Every sensory modality in the macaque is served by a series of cortical stations, each of which processes the sensory signal in turn. Signals in the later stations, located in the anterior temporo-insular cortex, can activate a circuit that runs through the limbic system to the neuromodulatory systems (e.g. cholinergic, noradrenergic, etc.) and back to the sensory cortical stations. We have proposed that as a result of the action of this circuit on neuromodulator release in sensory cortex, some of the neurons whose signals have just represented the sensory stimulus become linked together in a cell assembly that serves as the stored representation of that stimulus. Recognition, say of an object, occurs when an assembly formed on a first presentation of the object is reactivated by its re-presentation on a second occasion. Also, once formed, that assembly can be linked to assemblies representing other stimuli and other events, such as a food reward or a location, thereby investing the recognized object with meaning. The linkage involved in object-reward association appears to be mediated mainly by a limbo-neuromodulatory circuit running through the amygdala, the medial dorsal thalamic nucleus, orbital frontal cortex, and the basal nucleus of Meynert. Similarly, the linkage involved in object-place association seems to be mediated mainly by a second, parallel limbo-neuromodulatory circuit running through the hippocampus, the anterior thalamic nuclei, cingulate cortex, and the medial septal and diagonal band nuclei. Each of these circuits has reciprocal connections with one pair or the other of the assemblies described above. Thus, if these circuits have been activated, the sight of the object on a second occasion can lead not only to its recognition but also to recall of the food reward and the spatial location with which the object had been associated. Recognition and recall are two forms of cognitive memory, both of which can be distinguished from habit formation. The latter form of learning involves stimulus-response association specifically, and we have proposed that such learning depends largely on interactions between the cerebral cortex and the basal ganglia.
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