Abstract
Andersen et al. (1971) proposed that excitatory activity in the entorhinal cortex propagates topographically to the dentate gyrus, and on through a “trisynaptic circuit” lying within transverse hippocampal “slices” or “lamellae.” In this way, a relatively simple structure might mediate complex functions in a manner analogous to the way independent piano keys can produce a nearly infinite variety of unique outputs. The lamellar hypothesis derives primary support from the “lamellar” distribution of dentate granule cell axons (the mossy fibers), which innervate dentate hilar neurons and area CA3 pyramidal cells and interneurons within the confines of a thin transverse hippocampal segment. Following the initial formulation of the lamellar hypothesis, anatomical studies revealed that unlike granule cells, hilar mossy cells, CA3 pyramidal cells, and Layer II entorhinal cells all form axonal projections that are more divergent along the longitudinal axis than the clearly “lamellar” mossy fiber pathway. The existence of pathways with “translamellar” distribution patterns has been interpreted, incorrectly in our view, as justifying outright rejection of the lamellar hypothesis (Amaral and Witter, 1989). We suggest that the functional implications of longitudinally projecting axons depend not on whether they exist, but on what they do. The observation that focal granule cell layer discharges normally inhibit, rather than excite, distant granule cells suggests that longitudinal axons in the dentate gyrus may mediate “lateral” inhibition and define lamellar function, rather than undermine it. In this review, we attempt a reconsideration of the evidence that most directly impacts the physiological concept of hippocampal lamellar organization.
Highlights
In the discussion that follows, we address the question of whether the available anatomical evidence really negates the lamellar hypothesis, or whether longitudinal “translamellar” axons could be consistent with a model in which the granule cells are functionally separated from adjacent granule cells by lateral inhibition, and further, whether granule cell information transmitted to mossy cells and CA3 pyramidal cells via the undisputedly “lamellar” mossy fiber pathway is conveyed topographically to targets at multiple levels throughout the longitudinal axis of the hippocampus, inhibiting some targets and exciting others
SUMMARY AND CONCLUSION If the lamellar hypothesis is strictly defined from an anatomical perspective to imply that all excitatory activity must be restricted to single transverse slices no wider than the mossy fiber pathway, even a single axon traveling outside a thin transverse hippocampal “slice” might refute the entire hypothesis
There is little to be gained from such a restrictive definition of lamellar organization, which was neither stated nor implied in the original or subsequent discussions of the hypothesis (Andersen et al, 1971, 2000; Lømo, 1971, 2009)
Summary
The lamellar hypothesis of hippocampal function in its simplest original form posited that excitatory activity travels from the entorhinal cortex and through the hippocampus via a “trisynaptic circuit” lying within a series of parallel hippocampal “slices” or “lamellae” (Andersen et al, 1969, 1971) In this way, it was envisaged that temporal lobe interactions between the entorhinal cortex and the hippocampus were organized topographically, and that “lamellae” might operate independently, permitting a relatively simple structure to mediate complex behaviors. The original lamellar hypothesis (Andersen et al, 1971) did not anticipate all of the implications of the longitudinal axonal distributions of Layer II entorhinal neurons, dentate hilar mossy cells and CA3 pyramidal cells, and because these structural features can be Frontiers in Neural Circuits www.frontiersin.org
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