Abstract
The processing of neural information in neural circuits plays key roles in neural functions. Biophotons, also called ultra-weak photon emissions (UPE), may play potential roles in neural signal transmission, contributing to the understanding of the high functions of nervous system such as vision, learning and memory, cognition and consciousness. However, the experimental analysis of biophotonic activities (emissions) in neural circuits has been hampered due to technical limitations. Here by developing and optimizing an in vitro biophoton imaging method, we characterize the spatiotemporal biophotonic activities and transmission in mouse brain slices. We show that the long-lasting application of glutamate to coronal brain slices produces a gradual and significant increase of biophotonic activities and achieves the maximal effect within approximately 90 min, which then lasts for a relatively long time (>200 min). The initiation and/or maintenance of biophotonic activities by glutamate can be significantly blocked by oxygen and glucose deprivation, together with the application of a cytochrome c oxidase inhibitor (sodium azide), but only partly by an action potential inhibitor (TTX), an anesthetic (procaine), or the removal of intracellular and extracellular Ca2+. We also show that the detected biophotonic activities in the corpus callosum and thalamus in sagittal brain slices mostly originate from axons or axonal terminals of cortical projection neurons, and that the hyperphosphorylation of microtubule-associated protein tau leads to a significant decrease of biophotonic activities in these two areas. Furthermore, the application of glutamate in the hippocampal dentate gyrus results in increased biophotonic activities in its intrahippocampal projection areas. These results suggest that the glutamate-induced biophotonic activities reflect biophotonic transmission along the axons and in neural circuits, which may be a new mechanism for the processing of neural information.
Highlights
The processing of neural information in neural circuits plays a key role in neural functions [1,2] and functional neural circuits have been extensively investigated with in vitro and in vivo combinations of electrophysiological recording techniques and other approaches [3,4,5]
The number of spikes fired by neurons that originate from electrical and chemical transmission have been considered to be the primary mechanism for the encoding of neural information; the fire rate is not fully correlated to neural functions, and it is even very sparse or silent for most of the neurons in the hippocampus, neocortex and cerebellum under the appropriate behavioral conditions [8,9]
The biophotonic activities of the mouse brain slices bathed in a routine artificial cerebrospinal fluid (ACSF) were able to be detected and imaged spatiotemporally
Summary
The processing of neural information in neural circuits plays a key role in neural functions [1,2] and functional neural circuits have been extensively investigated with in vitro and in vivo combinations of electrophysiological recording techniques and other approaches [3,4,5]. It is well accepted that neuronal communication is mediated by bioelectricity and chemical molecules via the processes called electrical and chemical transmission, respectively, which mainly occur in axons and synapses [6]. They seem to provide explanations for the basic functions of the nervous system, the wide array of experimental observations regarding electrical and chemical transmission have made it difficult to construct general accepted concepts or principles to provide reasonable explanations of higher neural functions, such as sensory and motor control, vision, learning and memory, and cognition and consciousness. It has been believed that biophotons, being a coherent electromagnetic field inside the cells, may be the base of cell-to-cell communication [20], which has been demonstrated in plants, bacteria and certain animal cells [21,22]
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