Temporal maps in appetitive Pavlovian conditioning
Introduction
Learning about time is an integral part of associative learning (Balsam et al., 2010, Diaz-Mataix et al., 2013). Whether one considers such learning as the acquisition of a temporal map (Balsam and Gallistel, 2009, Honig and Urcuioli, 1981) or as the encoding of an attribute of the conditioned stimulus (CS) (Arcediano and Miller, 2002, Denniston and Miller, 2007, Molet and Miller, 2013) it is clear that temporal parameters have a large impact on learning and performance. The timing of events alters the speed with which anticipatory conditioned responses (CRs) emerge (Balsam and Gallistel, 2009, Gallistel and Gibbon, 2000, Gibbon and Balsam, 1981), the pattern of CR expression within the CS (Balsam et al., 2002, Brandon et al., 2003, Bitterman, 1965, Drew et al., 2005, Kirkpatrick and Church, 2003), and even the topography of the CR itself (Silva and Timberlake, 1997, Vogel et al., 2003, Smith, 1968, Holland, 1980). Additionally, once this temporal learning has occurred the information can be used in flexible ways. One feature of this flexibility makes it analogous to spatial maps; subjects can integrate temporal information across separate experiences when there are common elements in the learning episodes (Molet et al., 2012). Spatial maps of large areas are built up through sequential experiences of overlapping subsets of the total map (Collett et al., 2002, Gallistel and King, 2009, O’Keefe and Nadel, 1978, Shapiro et al., 1997). Though acquired sequentially, an integrated representation of the information can guide behavior to new locations (Blaisdell and Cook, 2005) or be used to infer novel routes to a goal (Foo et al., 2005, Foo et al., 2007, Gallistel, 1990, Tolman, 1948).
Evidence for a similar ability to integrate temporal information across separate experiences comes primarily from both second-order conditioning and sensory pre-conditioning (SPC) studies which have shown that animals have the ability to superimpose temporal maps from different training phases provided there are common elements in each phase (Molet et al., 2012). In an SPC experiment animals are first presented with forward pairings of two neutral CS's, A and B, where A immediately precedes B (A → B). In the next phase the value of one of these stimuli (B) is changed by pairing it with a motivationally significant event, for example a food unconditioned stimulus (US), B → Food. Once the CR has been established to B (B → CR), the integration of information across phases is evident when the changed value of B is reflected in a change in the value of A, even though A has never been directly associated with the US (A → CR). This integration reflects the animal's knowledge of the order and perhaps timing of events. For example, in a variant of the SPC procedure Miller and colleagues (Arcediano et al., 2003, Cole et al., 1995, Molet et al., 2012) showed that when B is backward paired with the US, B is not excitatory. Nevertheless, A controls a strong excitatory response as would be expected if subjects can infer that a US that comes before B would be expected just after A. Data like these encourage the view that animals are capable of integrating temporal information across experiences. Most studies have employed aversive conditioning paradigms and demonstrated that subjects can integrate order information. However the encoding and use of order information does not necessarily require a quantitative appreciation of time. The integration of temporal order and integration of quantitative temporal information may be separable processes mediated by different neural substrates (Buhusi and Meck, 2005, Eichenbaum, 2013, MacDonald et al., 2011, Ivry and Schlerf, 2008, Shapiro and Eichenbaum, 1999). Thus it is important to explore in more detail whether quantitative temporal information, like metric spatial information, can be integrated across experiences.
Only one appetitive conditioning study indicates that integration of quantitative temporal knowledge is possible (Leising et al., 2007). Here we explore this possibility in more detail. Experiment 1 sought to demonstrate temporal order integration in appetitive conditioning with a method similar to the aversive conditioning procedures of Arcediano et al. (2003). In subsequent experiments we explored the conditions that give rise to integration of quantitative temporal information across experiences.
Section snippets
Experiment 1
Experiment 1 sought to establish that temporal order information could be integrated across experiences in appetitive conditioning as demonstrated in aversive conditioning. Subjects were exposed to temporal information in two separate training phases as illustrated in Fig. 1. During the first phase of training two auditory cues (A and B) were presented in sequence. Two groups were exposed to these cues in forward order (A → B) as in a standard SPC experiment, while two groups experienced backward
Experiment 2
While the results of the previous experiment provide evidence of the integration of information, we did not find evidence of integration of the quantitative temporal relationship between the cues. Both Early-A and Late-A groups demonstrated similar high levels of responding throughout A. While this argues that the temporal order of A and B was preserved and integrated with the temporal location of the reward, it does not suggest that the quantitative temporal location of reward within A was
Experiment 3
Though Experiment 1 showed that animals could integrate temporal order information, responding to the SPC cues in Experiment 2 appeared to be dominated by generalization from the FOC cues. One possible reason for the difference between experiments may be the differing relation between cue onsets and offsets. In Experiment 1 all cues were non-overlapping, each with unique times of onset and offset. However in Experiment 2 A and B were completely embedded in C; the time of onset is shared between
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