Central olfactory connections in the macaque monkey

Abstract

The connections between the olfactory bulb, primary olfactory cortex, and olfactory related areas of the orbital cortex were defined in macaque monkeys with a combination of anterograde and retrograde axonal tracers and electrophysiological recording. Anterograde tracers placed into the olfactory bulb labeled axons in eight primary olfactory cortical areas: the anterior olfactory nucleus, piriform cortex, ventral tenia tecta, olfactory tubercle, anterior cortical nucleus of the amygdala, periamygdaloid cortex, and olfactory division of the entorhinal cortex. The bulbar axons terminate in the outer part of layer I throughout these areas and are most dense in areas that are close to the lateral olfactory tract. Labeled axons also were found in the superficial part of nucleus of the horizontal diagonal band. Retrograde tracers injected into the olfactory bulb labeled cells in the nucleus of the diagonal band and in all of the primary olfactory cortical areas except the olfactory tubercle. Electrical stimulation of the olfactory bulb evoked short‐latency unit responses and a characteristic field wave in the primary olfactory cortex. Multiunit activity in layer II tended to be of shorter latency than that in layer III and the endopiriform nucleus. Associational connections within the primary olfactory cortex were demonstrated with anterograde tracer injections into the piriform cortex and the entorhinal cortex. Injections into the piriform cortex near the lateral olfactory tract labeled axons in the deep part of layer I of many primary olfactory areas, but especially in areas near the tract. An injection into the rostral entorhinal cortex, distant to the lateral olfactory tract, labeled a complementary distribution of axons in deep layer I of olfactory areas medial and caudoventral to the tract. This organization resembles that reported in the primary olfactory cortex of the rat [Luskin and Price (1983) J. Comp. Neurol. 216:264–291]. The anterograde tracer injections into the piriform cortex and retrograde tracer injections into the orbital and medial prefrontal. Cortex and rostral insula label connections from the primary olfactory cortex to nine areas in the caudal orbital cortex, including the agranular insula areas Iam, lai, Ial, Iapm, and Iapl and areas 14c, 25, 13a, and 13m. The piriform cortex projects most heavily to layer I of these areas. Only Iam, Iapm, and 13a receive a substantial projection to the deeper layers. Areas Iam, Iapm, and 13a were also the only areas that responded with multiunit action potentials to olfactory bulb stimulation in anesthetized animals. Area Iam had predominantly short‐latency units, ranging from 4 to 6 msec after olfactory bulb stimulation: Area Iapm had predominantly longer latency units, with some units faithfully following the stimulus at latencies of 70–90 msec. A small region of area 13a had relatively long‐latency units. These neocortical connections and electrophysiological responses establish the presence of an olfactory representatioin in the posterior orbital cortex of the macaque. Similarities in the structure and connections of the primary olfactory cortex suggest a high degree of homology between the rat and monkey and allow inferences about the process of sequential olfactory activation in the primate. © 1994 Wiley‐Liss, Inc.