant-Pavlovian Interactions , 1977 .

[16]  M. A. MacIver,et al.  Neuroscience Needs Behavior: Correcting a Reductionist Bias , 2017, Neuron.

[17]  A. R. Wagner SOP: A Model of Automatic Memory Processing in Animal Behavior , 2014 .

[18]  M. Domjan Effects of the intertrial interval on taste-aversion learning in rats , 1980, Physiology & Behavior.

[19]  R. Rescorla,et al.  A theory of Pavlovian conditioning : Variations in the effectiveness of reinforcement and nonreinforcement , 1972 .

[20]  W. F. Prokasy,et al.  GSR CONDITIONING AND SENSITIZATION AS A FUNCTION OF INTERTRIAL INTERVAL. , 1964, Journal of experimental psychology.

[21]  N. Mackintosh The psychology of animal learning , 1974 .

[22]  Ralph R. Miller,et al.  Information processing in animals : memory mechanisms , 1983 .

[23]  P. Holland Conditioned stimulus as a determinant of the form of the Pavlovian conditioned response. , 1977, Journal of experimental psychology. Animal behavior processes.

[24]  H. Terrace,et al.  Autoshaping and Conditioning Theory , 1980 .

[25]  P. Barela Theoretical mechanisms underlying the trial-spacing effect in Pavlovian fear conditioning. , 1999, Journal of experimental psychology. Animal behavior processes.

[26]  Stephen Maren Neurobiology of Pavlovian fear conditioning. , 2001, Annual review of neuroscience.

[27]  P. Holland Intertrial interval effects in pavlovian serial feature positive discriminations , 1999 .

[28]  B. Campbell,et al.  Autonomic and behavioral correlates of appetitive conditioning in rats. , 1997, Behavioral neuroscience.

[29]  Justin A. Harris,et al.  Magazine approach during a signal for food depends on Pavlovian, not instrumental, conditioning. , 2013, Journal of experimental psychology. Animal behavior processes.

[30]  W. F. Prokasy,et al.  Classical conditioning II: Current research and theory. , 1972 .

[31]  J. Pearce,et al.  The strength of the orienting response during Pavlovian conditioning. , 1984, Journal of experimental psychology. Animal behavior processes.

[32]  S B Dunnett,et al.  Proactive interference effects on short-term memory in rats: I. Basic parameters and drug effects. , 1990, Behavioral neuroscience.

[33]  A. Dickinson,et al.  Neuronal coding of prediction errors. , 2000, Annual review of neuroscience.

[34]  J. Pearce,et al.  The strength of the orienting response during Pavlovian conditioning. , 1984, Journal of experimental psychology. Animal behavior processes.

[35]  P. Balsam,et al.  Context and Learning , 1985 .

[36]  S. Iversen,et al.  Proactive interference effects on short-term memory in rats: II. Effects in young and aged rats. , 1990, Behavioral neuroscience.

[37]  E. Kehoe,et al.  Fundamental Behavioral Methods and Findings in Classical Conditioning , 2002 .

[38]  Steven C Stout,et al.  Sometimes-competing retrieval (SOCR): a formalization of the comparator hypothesis. , 2007, Psychological review.

[39]  J. Pearce,et al.  The Strength of the Orienting Response during Blocking , 1984, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[40]  Ralph R. Miller,et al.  Sometimes-competing retrieval (SOCR): a formalization of the comparator hypothesis. , 2007, Psychological review.