Episodic memory or the ability to store context-rich information about everyday events depends on the hippocampal formation (entorhinal cortex, subiculum, presubiculum, parasubiculum, hippocampus proper, and dentate gyrus). A substantial amount of behavioral-lesion and anatomical studies have contributed to our understanding of the organization of how visual stimuli are retained in episodic memory. However, whether auditory memory is organized similarly is still unclear. One hypothesis is that, like the “visual ventral stream” for which the connections of the inferior temporal gyrus with the perirhinal cortex are necessary for visual recognition in monkeys, direct connections between the auditory association areas of the superior temporal gyrus and the hippocampal formation and with the parahippocampal region (temporal pole, perhirinal, and posterior parahippocampal cortices) might also underlie recognition memory for sounds. Alternatively, the anatomical organization of memory could be different in audition. This alternative “indirect stream” hypothesis posits that, unlike the visual association cortex, the majority of auditory information makes one or more synapses in intermediate, polymodal areas, where they may integrate information from other sensory modalities, before reaching the medial temporal memory system. This review considers anatomical studies that can support either one or both hypotheses – focusing on anatomical studies on the primate brain, primarily in macaque monkeys, that have reported not only direct auditory association connections with medial temporal areas, but, importantly, also possible indirect pathways for auditory information to reach the medial temporal lobe memory system.

The temporal pole (TP) is the rostralmost portion of the human temporal lobe. Characteristically, it is only present in human and nonhuman primates. TP has been implicated in different cognitive functions such as emotion, attention, behavior, and memory, based on functional studies performed in healthy controls and patients with neurodegenerative diseases through its anatomical connections (amygdala, pulvinar, orbitofrontal cortex). TP was originally described as a single uniform area by Brodmann area 38, and von Economo (area TG of von Economo and Koskinas), and little information on its cytoarchitectonics is known in humans. We hypothesize that 1) TP is not a homogenous area and we aim first at fixating the precise extent and limits of temporopolar cortex (TPC) with adjacent fields and 2) its structure can be correlated with structural magnetic resonance images. We describe here the macroscopic characteristics and cytoarchitecture as two subfields, a medial and a lateral area, that constitute TPC also noticeable in 2D and 3D reconstructions. Our findings suggest that the human TP is a heterogeneous region formed exclusively by TPC for about 7 mm of the temporal tip, and that becomes progressively restricted to the medial and ventral sides of the TP. This cortical area presents topographical and structural features in common with nonhuman primates, which suggests an evolutionary development in human species.

The cortical mantle is not homogeneous, so that three types of cortex can be distinguished: allocortex periallocortex and isocortex. The main distinction among those three types is based on morphological differences, in particular the number of layers, overall organization, appearance, etc., as well as its connectivity. Additionally, in the phylogenetic scale, this classification is conserved among different mammals. The most primitive and simple cortex is the allocortex, which is characterized by the presence of 3 layers, with one cellular main layer; it is continued by the periallocortex, which presents 6 layers, although with enough differences in the layer pattern to separate three different fields: presubiculum (PrS), parasubiculum (PaS), and entorhinal cortex (EC). The closest part to the allocortex (represented by the subiculum) is the PrS, which shows outer (layers I-III) and inner (V-VI) principal layers (lamina principalis externa and lamina principalis interna), both separated by a cell poor band, parallel to the pial surface (layer IV or lamina dissecans). This layer organization is present throughout the anterior-posterior axis. The PaS continues the PrS, but its rostrocaudal extent is shorter than the PrS. The organization of the PaS shows the layer pattern more clearly than in the PrS. Up to six layers are recognizable in the PaS, with layer IV as lamina dissecans between superficial (layers I-III) and deep (V-VI) layers, as in the PrS. The EC presents even more clearly the layer pattern along both mediolateral and rostrocaudal extent. The layer pattern is a thick layer I, layer II in islands, layer III medium pyramids, layer IV as lamina dissecans (not present throughout the EC extent), layer V with dark and big pyramids, and a multiform layer VI. The EC borders laterally the proisocortex (incomplete type of isocortex). Variations in the appearance of its layers justify the distinction of subfields in the EC, in particular in human and nonhuman primates. EC layers are not similar to those in the neocortex. The transition between the periallocortical EC and isocortex is not sharp, so that the proisocortex forms an intervening cortex, which fills the gap between the periallocortex and the isocortex.

Hippocampal formation plays a prominent role in episodic memory formation and consolidation. It is likely that episodic memory representations are constructed from cortical information that is mostly funnelled through the entorhinal cortex to the hippocampus. The entorhinal cortex returns processed information to the neocortex. Retrograde tracing studies have shown that neocortical afferents to the entorhinal cortex originate almost exclusively in polymodal association cortical areas. However, the use of retrograde studies does not address the question of the laminar and topographical distribution of cortical projections within the entorhinal cortex. We examined material from 60 Macaca fascicularis monkeys in which cortical deposits of either ³H‐amino acids or biotinylated dextran‐amine as anterograde tracers were made into different cortical areas (the frontal, cingulate, temporal and parietal cortices). The various cortical inputs to the entorhinal cortex present a heterogeneous topographical distribution. Some projections terminate throughout the entorhinal cortex (afferents from medial area 13 and posterior parahippocampal cortex), while others have more limited termination, with emphasis either rostrally (lateral orbitofrontal cortex, agranular insular cortex, anterior cingulate cortex, perirhinal cortex, unimodal visual association cortex), intermediate (upper bank of the superior temporal sulcus, unimodal auditory association cortex) or caudally (parietal and retrosplenial cortices). Many of these inputs overlap, particularly within the rostrolateral portion of the entorhinal cortex. Some projections were directed mainly to superficial layers (I–III) while others were heavier to deep layers (V–VI) although areas of dense projections typically spanned all layers. A primary report will provide a detailed analysis of the regional and laminar organization of these projections. Here we provide a general overview of these projections in relation to the known neuroanatomy of the entorhinal cortex.

Background: Vertebrates sense chemical stimuli through the olfactory receptor neurons whose axons project to the main olfactory bulb. The main projections of the olfactory bulb are directed to the olfactory cortex and olfactory amygdala (the anterior and posterolateral cortical amygdalae). The posterolateral cortical amygdaloid nucleus mainly projects to other amygdaloid nuclei; other seemingly minor outputs are directed to the ventral striatum, in particular to the olfactory tubercle and the islands of Calleja. Results: Although the olfactory projections have been previously described in the literature, injection of dextran-amines into the rat main olfactory bulb was performed with the aim of delimiting the olfactory tubercle and posterolateral cortical amygdaloid nucleus in our own material. Injection of dextran-amines into the posterolateral cortical amygdaloid nucleus of rats resulted in anterograde labeling in the ventral striatum, in particular in the core of the nucleus accumbens, and in the medial olfactory tubercle including some islands of Calleja and the cell bridges across the ventral pallidum. Injections of Fluoro-Gold into the ventral striatum were performed to allow retrograde confirmation of these projections. Conclusion: The present results extend previous descriptions of the posterolateral cortical amygdaloid nucleus efferent projections, which are mainly directed to the core of the nucleus accumbens and the medial olfactory tubercle. Our data indicate that the projection to the core of the nucleus accumbens arises from layer III; the projection to the olfactory tubercle arises from layer II and is much more robust than previously thought. This latter projection is directed to the medial olfactory tubercle including the corresponding islands of Calleja, an area recently described as critical node for the neural circuit of addiction to some stimulant drugs of abuse.