Aspiration lesions of the amygdala disrupt the rhinal corticothalamic projection system in rhesus monkeys

Abstract

In macaque monkeys, aspiration but not excitotoxic lesions of the medial temporal lobe limbic structures, the amygdala and hippocampus, produce a severe impairment in visual recognition memory. Furthermore, certain ventromedial cortical regions, namely the rhinal (i.e., entorhinal and perirhinal) cortex, are now known to be critical for visual recognition memory. Because the route taken by temporal cortical efferent fibers, especially perirhinal efferents, passes nearby the amygdala, it is possible that inadvertent damage to these fibers is produced by the aspirative but not the excitotoxic process, thereby accounting at least in part for the different behavioral outcomes of the two types of lesion. To test this idea, we assessed the integrity of the rhinal corticothalamic projection system after aspiration lesions of the amygdala. Three rhesus monkeys with unilateral amygdala removals received bilaterally symmetrical injections of a retrograde fluorescent tracer into the medial portion of the mediodorsal nucleus of the thalamus. Retrogradely labeled cells were identified using conventional fluorescence microscopy techniques. In all three cases, the rhinal cortex of the intact hemispheres contained moderate numbers of retrogradely labeled cells. By contrast, the rhinal cortex of the amygdalectomized hemispheres consistently contained few retrogradely labeled cells, and a direct comparison of the two hemispheres showed this difference to be statistically significant. A similar asymmetric pattern was observed for area TE but not for the cortex lining the dorsal bank of the superior temporal sulcus, nor for the rostral cingulate motor area, which was examined as a control. The results indicate that aspiration lesions of the amygdala not only remove the cell bodies of the amygdala, as intended, but also inadvertently disrupt projection fibers arising from cells in the rhinal cortex and area TE that pass nearby or through the amygdala en route to the thalamus. Behavioral studies examining the effects of aspiration lesions of the amygdala in nonhuman primates need to take these findings into consideration.

Selective Bilateral Amygdala Lesions in Rhesus Monkeys Fail to Disrupt Object Reversal Learning

“…Instead, damage to inferotemporal cortex appears to be responsible for the impairment (Baxter et al, 1999;. Together with evidence that aspirative removals of the amygdala disrupt the efferent projections of the rhinal cortex (Goulet et al, 1998), these findings indicate that damage to fibers passing near or through the amygdala, rather than loss of the cell bodies of the amygdala, accounts for some behavioral deficits observed after the aspirative removals. Given that lesions of rhinal cortex severely disrupt object reversal learning , it is possible that transection of rhinal cortical efferents, rather than amygdala damage, is responsible for the object reversal learning impairment seen after aspirative amygdala lesions.…”

In search of an auditory engram

“…The finding that the auditory memory of case Rh-2͞HϩPH was in fact preserved despite complete removal of the hippocampal system suggests a possible resolution of the contradiction, namely, that the impairment produced by the MT ablation resulted not from damage to the hippocampal system but from collateral damage, such as severing the projections of rSTG to downstream areas in the prefrontal cortex, medial thalamus, or both (e.g., see ref. 39). An anatomical study undertaken to examine this possibility (M. Munoz, M.M., and R.C.S., unpublished data) demonstrated that an MT removal does indeed disconnect rSTG anatomically from several prefrontal and medial thalamic areas.…”

Crossmodal binding of fear in voice and face

“…A role for the amygdala in crossmodal sensory processing has been proposed on the basis that surgical extirpations of the amygdala impaired intermodal, but not intramodal, performance on a delay nonmatch to sample (DNMS) task (32). However, subsequent experiments involving neurotoxic lesions to the amygdala failed to find deficits, whereas lesions to the anterior rhinal cortex resulted in major deficits (33). In studies with humans, amygdala damage has failed to result in deficits of intermodal sensory processing (9), although this negative finding was thought to reflect the fact that none of the tasks involved sensory-affective associations.…”