Three species were studied, the rabbit, opossum and rat. Lesions of the main olfactory bulb caused terminal degeneration, assayed by the Fink-Heimer method, to occur in the ipsilateral olfactory tubercle, prepyriform cortex (including its periamygdaloid part), ventrolateral entorhinal area, and in anterior and posterolateral divisions of the cortical amygdaloid nucleus. The various parts of the ipsilateral anterior olfactory nucleus and the rostroventral end of the anterior continuation of the hippocampus (hippocampal rudiment) also received this projection. Lesions of the accessory olfactory bulb, which receives its sensory input from the vomeronasal (Jacobson's) organ, caused terminal degeneration to occur in the medial amygdaloid nucleus and in a posteromedial part of the cortical amygdaloid nucleus. This projection was conveyed by an accessory olfactory tract, which is accompanied in part of its course by a small nucleus, the bed nucleus of the accessory olfactory tract. The accessory olfactory tract is initially a part of the lateral olfactory tract but becomes increasingly indivuated at more posterior levels. It parts company with the lateral olfactory tract at the rostral end of the amygdaloid region, and, in addition to distributing to the medio-cortical amygdaloid region, it enters the stria terminalis to terminate in the bed nucleus of the stria terminalis in a small region bearing cytoarchitectonic resemblance to the medial amygdaloid nucleus. The topographic segregation of the areas of termination of the olfactory and accessory olfactory (vomeronasal) projections is suggestive of a functional dichotomy in the organization of the olfactory system...

The medial (M) an posteromedial cortical (C3) amygdaloid nuclei and the nucleus of the accessory olfactory tract (NAOT) are designated the "vomeronasal amygdala" because they are the only components of the amygdala to receive a direct projection from the accessory olfactory bulb (AOB). The efferents of M and C3 were traced after injections of 3H-proline into the amygdala in male golden hamsters. Frozen sections of the brains were processed for autoradiography. The efferents of the "vomeronasal amygdala" are largely to areas which are primary and secondary terminal areas along the vomeronasal pathway, although the efferents from C3 and M terminate in different layers in these areas than do the projections from the vomeronasal nerve or the AOB. Specifically, C3 projects ipsilaterally to the internal granule cell layer of the AOB, the cellular layer of NAOT, and layer Ib of M. Additional fibers from C3 terminate in a retrocommissural component of the bed nucleus of the strain terminalis (BNST) bilaterally, and in the cellular layers of the contralateral C3. The medial nucleus projects to the cellular layer of the ipsilateral NAOT, layer Ib of C3, and bilaterally to the medial component of BNST. Projections from M to non-vomeronasal areas terminate in the medial preoptic area-anterior hypothalamic junction, ventromedial nucleus of the hypothalamus, ventral premammillary nucleus and possibly in the ventral subiculum. These results demonstrate reciprocal connections between primary and secondary vomeronasal areas between the secondary areas themselves. They suggest that M, but not C3, projects to areas outside this vomeronasal network. The medial amygdaloid nucleus is therefore an important link between the vomeronasal organ and areas of the brain not receiving direct vomeronasal input.

The anterior cortical (C1) and posterolateral cortical (C2) nuclei of the amygdala are designated the "olfactory amygdala" because they each receive direct projections from the main olfactory bulb. The efferents of these nuclei were traced after stereotaxic placement of 1-5 muCi tritiated proline in the corticomedial amygdala of the male golden hamsters. Following survival times of 12, 24, or 48 hours, 20 micron frozen sections of the brains were processed for light microscopic autoradiography. Efferents from C2 terminate in layers II and III of the olfactory tubercle and in layer Ib of pars ventralis and pars medialis of the anterior olfactory nucleus. Fibers from this nucleus also project to layers I and II of the infralimbic cortex and to the molecular layer of the agranular insular cortex. More posteriorly, fibers from C2 terminate in layer I of the dorsolateral entorhinal cortex, and in the endopiriform nucleus. From C1, efferent fibers travel in the stria terminalis and terminate in the precommissural bed nucleus of the stria terminalis and in the mediobasal hypothalamus. Efferents from C1 also innervate the molecular layer of C2, the amygdalo-hippocampal area, and the adjacent piriform cortex. Neurons in both C1 and C2 project to the molecular layer of the medial amygdaloid nucleus and the posteromedial cortical nucleus of the amygdala, the plexiform layer of the ventral subiculum, and the molecular layer of the lateral entorhinal cortex.

Previous studies suggest that the rostral corticomedial amygdala (CMA), particularly the medial nucleus, is an important site where vomeronasal and olfactory stimuli critical to male hamster copulatory behavior are processed. To test the possibility that mating deficits seen after lesions of the rostrally-placed medial nucleus may be due to the interruption of chemosensory afferents to more caudal areas, we injected tritiated amino acids into the accessory and main olfactory bulbs of male hamsters in which we had first produced bilateral electrolytic lesions or sham lesions in either the rostral CMA or basolateral amygdala, and then observed mating behavior. Autoradiographic analysis of "vomeronasal' projections from the accessory olfactory bulb and "olfactory' projections from the main bulb, revealed that rostral CMA lesions which damaged the medial nucleus and extended to the ventral surface of the brain (ventral lesions) interrupted vomeronasal input to the more caudally-placed posteromedial cortical nucleus, but spared olfactory inputs to adjacent caudal areas of the amygdala and piriform lobe. In contrast, lesions which damaged a major portion of the medial nucleus but left its ventral surface intact (dorsal lesions) spared both vomeronasal and olfactory inputs to more caudal areas. Animals with both dorsal and ventral lesions failed to mate postoperatively, whereas animals bearing sham lesions of basolateral amygdaloid lesions, which, like dorsal lesions, spared caudally-directed chemosensory afferents, continued to mate normally. We conclude that mating deficits seen after rostral CMA lesions are due primarily to destruction of the medial nucleus.

Deafferentation of the vomeronasal system by cutting the vomeronasal nerves severely impaired mating behavior in 44% of male hamsters over a 1--2 month period of postoperative testing, but the remaining males mated normally after the surgery. Damage to the main olfactory bulbs, concomitant to vomeronasal nerve cuts, did not account for this behavioral difference. Subsequent deafferentation of olfactory system by intranasal infusion of zinc sulfate solution (5 g ZnSO4--7H2O in 95 ml 0.5% NaCl) had no effect on intromission or ejaculation latencies of sham vomeronasal cut males but eliminated mating behavior 2 days after treatment in males with bilateral vomeronasal nerve cuts. Some of these males recovered the behavior in 1--3 weeks of post zinc sulfate testing. Histological analyses of the olfactory mucosa in 7 males on day 2 after zinc sulfate showed that 89--97% of the mucosa had been destroyed in 6 out of 7 of the males and 78% in the seventh. We conclude that destruction of the vomeronasal system irreparably reduces arousal necessary for mating in some hamsters but in other males sufficient arousal for this behavior to occur is mediated through the olfactory system, presumably in conjunction with other sensory inputs. Subsequent removal of the olfactory input in these animals eliminates the behavior.