Postnatal development of the entorhinal cortex: A stereological study in macaque monkeys

Abstract

The entorhinal cortex is the main gateway for interactions between the neocortex and the hippocampus. Distinct regions, layers, and cells of the hippocampal formation exhibit different profiles of structural and molecular maturation during postnatal development. Here, we provide estimates of neuron number, neuronal soma size, and volume of the different layers and subdivisions of the monkey entorhinal cortex (Eo, Er, Elr, Ei, Elc, Ec, Ecl) during postnatal development. We found different developmental changes in neuronal soma size and volume of distinct layers in different subdivisions, but no changes in neuron number. Layers I and II developed early in most subdivisions. Layer III exhibited early maturation in Ec and Ecl, a two-step/early maturation in Ei and a late maturation in Er. Layers V and VI exhibited an early maturation in Ec and Ecl, a two-step and early maturation in Ei, and a late maturation in Er. Neuronal soma size increased transiently at 6 months of age and decreased thereafter to reach adult size, except in Layer II of Ei, and Layers II and III of Ec and Ecl. These findings support the theory that different hippocampal circuits exhibit distinct developmental profiles, which may subserve the emergence of different hippocampus-dependent memory processes. We discuss how the early maturation of the caudal entorhinal cortex may contribute to path integration and basic allocentric spatial processing, whereas the late maturation of the rostral entorhinal cortex may contribute to the increased precision of allocentric spatial representations and the temporal integration of individual items into episodic memories.

Keywords: Macaca mulatta; RRID:SCR_000696, California National Primate Research Center Analytical and Resource Core; RRID:SCR_002526, Stereo Investigator; RRID:SCR_002865, SPSS; RRID:SCR_014199, Adobe Photoshop; allocentric spatial memory; episodic memory; hippocampal formation; infantile amnesia; medial temporal lobe; object memory; path integration.

Figure 1:

Low magnification photomicrographs of coronal sections through the adult rhesus monkey entorhinal cortex. Nissl-stained preparations, arranged from rostral (a) to caudal (d). Eo, olfactory subdivision; Er, rostral subdivision; Elr, lateral rostral subdivision; Elc, lateral caudal subdivision; Ei, intermediate subdivision; Ec, caudal subdivision; Ecl, caudal limiting subdivision. Scale bar = 1 mm.

Figure 2:

a. Unfolded map of the rhesus monkey entorhinal cortex illustrating the relative position of its seven subdivisions. Black arrows indicate the approximate rostrocaudal locations of the coronal sections illustrated in Figure 1. b. Percentage of the adult volume of the entire entorhinal cortex, at different ages during postnatal development. c. Percentage of the adult volumes of the seven subdvisions of the entorhinal cortex, at different ages during postnatal development. See main text for details.

Figure 3:

Percentage of the adult volume of the different layers of the seven subdivisions of the monkey entorhinal cortex, at different ages during postnatal development. a. area Eo; b. area Er; c. area Elr; d. area Ei; e. area Elc; f. area Ec; g. area Ecl. See main text for details.

Figure 4:

Percentage of the adult volume of neuronal soma size in the different layers of the seven subdivisions of the monkey entorhinal cortex, at different ages during postnatal development. a. area Eo; b. area Er; c. area Elr; d. area Ei; e. area Elc; f. area Ec; g. area Ecl. See main text for details.

Figure 5:

Summary of the different profiles of postnatal development in the seven subdivisions of the monkey entorhinal cortex. a. Volume of distinct layers. b. Neuronal soma size in distinct layers. See main text for details.