Object recognition and location memory in monkeys with excitotoxic lesions of the amygdala and hippocampus

Abstract

Earlier work indicated that combined but not separate removal of the amygdala and hippocampus, together with the cortex underlying these structures, leads to a severe impairment in visual recognition. More recent work, however, has shown that removal of the rhinal cortex, a region subjacent to the amygdala and rostral hippocampus, yields nearly the same impairment as the original removal. This raises the possibility that the earlier results were attributable to combined damage to the rostral and caudal portions of the rhinal cortex rather than to the combined amygdala and hippocampal removal. To test this possibility, we trained rhesus monkeys on delayed nonmatching-to-sample, a measure of visual recognition, gave them selective lesions of the amygdala and hippocampus made with the excitotoxin ibotenic acid, and then assessed their recognition abilities by using increasingly longer delays and list lengths, including delays as long as 40 min. Postoperatively, monkeys with the combined amygdala and hippocampal lesions performed as well as intact controls at every stage of testing. The same monkeys also were unimpaired relative to controls on an analogous test of spatial memory, delayed nonmatching-to-location. It is unlikely that unintended sparing of target structures can account for the lack of impairment; there was a significant positive correlation between the percentage of damage to the hippocampus and scores on portions of the recognition performance test, suggesting that, paradoxically, the greater the hippocampal damage, the better the recognition. The results show that, within the medial temporal lobe, the rhinal cortex is both necessary and sufficient for visual recognition.

Fig. 1.

Shaded regions indicate the location and extent of the intended lesion of the amygdala (oblique hatching) and hippocampus (gray) on standard coronal sections. Ventral (top right) and medial (bottom left) views of a standard rhesus monkey brain show the locations of these deep temporal lobe structures: amygdala, dotted line; hippocampus, dashed line. In addition, small arrows mark the boundaries of the entorhinal (ERh) and perirhinal (PRh) cortex, regions we intended to spare, on the coronal sections only (left hemisphere; +18, +16, +13, +10). Thenumerals indicate the distance in millimeters from the interaural plane.

Fig. 2.

Photomicrographs of Nissl-stained coronal sections showing the region of the medial temporal lobe in intact monkeys (a, c) and monkeys with excitotoxic lesions (b, d). a, Intact amygdala and portions of underlying rhinal cortex. b, Excitotoxic amygdala lesion in monkey AH7, photographed at the same magnification as a. Note the massive neuronal cell loss, gliosis, and atrophy in the amygdala, with relative preservation of neurons in the surrounding structures. c, Intact hippocampus, subicular complex, and underlying parahippocampal cortex.d, Excitotoxic hippocampal lesion in monkey AH1, photographed at the same magnification as c. Note the massive neuronal cell loss, gliosis, and atrophy in the hippocampus, partial cell loss in the subicular complex, and relative preservation of the surrounding regions.

Fig. 3.

Shaded regions on standard coronal sections indicate the location and extent of the excitotoxic amygdala and hippocampal lesions in monkeys AH1–AH3. Numeralsindicate the distance in millimeters from the interaural plane.

Fig. 4.

Photomicrographs of Nissl-stained coronal sections from monkey AH1. From top to bottom, the sections are approximately +17, +13, +8, and +4 mm from the interaural plane, respectively. Compare with Figures 2 and 3.

Fig. 5.

Photomicrographs of Nissl-stained coronal sections from monkey AH3. Left, top tobottom, The sections through the amygdala are approximately +18.5, +17, +16, and +14.5 mm from the interaural plane, respectively. Right, top tobottom, The sections through the hippocampus are approximately +11, +8, +6, and +4 mm from the interaural plane, respectively. Compare with Figures 2 and 3. Figure continues.

Fig. 5.

Photomicrographs of Nissl-stained coronal sections from monkey AH3. Left, top tobottom, The sections through the amygdala are approximately +18.5, +17, +16, and +14.5 mm from the interaural plane, respectively. Right, top tobottom, The sections through the hippocampus are approximately +11, +8, +6, and +4 mm from the interaural plane, respectively. Compare with Figures 2 and 3. Figure continues.

Fig. 6.

Shaded regions on standard coronal sections indicate the location and extent of the excitotoxic amygdala and hippocampal lesions in monkeys AH4–AH6. Numeralsindicate the distance in millimeters from the interaural plane.

Fig. 7.

Photomicrographs of Nissl-stained coronal sections from monkey AH4. From top to bottom, the sections are approximately +17, +13, +8, and +4 mm from the interaural plane, respectively. Compare with Figures 2 and 6.

Fig. 8.

Photomicrographs of Nissl-stained coronal sections from monkey AH5. From top to bottom, the sections are approximately +17, +13, +8, and +4 mm from the interaural plane, respectively. Compare with Figures 2 and 6.

Fig. 9.

Group mean scores on the DNMS performance test. The curves on the left show the effects of imposition of increasingly longer delays between sample presentation and choice, whereas the curves on theright show the effects of list-length testing. For each list item the minimal delay is 20 sec × the length of the list.SELECTIVE AH, Monkeys with bilateral excitotoxic lesions of the amygdala and hippocampus; NORMAL CONTROL, unoperated control monkeys.

Fig. 10.

Group mean scores on DNMS administered with a list length of 40 and reverse-order testing. Each pointrepresents the data obtained from a block of five sequential delays, the longest of which is shown on the abscissa. For example, the first point represents the mean score for delays ranging from 0.5 to 4.5 min, the second pointrepresents the mean score for delays ranging from 5.5 to 9.5 min, etc.SELECTIVE AH, Monkeys with bilateral excitotoxic lesions of the amygdala and hippocampus; NORMAL CONTROL, unoperated control monkeys.

Fig. 11.

Comparison between the results for monkeys with AH lesions (present study) and those for identically trained monkeys with rhinal cortex lesions reported by Meunier et al. (1993). AH (IBO), Monkeys with bilateral excitotoxic lesions of the amygdala and hippocampus (n = 7);Rh, monkeys with bilateral removals of the rhinal cortex (n = 7); CON, unoperated control monkeys (n = 8), consisting of the four controls from the present study plus the four controls from Meunier et al. (1993).