Beyond Spatial Memory: The Anterior Thalamus and Memory for the Temporal Order of a Sequence of Odor Cues

Abstract

Influential recent proposals state that the anterior thalamic (AT) nuclei constitute key components of an "extended hippocampal system." This idea is, however, based on lesion studies that used spatial memory tasks and there has been no evidence that AT lesions cause deficits in any hippocampal-dependent nonspatial tasks. The present study investigated the role of the AT nuclei in nonspatial memory for a sequence of events based on the temporal order of a list of odors, because this task has recently been shown to depend on the integrity of the hippocampal formation. After preoperative training, rats with excitotoxic lesions of the AT nuclei showed a severe and selective postoperative impairment when required to remember the order of pseudorandom sequences of six odors. The rats with AT lesions were able instead to learn two new tasks that required recognition memory and the identification of the prior occurrence of events independent of their order. These results strongly matched those described after hippocampal lesions and provide the first unequivocal evidence of a detrimental effect of an AT lesion on a nonspatial hippocampal-dependent memory task.

Unraveling the contributions of the diencephalon to recognition memory: A review

“…Comparisons between two objects, one presented 2 h previously, the other presented 1 h previously, found a normal preference for the older object after anterior thalamic lesions (Mitchell and Dalrymple-Alford 2005). In contrast, Wolff et al (2006) reported that rats with anterior thalamic lesions were impaired at discriminating the temporal order of odors. There are numerous differences in the procedures used to examine object and odor recency, including task difficulty, the requirement to learn a reinforced rule (only in the olfactory task), and the intervals between the recent and less recent stimuli.…”

“…It has repeatedly been found that lesions of the anterior thalamic nuclei do not affect standard SOR tasks Warburton and Aggleton 1999;Wilton et al 2001;Moran and Dalrymple-Alford 2003;Mitchell and Dalrymple-Alford 2005), nor do they affect novel odor detection (Wolff et al 2006). In the SOR studies, the retention delays have been extended up to 120 min, but no evidence has emerged of a time-dependent deficit.…”

Effects of number of items and interval length on the acquisition of temporal order discrimination in radial maze in rats

“…It is possible that memory strength of the first item that animals experienced 40 min before declined with the passage of time compared with that they experienced 4 min before, while memory strength of the lastly presented item in the study phase is thought to be equal, because the interval between the last item presentation and the beginning of the test phase was constant in both 4-min and 40-min interval groups. In fact, previous studies using odor stimuli showed that memory of items presented recently in the sequence was stronger than that presented previously (Fortin et al 2002;Wolff et al 2006). In case the subjects used this difference of memory strength in order to discriminate the order of items, the temporal order memory task with a 40-min interval was expected to be easier than that with a 4-min interval.…”

“…However, up to the present, this is not clear. Wolff et al (2006) proposed the importance of the first and/or the last items in the study phase and suggested the possibility that greater temporal lag effects shown in previous reports occurred because the largest lag condition was tested by two extreme items (the first vs. the last items), but other lag conditions contained various test pairs, at most only one extreme item. Although in every temporal lag condition except the largest lag there are various kinds of pairs that include or do not include extreme items, only a few previous studies analyzed the performance in each test pair within the same lag size.…”

“…A phenomenon that performance is better when subjects discriminate temporally distant items (larger lag) compared with temporally adjacent items (smaller lag) is termed a temporal lag effect. In rodents studies, temporal lag effect has been observed in temporal order memory of spatial locations (Chiba et al 1994(Chiba et al , 1997Gilbert et al 2001;Marquis et al 2003) and odors (Fortin et al 2002;Kesner et al 2002;Ergorul and Eichenbaum 2004;Wolff et al 2006). This effect was also observed in human studies (Hopkins et al 1995;St Jacques et al 2008;Pirogovsky et al 2009).…”