The Ventral Midline Thalamus (Reuniens and Rhomboid Nuclei) Contributes to the Persistence of Spatial Memory in Rats

Abstract

The formation of enduring declarative-like memories engages a dialog between the hippocampus and the prefrontal cortex (PFC). Electrophysiological and neuroanatomical evidence for reciprocal connections with both of these structures makes the reuniens and rhomboid nuclei (ReRh) of the thalamus a major functional link between the PFC and hippocampus. Using immediate early gene imaging (c-Fos), fiber-sparing excitotoxic lesion, and reversible inactivation in rats, we provide evidence demonstrating a contribution of the ReRh to the persistence of a spatial memory. Intact rats trained in a Morris water maze showed increased c-Fos expression (vs home cage and visible platform groups: Ͼ500%) in the ReRh when tested in a probe trial at a 25 d delay, against no change at a 5 d delay; behavioral performance was comparable at both delays. In rats subjected to excitotoxic fiber-sparing NMDA lesions circumscribed to the ReRh, we found normal acquisition of the water-maze task (vs sham-operated controls) and normal probe trial performance at the 5 d delay, but there was no evidence for memory retrieval at the 25 d delay. In rats having learned the water-maze task, lidocaine-induced inactivation of the ReRh right before the probe trial did not alter memory retrieval tested at the 5 d or 25 d delay. Together, these data suggest an implication of the ReRh in the long-term consolidation of a spatial memory at the system level. These nuclei could then be a key structure contributing to the transformation of a new hippocampal-dependent spatial memory into a remote one also depending on cortical networks.

Hippocampal Formation

“…Reuniens excitatory inputs apparently converge with inputs from EC on single pyramidal cell dendrites (unpublished observations). The synaptic organization of reuniens inputs to CA1 (and to Sub; see below) likely forms the substrate mediating the documented relevance of reuniens in learning (Loureiro et al, 2012). Like CA3, the CA1 field receives light noradrenergic, serotonergic, and dopaminergic projections (Swanson et al, 1987).…”

Functional heterogeneity of the limbic thalamus: From hippocampal to cortical functions

“…In fact, specific lesions to the intralaminar (Lopez et al, 2009;Moreau et al, 2013;Wolff et al, 2008a), midline (Loureiro et al, 2012) or even mediodorsal nuclei (Cain et al, 2006) spare spatial navigation, which further suggests that this ability specifically relies on ATN functions. Of course, the possible additional involvement of other thalamic nuclei cannot be excluded until they are explicitly tested under these conditions.…”

Orexin-dependent activation of layer VIb enhances cortical network activity and integration of non-specific thalamocortical inputs

“…Hence, acetylcholine-dependent recruitment of layer VIb may require synchrony between cholinergic and non-specific thalamic inputs, whereas orexin-dependent recruitment is likely to proceed on a more tonic mode. Non-specific thalamic nuclei collectively upregulate cortical arousal (Moruzzi and Magoun 1949;Jasper et al 1953), but these diverse nuclei subserve specific roles in sensory-motor and cognitive functions associated with well-defined and complementary innervations of cortical areas (Berendse and Groenewegen 1991;Van der Werf et al 2002;Vertes et al 2006;Hembrook and Mair 2011;Loureiro et al 2012;Cholvin et al 2013). Orexins promote arousal and vigilance and likewise change the firing of Rh neurons from bursting to tonic (Bayer et al 2002), which facilitates cortical activation and allows information transfer (McCormick and Bal 1997).…”