Dissociable performance on scene learning and strategy implementation after lesions to magnocellular mediodorsal thalamic nucleus

Abstract

Monkeys with aspiration lesions of the magnocellular division of the mediodorsal thalamus (MDmc) are impaired in object-in-place scene learning, object recognition, and stimulus-reward association. These data have been interpreted to mean that projections from MDmc to prefrontal cortex are required to sustain normal prefrontal function in a variety of task settings. In the present study, we investigated the extent to which bilateral neurotoxic lesions of the MDmc impair a preoperatively learnt strategy implementation task that is impaired by a crossed lesion technique that disconnects the frontal cortex in one hemisphere from the contralateral inferotemporal cortex. Postoperative memory impairments were also examined using the object-in-place scene memory task. Monkeys learnt both strategy implementation and scene memory tasks separately to a stable level preoperatively. Bilateral neurotoxic lesions of the MDmc, produced by 10 x 1 microl injections of a mixture of ibotenate and NMDA did not affect performance in the strategy implementation task. However, new learning of object-in-place scene memory was substantially impaired. These results provide new evidence about the role of the magnocellular mediodorsal thalamic nucleus in memory processing, indicating that interconnections with the prefrontal cortex are essential during new learning, but are not required when implementing a preoperatively acquired strategy task. Thus, not all functions of the prefrontal cortex require MDmc input. Instead, the involvement of MDmc in prefrontal function may be limited to situations in which new learning must occur.

Figure 1.

MDmc lesions. Schematic diagrams of six sections, 1 mm apart, through the posterior medial thalamus of a monkey taken from Gaffan and Murray (1990). The next three columns show photomicrographs of the MDmc lesions for MD1, MD2, and MD3 corresponding as closely as possible to the each of the schematic diagrams. Arrowheads indicate the site of each lesion. AD, Anterodorsal nucleus; AM, anteromedial nucleus; AV, anteroventral nucleus; Ca, caudate nucleus; CeM, central medial nucleus; CL, central lateral nucleus; CM, center median nucleus; CSL, central superior lateral nucleus; FX, fornix; Hl, lateral habenular nucleus; Hm, medial habenular nucleus; Hpt, habenulopeduncular tract; IT, inferotemporal cortex; LD, lateral dorsal nucleus; Li, limitans nucleus; LP, lateral posterior nucleus; MD, mediodorsal nucleus; MDdc, mediodorsal nucleus, densocellular portion; MDmc, magnocellular portion; MDmf, mediodorsal nucleus, multiformis portion; MDpc, mediodorsal nucleus, parvocellular portion; MG, medial geniculate complex; Mm, mamillary complex; Mtt, mamillothalamic tract; Pa, paraventricular nucleus; Pc, paracentral nucleus; Pf, parafascicular nucleus; Pla, anterior pulvinar nucleus; Pli, inferior pulvinar nucleus; Pl, lateral pulvinar nucleus; Po, posterior nucleus; Pa, parataenial nucleus; R, reticular nucleus; Re, reuniens nucleus; Rh, rhomboid nucleus; SG, suprageniculate nucleus; SN, substantia nigra; St, stria terminalis; Sub, subthalamic nucleus; VA, ventral anterior nucleus; VLa, ventral lateral nucleus, anterior portion; VLp, ventral lateral nucleus, posterior portion; VMb, ventral medial nucleus, basal portion; VMp, ventral medial nucleus, principal portion; VPi, ventral posterior inferior nucleus; VPl, ventral posterior lateral nucleus; VPm, ventral posterior medial nucleus; Zi, zona incerta.

Figure 2.

Scene learning. Mean percentage error on trials 2–8 of lists of new scene learning during preoperative and postoperative performance tests for MDmc, control, and full disconnection of frontal lobe from the inferotemporal cortex (FL by IT) (Browning et al., 2005) groups. Data presented are from individual animals.

Figure 3.

Scene learning. Mean learning curves for group neurotoxic magnocellular MDmc lesions and control monkeys during both preoperative and postoperative performance tests learning new sets of 20 scenes in eight repetition trials in a single session.

Figure 4.

Scene learning. A, Preoperative (preop) and postoperative (postop) learning curves for groups neurotoxic magnocellular MDmc lesions and controls. Data are grouped according to the outcome of the first trial of any problem, where 1C indicates scores when the first trial of each scene was correct and 1W indicates when the first trial was wrong. B, Preoperative (preop) and postoperative (postop) learning curves for the full disconnection of frontal lobe from the inferotemporal cortex (FL by IT), published previously by Browning et al. (2005).

Figure 5.

Strategy implementation. The mean trials/reward ratios for neurotoxic magnocellular MDmc lesions, controls, and full disconnection of frontal lobe from the inferotemporal cortex (FC by IT) (Gaffan et al. (2002) monkeys during both preoperative and postoperative performance tests are shown. Data presented are from individual animals.