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, Iai, 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.(ABSTRACT TRUNCATED AT 400 WORDS)

Left hippocampal volume loss in Alzheimer's disease is reflected in performance on odor identification: A structural MRI study

“…The hippocampal area (MTL-H) included both the hippocampal formation and the retrosplenial gyri. Interestingly, all of these areas, with the possible exception of the lingual gyrus, receive olfactory projections (Carmichael et al, 1994;Cerf-Ducastel & Murphy, 2001;Price et al, 1991). It should be appreciated that the primary olfactory areas are more anatomically discreet than those relatively large regions of interest investigated in the present study.…”

“…Nevertheless, highly significant correlations were observed in the present study between odor threshold and volume of the amygdala in normal elderly persons (see Table 3). Only rarely in neuroimaging studies of olfaction has activation been detected in mesial temporal areas of amygdala (Cerf-Ducastel & Murphy, 2001;Small et al, 1997;Sobel et al, 2000;Zald & Pardo, 1997, entorhinal cortex (Cerf-Ducastel & Murphy, 2001;Levy et al, 1997;Zald & Pardo, 2000), parahippocampal gyrus, or hippocampus (Cerf-Ducastel & Murphy, 2001;Levy et al, 1997;Small et al, 1997;Zald & Pardo, 2000); although electrophysiological and anatomical studies indicate that the anterior cortical nucleus of the amygdala, the periamygdaloid area and the lateral entorhinal cortex receive direct projections from the olfactory bulb through the lateral olfactory track (Biella & De Curtis, 2000;Carmichael et al, 1994;Price, 1985;1987). The entorhinal area also receives olfactory projections from the amygdaloid area and the piriform cortex.…”

“…The entorhinal cortex is multimodal and its integrity is critical for the flow of olfactory information. In addition to hippocampal projections, entorhinal cortex projects to orbital frontal cortex and receives input from frontal cortex and amygdala, areas important for olfactory function (Carmichael et al, 1994). Thus, areas that evidence early neuropathy in Alzheimer's disease, particularly in the mesial temporal lobe, are areas that, in addition to their well-known importance for memory function (Squire, 1992), are also critical for the processing of olfactory information.…”

Altered Insula Response to Taste Stimuli in Individuals Recovered from Restricting-Type Anorexia Nervosa

“…However, discrimination of subregions of the insula is difficult because of the absence of landmarks. Functional divisions of the insula are based on cytoarchitectural, connectional and behavioral studies in higher primates (Kaada et al, 1953;Mesulam and Mufson, 1982;Carmichael et al, 1994). In general, the anterior, less differentiated half of the insula receives the majority of projections from the amygdala and thalamic taste centers, making it an ideal site for the formulation of hedonic representations of taste.…”

Attention to Odor Modulates Thalamocortical Connectivity in the Human Brain

“…The sense of smell is distinguished from other sensory modalities by its unique anatomical organization (Price, 1990;Carmichael et al, 1994;Shipley and Ennis, 1996). Afferent projections from the nasal periphery remain ipsilateral all the way to primary olfactory (piriform) cortex, and odor inputs can access limbic brain areas in as few as two synapses (Gottfried and Zald, 2005).…”