In dynamic environments, the ability to engage in adaptive behaviors is essential to meet basic needs and desires. This sometimes requires updating the current understanding of rules governing events or actions. A large literature has documented that such goal-directed behaviors rely on highly flexible cognitive processes that appear to be largely supported by prefrontal cortical areas (O'Doherty et al., 2017; Parkes and Coutureau, 2018). However, mounting experimental evidence indicates that functional interactions between prefrontal and subcortical areas are essential to support these functions (Balleine and O'Doherty, 2010; Verschure et al., 2014). In particular, the contribution of several thalamic nuclei is now better understood and acknowledged in current views on the functioning of thalamocortical circuits (Pergola et al., 2018; Rikhye et al., 2018b; Wolff and Vann, 2019).

Recently, the interactions between the medial prefrontal cortex (mPFC) and the mediodorsal thalamus (MD) have been highlighted in multiple behavioral setups and through various causal interventions (Bradfield et al., 2013; Browning et al., 2015; Bolkan et al., 2017; Schmitt et al., 2017; Alcaraz et al., 2018; Marton et al., 2018; Rikhye et al., 2018a). For instance, we recently reported that thalamocortical and corticothalamic pathways connecting the mPFC and the MD support complementary but dissociable aspects of goal-directed behavior (Alcaraz et al., 2018). However, the mPFC is not the only cortical recipient of MD projections as the orbitofrontal cortex (OFC) is also one of its main cortical targets (Groenewegen, 1988; Alcaraz et al., 2016). Interestingly, while the OFC has long been associated with stimulus-outcome predictions (Balleine et al., 2011; McDannald et al., 2014; Stalnaker et al., 2014), its contribution to flexible goal-directed responding has now also been highlighted (Gremel and Costa, 2013; Bradfield et al., 2015; Bradfield et al., 2018; Panayi and Killcross, 2018; Parkes et al., 2018). Beyond MD afferents, the OFC is also the recipient of a massive projection from the submedius thalamus (Sub) (Yoshida et al., 1992; Alcaraz et al., 2015; Kuramoto et al., 2017). While this region is currently poorly understood, it was recently demonstrated to support the updating of stimulus-outcome associations, in a manner that was highly reminiscent of OFC functions (Alcaraz et al., 2015). This suggests that a complex interplay occurs between the OFC and its thalamic afferents when flexible responding is essential.

Thus, in the present study, we aimed to build upon our previous study (Alcaraz et al., 2018) and to disentangle the functional interactions of the OFC with its two main thalamic afferents. To this end, we used an instrumental training paradigm allowing to test for initial action-outcome encoding but also its reversal (Parkes et al., 2018). The latter forces rats to engage in flexible responding. We then assessed the impact of disconnecting the OFC either from its MD afferent (Experiment 1) or from its Sub afferent (Experiment 2). We found that disconnecting the OFC from the MD left instrumental performance unaltered throughout all phases of testing. Interestingly, disconnecting the OFC from the Sub produced a marked and selective impairment in goal-directed responding following action-outcome reversal. The current set of results, together with prior evidence (Alcaraz et al., 2018), indicate that distinct thalamocortical circuits may act in parallel as a function of current behavioral demand.

In a recent study, we showed that functional interactions between the mediodorsal thalamus (MD) and the medial prefrontal cortex are essential for goal-directed decision-making (Alcaraz et al., 2018). As the MD also connects with the orbitofrontal cortex (OFC), a region now known to play a role in goal-directed behavior (Parkes et al., 2018), the present study primarily aimed to extend our prior findings by focusing on MD-OFC interactions. We found that disconnecting the OFC from the MD produced no detectable impairment, even after reversal of action-outcome contingencies. This prompted us to examine whether thalamocortical interactions between the OFC and its other main thalamic afferent, the submedius thalamic nucleus (Sub), could support performance in this situation. The results clearly indicated a specific role for the OFC-Sub circuit in guiding choice after action-outcome contingency reversal. Taken as a whole, the data suggest an important role for this thalamocortical circuit in goal-directed behavior and further underscore the functional importance of a still poorly known thalamic region.

The MD is now acknowledged as a major partner of the prefrontal cortex for cognition, from rodent to primate, including humans (Bradfield et al., 2013; Browning et al., 2015; Wolff et al., 2015; Parnaudeau et al., 2018; Pergola et al., 2018; Rikhye et al., 2018b; Wolff and Vann, 2019). However, to date, most experimental studies have examined its functional interactions with the medial prefrontal cortex (Bolkan et al., 2017; Schmitt et al., 2017; Alcaraz et al., 2018; Marton et al., 2018; Rikhye et al., 2018a), thus neglecting the potential importance of its abundant connections with the OFC (Alcaraz et al., 2016; Murphy and Deutch, 2018). The present study does not support the idea that these interactions are important for goal-directed behavior, even in a setup known to engage OFC functions (Parkes et al., 2018). The functional relevance of the OFC-MD connections has been documented in other settings as both MD and OFC neurons were found to code for task-relevant elements in an odor-discrimination task (Courtiol and Wilson, 2016); however, this feature was not affected by inhibition of the corticothalamic pathway (Courtiol et al., 2019). In the primate, disconnecting the MD from the ventrolateral and orbital cortex impairs adaptive decision-making after selective outcome devaluation (Browning et al., 2015). By contrast, we observed the same effect after disconnecting the MD from the medial prefrontal cortex (Alcaraz et al., 2018) but not the OFC (present data). This certainly calls for further work to document the functional equivalence of prefrontal territories in rodent and primate (Laubach et al., 2018), especially when the functional parcellation of the OFC is now becoming clearer (Izquierdo, 2017; Panayi and Killcross, 2018). Thus, more work is needed to identify the functions that may be supported by connections between the OFC and the MD. An attractive prospect could be to rely on situations where choice is guided by stimulus-outcome associations, as previously suggested (Ostlund and Balleine, 2008; Wolff et al., 2015; Alcaraz et al., 2016).

Disconnecting the OFC from the Sub did not impair the ability to learn action-outcome associations and to use this information to guide choice. However, when action-outcome associations were reversed, rats with contralateral lesions of the OFC-Sub pathway were unable to integrate this new information to guide subsequent choice between the two actions. This does not necessarily imply that these animals were unable to notice these changes during the reversal phase. If that was the case they would show a devaluation effect consistent with the original contingencies, which was not observed during that test. Instead, reduced responding was observed for both actions, suggesting that these rats could not accurately segregate multiple action-outcome contingencies. It is also possible that reversal learning was incomplete. Indeed, the current study did not assess whether contralateral lesioned rats would learn the reversed contingencies with additional training but even if that was the case, it is clear that reversal learning is at least slowed down by OFC-Sub disconnection. Both hypotheses therefore point to a specific deficit in updating contingency information rather than an overall deficit in learning the relationship between actions and their outcomes. This is consistent with a prior study indicating a deficit in the ability to update stimulus-outcome contingencies in Sub lesioned rats (Alcaraz et al., 2015). Overall, this suggests that connections between the OFC and the Sub are critical to distinguish between learning experiences or task states (Wilson et al., 2014). It is also consistent with the emerging view that the cognitive thalamus critically assists the cortex to ensure that mental representations or cognitive maps are still relevant (Wolff and Vann, 2019).

A limitation of the present approach however lies in the lesion disconnection procedure. While targeting projection-defined cortical and thalamic neurons previously enabled us to differentiate the functional contribution of thalamocortical and corticothalamic pathways (Bolkan et al., 2017; Alcaraz et al., 2018), it is not possible with this lesion approach to assign specific functions to OFC-to-Sub and Sub-to-OFC pathways. Moreover, while thalamocortical projections are known to be almost exclusively ipsilateral, returning corticothalamic pathways cross to the other hemisphere (Négyessy et al., 1998). Thus, the latter would not be compromised with the present approach. Keeping this in mind, we cannot formally exclude that targeting more efficiently both thalamocortical and corticothalamic pathways would produce different results when addressing the OFC-MD circuit. By contrast, this further clarifies the involvement of the OFC-Sub circuit, as the remaining contralateral corticothalamic pathways were not sufficient to support the updating of instrumental contingencies.

Together with prior evidence concerning the MD (Alcaraz et al., 2018) and the Sub (Alcaraz et al., 2015), the present set of data clarify the nature of the functional interactions between cortical and thalamic areas. First, distinct thalamocortical circuits appear to support instrumental performance, depending on whether updating of the associative structure of the task is required: after initial instrumental training, functional interactions between the mPFC and the MD but not the OFC and the Sub are necessary to guide choice based on current goal value but the exact opposite pattern is found after action-outcome reversal. In other words, there is striking double dissociation regarding the functional involvement of the mPFC-MD and the OFC-Sub circuits in instrumental performance. This major result fits well with novel conceptions of the functioning of thalamocortical circuits, emphasizing parallel and synergetic information processing to achieve cognitively relevant functions (Rikhye et al., 2018b; Wolff and Vann, 2019). Second, the present data are in agreement with a broader conception of OFC functions but they also highlight the contribution of a poorly understood thalamic region. The Sub indeed appears to be important to update not only stimulus-outcome but also action-outcome associations, consistent with the idea that thalamic nuclei may help to shape mental representations (Wolff and Vann, 2019). Finally, it would be very useful to document the functions that may be supported by OFC-MD connections. As thalamic afferents from both the Sub and the MD terminate within the same OFC loci (Alcaraz et al., 2015; Alcaraz et al., 2016), this would provide an ideal venue to investigate the functional relevance of convergence in cognition (Man et al., 2013).

In conclusion, the present study complements prior findings to broaden our understanding of the functioning of thalamocortical circuits. Rather than acting as isolated loops assigned to specific functions, they would be better described as supporting each other in the face of changing circumstances. An influential view posits that cortical areas may communicate directly but also indirectly through the thalamus (Sherman, 2016; Sherman, 2018; Usrey and Sherman, 2019). One consequence of this functional organization is that convergent and divergent thalamocortical and corticothalamic pathways may help to recruit the currently relevant circuit and/or to gate the most meaningful inputs (Wolff and Vann, 2019). Thus, ensuring the accuracy of mental representations over time, and over changing circumstances, likely necessitates the cooperation of multiple circuits. As noted previously, this suggests cautious use of causality concepts to interpret data in contemporary neurosciences (Yoshihara and Yoshihara, 2018). Thalamic research has now entered a new era and we can expect in the coming years a more systematic assessment of thalamocortical circuits that should provide important insights to better apprehend mental conditions best described as connectivity disorders such as schizophrenia (Anticevic et al., 2014), obsessive-compulsive behaviors (Greenberg et al., 2010; Monteiro and Feng, 2016) or addiction (Balleine et al., 2015).

All data generated or analysed during this study are included in the manuscript and supporting files.

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Author details

1. Virginie Fresno

   1. CNRS, INCIA, UMR 5287, Bordeaux, France
   2. Université de Bordeaux, INCIA, UMR 5287, Bordeaux, France

   Contribution

   Data curation, Formal analysis, Investigation, Methodology

   Competing interests

   No competing interests declared

2. Shauna L Parkes

   1. CNRS, INCIA, UMR 5287, Bordeaux, France
   2. Université de Bordeaux, INCIA, UMR 5287, Bordeaux, France

   Contribution

   Conceptualization, Funding acquisition, Methodology, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7725-8083

3. Angélique Faugère

   1. CNRS, INCIA, UMR 5287, Bordeaux, France
   2. Université de Bordeaux, INCIA, UMR 5287, Bordeaux, France

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

4. Etienne Coutureau

   Université de Bordeaux, INCIA, UMR 5287, Bordeaux, France

   Contribution

   Conceptualization, Funding acquisition, Methodology, Writing—review and editing

   Contributed equally with

   Mathieu Wolff

   For correspondence

   etienne.coutureau@u-bordeaux.fr

   Competing interests

   No competing interests declared

5. Mathieu Wolff

   Université de Bordeaux, INCIA, UMR 5287, Bordeaux, France

   Contribution

   Conceptualization, Supervision, Funding acquisition, Investigation, Methodology, Writing—original draft, Project administration

   Contributed equally with

   Etienne Coutureau

   For correspondence

   mathieu.wolff@u-bordeaux.fr

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3037-3038

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