The nonhuman primate amygdala is necessary for the acquisition but not the retention of fear-potentiated startle.

BACKGROUND: In a previous study, we found that rhesus monkeys prepared with bilateral lesions of the amygdala failed to acquire fear-potentiated startle to a visual cue. However, a second group of monkeys, which received the lesion after training, successfully demonstrated fear-potentiated startle learned prior to the lesion. METHODS: In the current experiment, the eight monkeys used in the second part of the original study, four of which had bilateral amygdala lesions and the four control animals, were trained using an auditory cue and tested in the fear-potentiated startle paradigm. This test was performed to determine whether they could acquire fear-potentiated startle to a new cue. RESULTS: Monkeys with essentially complete damage to the amygdala (based on histological analysis) that had retained and expressed fear-potentiated startle to a visual cue learned before the lesion failed to acquire fear-potentiated startle to an auditory cue when training occurred after the lesion. CONCLUSIONS: The results suggest that while the nonhuman primate amygdala is essential for the initial acquisition of fear conditioning, it does not appear to be necessary for the memory and expression of conditioned fear. These findings are discussed in relation to a network of connections between the amygdala and the orbitofrontal cortex that may subserve different component processes of fear conditioning.

Acoustic startle reflex in rhesus monkeys: a review.

Modulation of the acoustic startle response is a simple and objective indicator of emotionality and attention in rodents and humans. This finding has proven extremely valuable for the analysis of neural systems associated with fear and anxiety. Until recently, there have been few efforts to develop acoustic startle measurement in non-human primates. Here we review recent work in which whole body acoustic startle amplitude has been measured in rhesus monkeys. Initial studies revealed that the amplitude of whole body startle in monkeys, as in rodents and humans, is directly proportional to acoustic stimulus intensity and gradually habituates with repeated exposures. Presentation of a weak acoustic stimulus 25-5,000 msec before a startle stimulus reduces startle amplitude by 40-50% depending on inter-stimulus interval length (prepulse inhibition). We have also measured significant fear-potentiated startle in the presence of a visual stimulus after pairing it with an inescapable pulse of pressurized air (fear-potentiated startle). This effect was reduced by diazepam and morphine, but not by buspirone. Ibotenic acid-induced lesions of the amygdala prevented the acquisition of fear-potentiated startle but, remarkably, did not prevent the expression of fear-potentiated startle when fear conditioning was carried out prior to the lesion. Finally, we have developed an objective measure of fear inhibition in monkeys using a novel conditioned inhibition procedure identical to one used in rats and humans. Our data demonstrate that acoustic startle in non-human primates successfully bridges rodent and human research. The opportunity now emerges to link concepts developed in rodents to the more complex neuroanatomical and cognitive processes common to monkeys and humans.

Perirhinal and parahippocampal cortices of the macaque monkey: projections to the neocortex.

We investigated the topographic and laminar organization of the efferent cortical projections of the perirhinal and parahippocampal cortices. Area 36 of the perirhinal cortex projects preferentially to areas TE and TEO, whereas area TF of the parahippocampal cortex projects preferentially to the posterior parietal cortex and area V4. Area TF projects to many regions of the frontal lobe, whereas area 36 projects mainly to the orbital surface. The insular and cingulate cortices receive projections from areas 36 and TF, whereas only area TF projects to the retrosplenial cortex. Projections to the superior temporal gyrus, including the dorsal bank of the superior temporal sulcus, arise predominantly from area TF. Area 36 projects only to rostral levels of the superior temporal gyrus. Area TF has, in general, reciprocal connections with the neocortex, whereas area 36 has more asymmetric connections. Area 36, for example, projects to more restricted regions of the frontal cortex and superior temporal sulcus than it receives inputs from. In contrast, it projects to larger portions of areas TE and TEO than it receives inputs from. The efferent projections of areas 36 and TF are primarily directed to the superficial layers of the neocortex, a laminar organization consistent with connections of the feedback type. Projections to unimodal visual areas terminate in large expanses of the cortex, but predominantly in layer I. Projections to other sensory and polymodal areas, in contrast, terminate in a columnar manner predominantly in layers II and III. In all areas receiving heavy projections, the projections extend throughout most cortical layers, largely avoiding layer IV. We discuss these findings in relation to current theories of memory consolidation.