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 multi-nuclei" 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.

Figure 1.

(Upper) Summary diagram showing the key connections in the macaque monkey of those medial diencephalic nuclei that form the focus of this review. The emphasis is on diencephalic connections with the medial temporal lobe and with the prefrontal cortex, and, for this reason, the various, direct cortico-cortical connections between the medial temporal lobe, posterior cingulate cortices, and prefrontal cortex are not depicted. It should be noted that none of the medial temporal projections to the medial diencephalon originate in the hippocampus proper. The thickness of the lines reflects the density of each projection. (Lower) Summary of thalamic projections to the hippocampus and rhinal cortices in macaque monkeys (Amaral and Cowan 1980; DeVito 1980; Insausti et al. 1987; Gower 1989). Dashed lines represent light projections. Abbreviations: AD, anterior dorsal nucleus; AM, anterior medial nucleus; AV, anterior ventral nucleus; CM, center median nucleus; DLPFC, dorsolateral prefrontal cortex; LD, lateral dorsal nucleus; MB, mammillary bodies; MD, medial dorsal nucleus, including pars magnocellular (mc); mPULV, medial pulvinar; MTT, mammillothalamic tract; OFC, orbital frontal cortex; Pa, paraventricular nucleus; PFC, prefrontal cortex; Pt, parataenial nucleus; Re, nucleus reuniens; Rh, rhomboid nucleus. The numbers correspond to cortical areas.

Figure 2.

Mammillary body atrophy is associated with disproportionate recall vs. recognition impairments (Tsivilis et al. 2008). The graph shows recall and recognition scores (and standard error) for the 11 colloid cyst cases with the smallest mammillary bodies (SMBG) from a total of 38 cases. The scaled scores are compiled from multiple tests (WMS-III, Warrington RMT, and the Doors and People Test). The comparison scores are those of the 11 colloid cyst cases with the largest mammillary body volumes (LMBG) from the same pool of 38 cases. The y-axis shows the mean scaled scores, and so a normal population would be expected to have a mean ≈10.0. Patients with the smallest mammillary bodies were significantly impaired on recall but not recognition.

Figure 3.

Evidence that mammillary body atrophy selectively disrupts recollective-based recognition (Vann et al. 2009a,b). Findings are shown for three tests designed to distinguish recollective-based from familiarity-based recognition. Colloid cyst patients were separated according to the size of their mammillary bodies to create two groups (both n = 9)—small mammillary bodies (SMB) and large mammillary bodies (LMB). Measures of recollection and familiarity were derived using the remember/know (R/K) procedure (A) and receiver operating characteristic (ROC) curves (C), leading to estimates of recollection and familiarity derived from these ROC curves (D). (B) The psychometric data from a larger group of 62 colloid cyst patients were also analyzed using structural equation modeling (SEM), and estimates of recollection and familiarity were derived from the best fit model. Data presented in histograms are means ± standard error of the mean. Group differences: **P < 0.01, ***P < 0.005.

Figure 4.

Delayed nonmatching-to-sample (DNMS) performance of cynomolgus monkeys with surgical lesions of the rhinal sulcus plus amygdala (RhA), medial thalamus (MT, i.e., Ath plus Pth), anterior medial thalamus (Ath), posterior medial thalamus (Pth), mammillary bodies (MB), fornix (FX), ventromedial prefrontal cortex (VMF), and dorsolateral prefrontal cortex (DLF). Performance is represented as the Z score difference from the normal control group in each study. In all cases, the graphs depict mean performance over three retention delays (30 sec, 60 sec, 120 sec). All Z scores are worse than the controls, i.e., all are –Z scores. Data are only taken from studies using very similar training and testing methods (Aggleton and Mishkin 1983a,b, 1985; Bachevalier et al. 1985a; Bachevalier and Mishkin 1986; Murray and Mishkin 1986).

Figure 5.

Schematic showing the proposed balance of action from diencephalic nuclei upon two independent components of recognition memory—recollective-based recognition (R) and familiarity-based recognition (K). The gradation from white (R) to black (K) is used to represent the relative involvement of the various diencephalic nuclei with these two information types. With the exception of the mammillary bodies, it seems unlikely that any other region has a purely selective effect on either R or K. Abbreviations: ATN, anterior thalamic nuclei; Intra, intralaminar thalamic nuclei; MB, mammillary bodies; MD, medial dorsal thalamic nucleus; Mid, midline thalamic nuclei.