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

Abstract

Both clinical investigations and studies with animals reveal nuclei within the diencephalon that are vital for recognition memory (the judgment of prior occurrence). This review seeks to identify these nuclei and to consider why they might be important for recognition memory. Despite the lack of clinical cases with circumscribed pathology within the diencephalon and apparent species differences, convergent evidence from a variety of sources implicates a subgroup of medial diencephalic nuclei. It is supposed that the key functional interactions of this subgroup of diencephalic nuclei are with the medial temporal lobe, the prefrontal cortex, and with cingulate regions. In addition, some of the clinical evidence most readily supports dual-process models of recognition, which assume two independent cognitive processes (recollective-based and familiarity-based) that combine to direct recognition judgments. From this array of information a "multi-effect multinuclei" model is proposed, in which the mammillary bodies and the anterior thalamic nuclei are of preeminent importance for recollective-based recognition. The medial dorsal thalamic nucleus is thought to contribute to familiarity-based recognition, but this nucleus, along with various midline and intralaminar thalamic nuclei, is also assumed to have broader, indirect effects upon both recollective-based and familiarity-based recognition.Clinical studies repeatedly show that diencephalic pathology can impair recognition memory. Even so, there is no agreed locus within the diencephalon responsible for this memory loss and, hence, no agreed mechanism to explain the impairment. The present review examines both clinical and animal findings, and from this information a multi-effect multi-nuclei (MEMN) model emerges to explain the contributions of the diencephalon to recognition memory.At the outset, it is necessary to refine the focus of this review and to define some of its principal terms. The diencephalon comprises the thalamus and hypothalamus but, as will be explained, only the more medial parts of the diencephalon will be considered in detail. Recognition memory refers to the ability to detect whether a stimulus (e.g., a word, face, picture, object, or sound) has previously been encountered. As a consequence, this review is not about item identification (sometimes also confusingly referred to as recognition). Likewise, conditions that have broad disruptive effects on cognition, e.g., dementia, will not be considered even though recognition is typically impaired. Distinctions will be made between "item recognition," where the task is to determine if an individual item is novel or familiar, and "associative recognition," where all the individual items being experienced are familiar, but their particular combination is novel. A further, distinct ability is "recency" discrimination-the ability to determine which of two familiar stimuli has been experienced more recently. Both studies of amnesia and electrophysiological recordings show how recency memory and recogniti...

The medial dorsal thalamic nucleus and the medial prefrontal cortex of the rat function together to support associative recognition and recency but not item recognition

“…In a recent review Aggleton et al (2011) proposed a new model of thalamic contributions to recognition memory, the multi-effect multinuclei (MEMN) model. This model asserts that the MD can contribute to both familiarity and recollective processes either directly via an interaction with the prefrontal cortex or indirectly as a result of cortical diaschesis .…”

A deficit in familiarity-driven recognition in a right-sided mediodorsal thalamic lesion patient.

“…If the thalamic connectivity of the hippocampal system was partially disrupted by lesions of the central medial midline nucleus and/or the MTT, then the DPSD/MEMN view would predict a disruption of recollection such that any evidence of impaired recollection and free recall of visual information might be attributable this. Similarly, if OG's right-sided medial thalamic damage disrupted projections with other subcortical structures considered to modulate arousal and attention (Aggleton et al, 2011), then the DPSD/MEMN view again would predict that recollection would have been likely to have been more disrupted than familiarity insofar as it is more arousal and attention demanding.…”

“…The suggestion is that they do this either by modulating a subcortical-cortical arousal and attention system that includes the reticular activating system and the reticular thalamic nucleus (Portas et al, 1998;Van der Werf, Witter, & Groenewegen, 2002;Van Der Werf, Jolles, Witter & Uylings, 2003) or by disrupting learning and memory by disconnecting indirect projections between the intralaminar (center median) and midline (central medial, paraventricular, parataenial, rhomboid, reuniens) thalamic nuclei and the hippocampal formation (Amaral & Cowan, 1980). The MEMN model also suggests that damage to the midline nuclei could impair familiarity because, like the mMDT, a subset of these midline nuclei (paraventricular, parataenial, rhomboid, reunion) are connected with the perirhinal and entorhinal cortices (see Aggleton et al, 2011;Pergola et al, 2012). Consequently, damage to the midline nuclei may also cause a familiarity deficit.…”

“…A recent thalamic extension of the Aggleton and Brown (1999) model (Aggleton, Dumont, & Warburton, 2011) provided a possible mechanism by which recollection impairments can develop following pathology that falls outside of the core hippocampal system. This multieffect multinuclei (MEMN) model includes the DPSD proposal that the core hippocampal system is selectively critical for recollection and the perirhinal-mMDT circuit for familiarity but adds the suggestion that other medial thalamic nuclei-comprising the intralaminar (center median) and midline (central medial, paraventricular, parataenial, rhomboid, reuniens) thalamic nuclei-can influence recollection.…”

Transient relay function of midline thalamic nuclei during long-term memory consolidation in humans

“…However, rodent hippocampal-mPFC fibers are unidirectional and rather unevenly distributed over the hippocampus (Vertes et al 2007;Hoover and Vertes 2012) and thus, an indirect interaction appears necessary if a bidirectional information flow between mPFC and hippocampus is required during systems consolidation. The rat's thalamic midline structures (nucleus reuniens/rhomboid nucleus) are reciprocally connected to both the mPFC and hippocampus as well as to posterior representational areas (Aggleton and Brown 1999;Van der Werf et al 2002;Vertes et al 2006Vertes et al , 2007Hoover and Vertes 2012;Cassel et al 2013;Wheeler et al 2013) that seems also evident in nonhuman primates (Amaral and Cowan 1980;DeVito 1980;Aggleton et al 1986Aggleton et al , 2011Hsu and Price 2007). Indeed, the nucleus reuniens acts as a hippocampal-mPFC relay during memory encoding in mice determining specificity/generalization of memory attributes (Xu and Südhof 2013).…”