A number of studies have been carried out on thalamic amnesia, with the aim of clarifying the role of thalamic nuclei and bundles in memory processes (von Cramon et al., 1985; Cipolotti et al., 2008; Carlesimo et al., 2011; Pergola et al., 2012). Dense pathways link the medial temporal lobe to the anterior part of the thalamus (Aggleton and Brown, 1999; Aggleton et al., 2011). More precisely, the Mamillothalamic tract/Anterior thalamic nucleus (MTT/AN) complex is thought to be critical for memory because of its direct and indirect connections with the hippocampus (Ghika-Schmid and Bogousslavsky, 2000; Van der Werf et al., 2000; Aggleton et al., 2011; Edelstyn et al., 2012). The mediodorsal (MD) may also play a role in memory, because of its direct connections with anterior subhippocampal structures, most notably the perirhinal cortex (Aggleton et al., 2011). An influential dual-process model suggested that the AN/MTT complex is critical for recollection, the ability to retrieve part of the experience associated with a stimulus, while the MD is important for familiarity, a simpler process related to the mere feeling that the stimulus has been experienced before (Aggleton and Brown, 1999). Contrary to single-process theories that state that recollection and familiarity map on to strong and weak memories, this model therefore assumed that these two processes are functionally and anatomically independent.

However, subsequent findings did not fully support this simple anatomical-functional dissociation. Although patients with AN lesions have impaired recollection, they also usually have lesions of other diencephalic structures, which sometimes hampers interpretation of the results (reviewed in Aggleton et al., 2011). Thus, a recurrent problem is that the AN’s role in recognition memory is often deduced from lesions to adjacent afferent structures, such as the mammillary bodies or the MTT, in the absence of specific AN damage (Carlesimo et al., 2007; Tsivilis et al., 2008; Vann et al., 2009). Some results also appear to contradict the model’s predictions. For example, Cipolotti et al. (2008) reported the case of two patients who both had damage to the left AN/MTT and MD. One of the patients also had damage to the right AN/MTT (and lateral dorsal nucleus), while the other had damage to the right MD. According to Aggleton and Brown’s model, these right-sided lesions should have meant that, for visual material, familiarity should have been preserved in the first patient and recollection should have been preserved in the second. However, these predictions were not borne out. Furthermore, in some patients with an AN lesion, familiarity is also impaired, albeit to a lesser extent than recollection (Kishiyama et al., 2005).

Similarly, we have yet to pinpoint the role of the MD in memory (Edelstyn et al., 2012; Cipolotti et al., 2008; Pergola et al., 2012; Tu et al., 2014). Experimental, selective, lesions of the medial region of the thalamus induced recognition memory impairment in nonhuman primates. It was hypothesised that they could more precisely be related to lesions of the magnocellular part of the MD (Aggleton and Mishkin, 1983a, Aggleton and Mishkin, 1983b; Parker et al., 1997). However, the magnitude of the impairment was moderate compared to direct lesions of the perirhinal cortex. Indeed, Aggleton and Brown (1999) noted that there could be other output routes from the perirhinal cortex to the rest of the brain than only through the MD. Furthermore, recordings in the MD (and in the paraventricular midline thalamic nuclei as well) in nonhuman primates revealed neurons that were sensitive to repetition, apparently supporting the view that this nucleus could be in involved in memory processes (Fahy et al., 1993).

In the human, Zoppelt et al. (2003) assessed recollection and familiarity in a group of five patients with MD lesions (three right, two left). These patients exhibited impairment of both processes, prompting the authors to argue for a role of the MD in recollection. Soei et al. (2008) reported impaired relational memory in six patients with MD damage (three left, two right, one bilateral). However, none of them exhibited nonrelational memory impairment, suggesting overall impaired recollection but preserved familiarity after MD damage. Recent studies using more refined imaging approaches to localize lesions have corroborated the idea that MD damage results in a recollection deficit (Pergola et al., 2012; Tu et al., 2014). By contrast, Edelstyn et al. (2016) described in a case study a patient with right MD damage who had a more pronounced deficit of familiarity than of recollection. This study followed two fMRI studies by the same group, which had evidenced activation of the MD in relation to familiarity (Montaldi et al., 2006; Kafkas and Montaldi, 2014). The MD may therefore play a role in recollection despite the prediction made by Aggleton and Brown (1999) (reviewed in Aggleton et al., 2011, and Carlesimo et al., 2015), and few studies have so far reported evidence in favour of the MD’s role in familiarity. Consequently, it has been suggested that the MD plays an indirect role in recollection because of its pattern of connectivity with the frontal lobes. A distinction has been drawn between the MDpc, which may be involved in recollection, and the MDmc, whose role remains more elusive (Pergola et al., 2012; Carlesimo et al., 2015). Furthermore, the role of other thalamic nuclei, such as the midline and intralaminar nuclei, which are often damaged along with the MD, has also been discussed.

Since neuropsychological investigations have pointed to a mixed pattern rather than a pure dissociation, Aggleton et al. (2011) revised their initial dual-process model of recollection and familiarity to integrate the complex connectivity of the thalamus. Their new multi-effect multi-nuclei (MEMN) model took into account the specific connectivity pattern of each thalamic nucleus. It described a continuum, rather than a dissociation, between the MTT/AN and MD. Furthermore, it suggested that the midline and intralaminar nuclei play a transitional role in recollection and familiarity (i.e., they influence these processes to varying extents). The authors particularly emphasized the MD’s role in familiarity, owing to its afferent connection from the perirhinal cortex, as well as in other cognitive functions, which could then impact recollection.

Overall, Aggleton’s models have received only mixed support concerning the role of the MD in familiarity, and this nuclei’s more general role in memory remains to be clarified. One of the problems facing researchers is the difficulty of recruiting large homogeneous groups of patients. Many studies report on one or a few patients at the most, and when samples are larger, they often include patients with both right and left damage to the thalamus, even though the thalamus exhibits a laterality effect (Edelstyn et al., 2012). In addition, the methods used to identify which thalamic nucleus has been damaged are usually limited to visual inspection, or else do not take all the damaged nuclei into account. Consequently, the aim of the current study was to overcome these limitations and assess how familiarity and recollection are affected by thalamic stroke, depending on which nuclei or bundles (e.g., MTT) are damaged. For this purpose, we recruited 14 patients with a first left thalamic stroke, along with 25 matched controls. All participants underwent a series of three verbal recognition memory tasks, each measuring recollection and familiarity in a different way, thus allowing us to assess these processes independently of the method used (Yonelinas, 2001; Bowles et al., 2007). An automated atlas was used to identify the location and extent of the damage to thalamus nuclei on the patients’ high-resolution 3D MRI (Danet et al., 2015). Two complementary methods were used to assess damage to the MTT. Given the updated MEMN model, we expected to observe impaired recollection in the case of AN or MTT lesions, and impaired familiarity and recollection in the case of MD lesions (Aggleton et al., 2011).

In the present study, we found that a large group of patients with left thalamic infarcts involving mainly the MD nucleus showed impaired recollection. Among the patients, those with MTT damage exhibited lower recognition performance. Unexpectedly, and contrary to the prediction that could be made following current models, patients with MD damage and intact MTT showed no familiarity impairment as well.

At first sight, our results appear to contradict the predictions made by Aggleton and colleagues models. In the original model, the MD supported familiarity (Aggleton and Brown, 1999), and the AN recollection. In the revised model, the MD supports familiarity and has an indirect effect on recollection. Both models predict that familiarity will be impaired following an MD lesion, regardless of whether recollection is impaired. Aggleton et al. (2011) stressed that this hypothesis remained unproven, even though two previous studies had suggested that there was no clear evidence of impaired familiarity following MD lesions (Zoppelt et al., 2003; Soei et al., 2008). However, a recent single-case study did report impaired familiarity following MD damage (Edelstyn et al., 2016). Using a task based on subjective report (Remember-Know paradigm), the authors found a dissociation between recollection and familiarity in patient OG. In a previous publication, they had localized the patient’s damage in the right MD, internal medullary lamina, intralaminar and midline nuclei according to Mai et al. (2004) and the method of Carlesimo et al. (2007). Comparing OG with 10 matched healthy controls they observed a significantly lower familiarity only for visual material (faces) whereas recollection was spared in the verbal and visual modality. In our study, we did not find any impairment of familiarity following an MD lesion in our group of 12 patients. We assessed familiarity in three different tasks, but none of these revealed a significant impairment, either at group or individual level. This was all the more surprising as our patients had a wide variety of thalamic lesions, although all of these were focused on the MD region. We had, therefore, expected at least some of the patients to display impaired familiarity. We found a moderate impairment of familiarity after averaging the familiarity indices across the three tasks (effect size A = 0.73). This appeared to be explained by lower overall familiarity in patients with concomitant MTT damage (Figure 5). Several possibilities need to be considered, however, before we can reach a conclusion as to the meaning of this finding.

A possibility is that familiarity is not impaired following MD lesions. Familiarity could in fact not depend on the MD, and possibly not on any thalamic nucleus at all. Familiarity is assumed to be a fast process (Brown and Aggleton, 2001), and it could be argued that direct connections between the MTT and the prefrontal cortex are more efficient than connections relayed by the thalamus although there are neural mechanisms that keep thalamo-cortical conduction velocity constant and fast across the cortex (Salami et al., 2003).

Interestingly, there are no connections between the perirhinal cortex and the thalamus in rodents (although, there are in nonhuman primates; for a review, see Aggleton et al., 2011), suggesting that this thalamic relay may not be absolutely critical in recognition memory tasks. Both lesion and electrophysiological studies in non-human primates suggested that the MD might play a role in recognition memory (Aggleton and Mishkin, 1983a, 1983b; Parker et al., 1997; Fahy et al., 1993). However, the impact on the performance of lesions of the MD was moderate (i.e., less severe than direct perirhinal cortex lesions). Furthermore, the idea that the MD could play a role in familiarity was not demonstrated, but seems to be merely an inference stemming from the observation that there are some direct connections from the perirhinal cortex to this nucleus (Aggleton et al., 1986; Russchen et al., 1987; Aggleton and Mishkin, 1983a). However, the importance of these connections and their functional role remains to be clarified. For example, the activity of the AN and of the neocortex was registered using implanted electrodes in epileptic patients during a memory task. The authors found that the activity of the two regions became synchronized during successful storage, providing direct evidence of the involvement of the AN in memory (Sweeney-Reed et al., 2014). Such a direct measure of the activity of the MD during a task based on familiarity could help making progress on this issue.

The idea that familiarity could be selectively impaired is based on a dual view of familiarity and recollection, whereby these processes would be functionally and anatomically independent. Many studies have shown that recollection can, indeed, be selectively impaired (Tsivilis et al., 2008; Vann et al., 2009). Recollection, therefore, appears to depend on a relatively well-circumscribed neural network, hierarchically organized, in which the hippocampus and diencephalic structures are critical components. Any lesion to this network impairs recollection, particularly since some of these areas are particularly sensitive to various neurological insults and are rather small (and thus easily damaged in their entirety). It is, therefore, tempting to see familiarity as a process paralleling recollection, both functionally and anatomically, with a similar network of dedicated brain areas. However, this does not have to be necessarily the case. Although it is quite easy to find patients with severe isolated impaired recollection, finding patients with isolated impaired familiarity remains surprisingly difficult to evidence. Indeed, very few studies have reported impaired familiarity but preserved recollection (Bowles et al., 2007; Martin et al., 2011; Brandt et al., 2016). Therefore, a possibility could be that familiarity could depend on a wider, more diffuse and partly redundant neural system. For example, the areas processing familiarity in the visual ventral streams could be rather large so that after a lesion, remaining preserved cortical patches could still partly process familiarity. Following up on this idea, it could be that the MD plays a role in familiarity, but that the neural system supporting familiarity could cope with MD lesions through redundancy or direct temporo-frontal connections. Here, we argue that the models of the brain network supporting familiarity could be revised without a priori attempt to parallel the one supporting recollection.

This idea is supported by recent suggestions that the view of familiarity as a single process is oversimplified, and that it actually follows a cascade of different simpler processes, such as perceptual and conceptual fluency, process attribution and post-retrieval monitoring (Whittlesea and Williams, 2000; Montaldi and Mayes, 2010; Besson et al., 2015). In other words, it is as yet unclear which aspect of familiarity is impaired after an MD lesion. If it is a higher-order process, performance could remain at a reasonably good level, but with impairment of some phenomenological aspect of familiarity. As recognition memory tasks are usually not designed to assess familiarity subprocesses, this may have gone unnoticed in both ours and previous studies. Future studies will therefore need to include tasks that concentrate on specific characteristics of familiarity, such as speed (Besson et al., 2012, 2015) or visuoperceptual processing (Migo et al., 2009).

In sum, familiarity was not found to be impaired across three different tasks relying on different measures of familiarity following MD damage, apparently contradicting the simple, dual-process, view of the role of the thalamus in memory. By contrast, this finding is a call to revisit models of familiarity and the role the MD plays in this process.

This leaves open the question of why the patients with damage to both the MD and the MTT exhibited impaired familiarity, whereas those with MD damage alone did not. Interestingly, the only other patient to be described in the literature as displaying impaired familiarity following MD damage also had an MTT lesion (Edelstyn et al., 2016), thus supporting our findings. Consequently, combined MTT and MD lesions may impair familiarity. This would hold true only for some patients, since not all our patients with combined MTT/MD damage exhibited impaired familiarity, compared with controls. Only one patient in our study had a lower familiarity score than that of the poorest performing control. One explanation for this finding is that another tract was damaged along with the MTT in some patients, such as the inferior thalamic peduncle, which connects the perirhinal cortex to the MD (Aggleton and Brown, 1999). An alternative explanation, however, is that this was related to damage to other thalamic nuclei. The patients with combined MTT/MD damage also had larger thalamic lesions overall, involving other nuclei besides the MD, such as the midline nuclei. They also present lower performance on recognition memory tasks (Figure 3) or memory in general (Danet et al., 2015) so that a specific role for the MTT in familiarity seems at present improbable. Undetermined anatomical factors could explain this result.

Our group of patients had impaired recollection. Given the known role of the MTT/AN complex in recollection (Tsivilis et al., 2008; Vann et al., 2009), it is no surprise that patients with lesions to this complex had impaired recollection. However, our subgroup of patients who had lesions in the MD region, but not of the MTT/AN complex, also exhibited impaired recollection. Recollection correlated with performance, but familiarity did not, suggesting that impaired recollection was responsible for impaired performance.

These findings appear to be highly consistent with previous results. Pergola et al. (2012) measured the contribution of recollection using a dissociation paradigm. Participants had to learn picture pairs. In a yes/no recognition phase, they were shown single-picture targets mixed with distractors. For all ‘yes’ responses, they were asked to recall the other picture in the pair. Twelve patients with MD lesions (six left, six right) were included in their study. Results showed that cued recall, taken as an index of recollection, correlated with MDpc volume loss. In line with Van der Werf et al. (2003), Pergola et al., therefore, argued for a role of this region in recollection, owing to its connectivity with the dorsolateral prefrontal cortex. More recently, Tu et al. (2014) reported selective impairment of delayed recall in seven patients with a left MD lesion but no MTT damage. Across these studies, the MD’s role in recall and recollection appears clear. This is also the case in our study. These findings are globally in line with Aggleton et al. (2011)’s model, and appear to corroborate this part of it.

Mitchell and Chakraborty (2013) reviewed the findings on MD lesion effects in 52 animal studies. These authors found that the MD has a number of subdivisions, each with its own neural circuit connecting it with the prefrontal cortex. They suggested that the MD plays a broad role in the regulation of cortical synchrony between medial temporal lobe structures and the prefrontal cortex. According to this view, recollection could be impaired following MD damage because of this lack of synchrony. Actually another explanation as to why the MD could be involved in recollection is that it could be involved in executive functions. However, we did not find any such correlation in the present study. Of note, nuclei other than the MD (central median and parafascicular) have been associated with a dysexecutive syndrome (Liebermann et al., 2013).

It should be noted that more work needs to be done to better understand the involvement of the thalamus, and particularly of the MD, in memory. It is at present difficult to precisely image the nuclei and tracts running within the thalamus. Dedicated structural MRI sequences, rather than state of the art but standard ones, could be developed in the near future and help refining current results. 7 Tesla, as opposed to current 3 Tesla, imaging in patients could also potentially be useful. This is important since specific lesions of the MD in non-human primates may result in quite different lesions than those resulting from thalamic strokes in the human. Comparisons are thus not entirely straight forward. There are also currently debates regarding how recollection and familiarity should be quantified and modelled, and whether dual-process approaches such as the ones we used in the current study, although widely used, are appropriate (Wixted et al., 2010; Pazzaglia et al., 2013; Moran and Goshen-Gottstein, 2015; Didi-Barnea et al., 2016). More specific issues have also not been clearly addressed in the literature on the thalamus regarding, for example, the impact of a possible left/right thalamic asymmetry on Aggleton et al. (2011) model. For example, we used verbal stimuli (words) in patients with left-sided lesions of the thalamus. However, it is noteworthy that the only study having reported impaired familiarity in a patient with MD (and MTT) lesions used faces in a patient with right-sided lesion. As noted earlier, future studies in patients could also favour tasks focusing specifically on familiarity processes (Migo et al., 2009; Besson et al., 2012).

In conclusion, even if the role of the MD in recognition memory becomes clearer, work needs to be continued to clarify the involvement of the thalamus in memory. Our study suggests that models of familiarity assigning a critical role to the MD should be reappraised.

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Author details

1. Lola Danet

   1. Toulouse NeuroImaging Center, Université de Toulouse, Inserm, Toulouse, France
   2. Brain and Cognition Research Centre, CNRS, University of Toulouse Paul Sabatier, Toulouse, France
   3. Neurology Department, CHU Toulouse Purpan, Toulouse, France

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Supervision, Validation, Visualization, Methodology, Writing—original draft, Writing—review and editing

   For correspondence

   lola.danet@inserm.fr

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-8507-6749

2. Jérémie Pariente

   1. Toulouse NeuroImaging Center, Université de Toulouse, Inserm, Toulouse, France
   2. Neurology Department, CHU Toulouse Purpan, Toulouse, France

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing

   Competing interests

   No competing interests declared

3. Pierre Eustache

   Toulouse NeuroImaging Center, Université de Toulouse, Inserm, Toulouse, France

   Contribution

   Data curation, Writing—review and editing

   Competing interests

   No competing interests declared

4. Nicolas Raposo

   1. Toulouse NeuroImaging Center, Université de Toulouse, Inserm, Toulouse, France
   2. Neurology Department, CHU Toulouse Purpan, Toulouse, France

   Contribution

   Data curation, Writing—review and editing

   Competing interests

   No competing interests declared

5. Igor Sibon

   Department of Diagnostic and Therapeutic Neuroimaging, University of Bordeaux, Bordeaux University Hospital, Bordeaux, France

   Contribution

   Data curation, Writing—review and editing

   Competing interests

   No competing interests declared

6. Jean-François Albucher

   1. Toulouse NeuroImaging Center, Université de Toulouse, Inserm, Toulouse, France
   2. Neurology Department, CHU Toulouse Purpan, Toulouse, France

   Contribution

   Data curation, Writing—review and editing

   Competing interests

   No competing interests declared

7. Fabrice Bonneville

   1. Toulouse NeuroImaging Center, Université de Toulouse, Inserm, Toulouse, France
   2. Neurology Department, CHU Toulouse Purpan, Toulouse, France

   Contribution

   Data curation, Writing—review and editing

   Competing interests

   No competing interests declared

8. Patrice Péran

   Toulouse NeuroImaging Center, Université de Toulouse, Inserm, Toulouse, France

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Visualization, Methodology, Writing—review and editing

   Competing interests

   No competing interests declared

9. Emmanuel J Barbeau

   Brain and Cognition Research Centre, CNRS, University of Toulouse Paul Sabatier, Toulouse, France

   Contribution

   Conceptualization, Software, Formal analysis, Supervision, Visualization, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0836-3538

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