The pFC plays a key role in flexible, context-specific decision making. One proposal [Machens, C. K., Romo, R., & Brody, C. D. Flexible control of mutual inhibition: A neural model of two-interval discrimination. Science, 307, 1121–1124, 2005] is that prefrontal cells may be dynamically organized into opponent coding circuits, with competitive groups of cells coding opposite behavioral decisions. Here, we show evidence for extensive, temporally evolving opponent organization in the monkey pFC during a cued target detection task. More than a half of all randomly selected cells discriminated stimulus category in this task. The largest set showed target-positive activity, with the strongest responses to the current target, intermediate activity for a nontarget that was a target on other trials, and lowest activity for nontargets never associated with the target category. Second most frequent was a reverse, antitarget pattern. In the ventrolateral frontal cortex, opponent organization was strongly established in phasic responses at stimulus onset; later, such activity was widely spread across dorsolateral and ventrolateral sites. Task-specific organization into opponent cell groups may be a general feature of prefrontal decision making.

Six monkeys were trained preoperatively in an automated object-in-place memory task in which they learned 20 new scenes in each daily session. Three of the six monkeys then received stereotaxically guided bilateral mamillary body lesions, leaving the fornix intact, while the other three received a control operation. Postoperatively the control animals' rate of learning new scenes was unchanged, but the animals with mamillary body lesions showed a severe impairment, equal to that seen in previous experiments after fornix transection. All six animals were then given fornix transection, in addition to the existing mamillary or control operation. The control group now showed, after fornix transection, an impairment equal to that of the animals with mamillary body lesions alone. But the animals with mamillary body lesions did not show any additional impairment following fornix transection. We conclude that (1) the role of the mamillary bodies in a model of human episodic memory is as important as the role of the fornix, (2) the fornix and mamillary bodies form a single functional memory system, since the effect of lesions in both parts is no more severe than the effects of a lesion in one of the parts alone, and (3) the idea that the functional effects of fornix transection result from cholmergic deafferentation of the hippocampus receives no support from the present results; rather, they support the idea that in primates the fornix and mamillary bodies, together with connected structures, including the subiculum, mamillo-thalamic tract, anterior thalamic nuclei, and cingulate bundle, form a cortico-cortical association pathway for episodic memory.

A series of five experiments investigated the relationship between object memory and scene memory in normal and fornix-transected monkeys. An algorithm created formally defined background and objects on a large visual display; the disposition of some particular objects in particular places in a particular background constitutes a formally defined scene . The animals learned four types of discrimination problem: (1) object-in-place discrimination learning, in which the correct (rewarded) response was to a particular object that always occupied the same place in a particular unique background, (2) place discrimination learning, in which the correct response was to a particular place in a unique background, with no distinctive object at that place, (3) object discrimination learning in unique backgrounds, in which the correct response was to a particular object that could occupy one or the other of two possible places in a unique background, and (4) object discrimination learning in varying backgrounds, in which the correct response was to a particular object that could appear at any place in any background. The severest impairment produced by fornix transection was in object-in-place learning. Fornix transection did not impair object discrimination learning in varying backgrounds. The results from the other two types of learning task showed intermediate severity of impairment in the fornix-transected animals. The idea that fornix transection in the monkey impairs spatial memory but leaves object memory intact is thus shown to be an oversimplification. The impairments of object memory in the present experiments are analogous to the impairments of episodic memory seen in human amnesic patients.

Patients with visual associative agnosia have a particular difficulty in identifying visually presented living things (plants and animals) as opposed to nonliving things. It has been claimed that this effect cannot be explained by differences in the inherent visual discriminability of living and nonliving things. To test this claim further, we performed two experiments with normal subjects. In Experiment 1 normal human observers were asked to identify objects in tachistoscopically presented line drawings. They made more errors with living things than with nonliving things. In Experiment 2 normal monkeys learned to discriminate among the same line drawings for food reward. They made many more errors in discriminating among living things than nonliving things. Agnosic patients' responses to the same line drawings were made available to us for correlative analysis with the subjects' responses to these drawings in Experiments 1 and 2. We conclude that a category-specific visual agnosia for living things can arise as a consequence of a modality-specific but not category-specific impairment in visual representation, since living things are more similar to each other visually than nonliving things are.