Timing of omitted events: An analysis of temporal control of inhibitory behavior

Abstract

This paper reviews research designed to investigate the temporal control of inhibitory responding using rats as subjects. One area of investigation has focused on the role of temporal variables in conditioned inhibition produced using Pavlov's (1927) procedure. These studies have found that evidence of conditioned inhibition obtained by negative summation testing is strongest when the conditioned inhibitor signals the omission of the US at the same temporal location as a transfer excitor signals presentation of the US (e.g., Barnet & Miller, 1996). Similarly, retardation of acquisition of behavioral control by a previously inhibitory CS is maximal when the inhibitory CS is paired with the US at the same temporal location as the inhibitor had previously signaled US omission (Burger, Denniston, & Miller, 2001). Other lines of research designed to assess the associative structure of temporal control of inhibition (e.g., Denniston, Blaisdell, & Miller, 2004) are reviewed, as is the assessment of temporal control of inhibition produced through extinction (Denniston & Miller, 2003). These collective observations are discussed in terms of the temporal coding hypothesis (Matzel, Held, & Miller, 1988). Timing of Omitted Events: An Analysis of Temporal Control of Inhibitory BehaviorThe analysis of temporal variables in conditioned behavior has been widely studied since the pioneering work of Pavlov (1927). Pavlov's studies of inhibition of delay revealed that following conditioned stimulus (CS)-unconditioned stimulus (US) pairings with a CS of long duration, conditioned responding was maximal during the latter parts of the CS. Pavlov's early work both highlighted the importance of timing in conditioned behavior and provided the foundation for a thorough analysis of how animals both perceive and use temporal information. For the last 40 years, the study of animal timing has been inspired and led by Russell Church. A few of the many great contributions of Church's work include the development of the peak procedure (Roberts & Church, 1978) and theorizing concerning internal clocks (Church, 1984) that model how animals learn about expected times of reinforcement and subsequently use this information in order to control conditioned responding. In contrast to this large literature, the present article summarizes the findings from a far smaller collection of research that has attempted to study analogous questions in inhibitory learning; specifically how animals temporally encode omitted events.Mailing Address: James C. Denniston, Department of Psychology, Appalachian State University, Boone, NC 28608, TEL: (828) 262-8640, FAX: (828) 262-2974, E-mail: dennistonjc@appstate.edu. Support for this research was provided by National Institute of Mental Health Grant 33881. We thank Bridget McConnell, Gonzalo P. Urcelay, Koji Urushihara, Daniel S. Wheeler, and James Witnauer for comments on an earlier version of this manuscript. For information concerning this research, contact James C. Denniston at dennistonjc@appstate.edu. NI...

A Rescorla-Wagner Drift-Diffusion Model of Conditioning and Timing

“…Conditioned inhibition poses higher technical challenges for a model of learning and timing as responses cannot be directly observed. To assess conditioned inhibition two types of measures are used (Denniston and Miller, 2007): summation and retardation tests. There are different procedures that can generate inhibition, so we refer here specifically to the inhibition produced by alternating A+ with AB-trials.…”

“…In retardation tests, the inhibitor by itself is now paired with the US, and it is said to pass the test if acquisition is slower than with a neutral stimulus. Denniston and Miller (2007) reviewed a series of studies that varied the durations of the training excitor and that between the inhibitor and the training excitor. The studies showed that conditioned inhibition is observed when the temporal relations between training and testing are preserved, and not otherwise.…”

Determinants of cue interactions

“…1 Note that there are no inhibitory associations. Behavior indicative of inhibition arises as a result of the relative values of different excitatory associations (see Denniston and Miller, 2007).…”

Molecular mechanisms underlying formation of long-term reward memories and extinction memories in the honeybee (Apis mellifera)

“…Several learning phenomena known from studies on classical conditioning in vertebrates have been demonstrated in honeybees, including trace conditioning (Szyszka et al 2011), backward conditioning (Bitterman et al 1983Hellstern et al 1998;Dacher and Smith 2008;Felsenberg et al 2014a), second-order conditioning (Hussaini et al 2007), extinction learning (Sandoz and Pham-Delegue 2004;Stollhoff et al 2005;Eisenhardt and Menzel 2007;Stollhoff and Eisenhardt 2009;Plath et al 2012), sensory preconditioning (Müller et al 2000, and blocking (Guerrieri et al 2005; for a contrasting review, see Gerber and Ullrich 1999), latent inhibition (Chandra et al 2010), and occasion setting (Mota et al 2011). These phenomena are surprisingly similar to vertebrates, in which they were initially described (Bouton 1993;Fanselow 1998;Schmajuk et al 1998;Myers and Davis 2002;Gewirtz and Davis 2006;Denniston and Miller 2007;Raybuck and Lattal 2014). This suggests that the underlying neuronal mechanisms are also likely based on common principles.…”