Abstract
Ultimately associative learning is a function of the temporal features and relationships between experienced stimuli. Nevertheless how time affects the neural circuit underlying this form of learning remains largely unknown. To address this issue, we used single-trial auditory trace fear conditioning and varied the length of the interval between tone and foot-shock. Through temporary inactivation of the amygdala, medial prefrontal-cortex (mPFC), and dorsal-hippocampus in rats, we tested the hypothesis that different temporal intervals between the tone and the shock influence the neuronal structures necessary for learning. With this study we provide the first experimental evidence showing that temporarily inactivating the amygdala before training impairs auditory fear learning when there is a temporal gap between the tone and the shock. Moreover, imposing a short interval (5 s) between the two stimuli also relies on the mPFC, while learning the association across a longer interval (40 s) becomes additionally dependent on a third structure, the dorsal-hippocampus. Thus, our results suggest that increasing the interval length between tone and shock leads to the involvement of an increasing number of brain areas in order for the association between the two stimuli to be acquired normally. These findings demonstrate that the temporal relationship between events is a key factor in determining the neuronal mechanisms underlying associative fear learning.
Highlights
The mammalian brain is able to associate events across a broad range of time intervals, from millisecond (Christian and Thompson, 2003; Woodruff-Pak and Disterhoft, 2008) to hours (Welzl et al, 2001; Stehberg and Simon, 2011)
Results presented in Experiments 1 and 2 suggest that the medial prefrontal-cortex (mPFC) is required for trace fear conditioning (tFC) acquisition regardless the length of the trace interval
Previous studies using conditioning protocols consisting of multiple trials of co-terminating tone–shock pairings have shown that under such conditions associative fear learning is independent of the mPFC (Morgan and LeDoux, 1995; Corcoran and Quirk, 2007)
Summary
The mammalian brain is able to associate events across a broad range of time intervals, from millisecond (Christian and Thompson, 2003; Woodruff-Pak and Disterhoft, 2008) to hours (Welzl et al, 2001; Stehberg and Simon, 2011). In auditory trace fear conditioning (tFC), the two stimuli are separated in time In this paradigm tone–shock association has been shown to occur across different trace intervals lengths, from 0.5 to 45 s (Baeg et al, 2001; Quinn et al, 2002; Misane et al, 2005), being acquired after a single-trial (Stiedl and Spiess, 1997; Misane et al, 2005). This paradigm is suited to investigate how differences in the temporal distance between two stimuli may influence the mechanisms underlying associative learning
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