Functional development of olfactory nerve‐related neural circuits in the embryonic chick forebrain revealed by voltage‐sensitive dye imaging

• Published in: The European journal of neuroscience Vol. 56; no. 6; pp. 4914 - 4929
• Main Authors: Sato, Katsushige, Momose‐Sato, Yoko
• Format: Journal Article
• Language: English
• Published: Chichester Wiley Subscription Services, Inc 01-09-2022
• Subjects: Anatomy; chick embryo; Circuits; Dyes; Embryogenesis; Forebrain; Functional morphology; Glutamic acid receptors (ionotropic); Magnesium; N-Methyl-D-aspartic acid receptors; Neural networks; Olfactory bulb; Olfactory nerve; Olfactory pathways; Olfactory system; optical recording; Pallium; Smell; Voltage; voltage‐sensitive dye
• ISSN: 0953-816X; 1460-9568
• DOI: 10.1111/ejn.15788

Multiple‐site optical recordings with NK2761, a voltage‐sensitive absorption dye, were applied to the embryonic chick olfactory system, and the functional development of olfactory nerve (N.I)‐related neural circuits was examined in the forebrain. The stimulation of the N. I elicited neural responses in N.I‐olfactory bulb (OB)‐forebrain preparations at the embryonic 8–12 day (E8‐E12) stages. At the E11 stage, we functionally identified two circuits projecting from the OB to the forebrain. The first circuit passed through the ventral side of the forebrain and spread in the dorso‐caudal direction, whereas the second circuit passed through the dorsal side to the first circuit. Pharmacological experiments showed that N‐methyl‐D‐aspartate (NMDA) receptor function was more significant for the transfer of sensory information in these circuits. The functional development of N.I‐related circuits was investigated, and the results obtained revealed that the ventral circuit was generated earlier than the dorsal circuit. Neural responses in the ventral circuit were detected from the E9 stage in normal physiological solution and the E8 stage in Mg2+‐free solution, which activated NMDA receptor function. At the E10 stage, neural responses in the dorsal circuit were clearly recognised in addition to ventral responses. We attempted to identify possible candidates for relay nuclei in the forebrain by comparing contour line maps of the optical signal amplitude with previously reported neuroanatomical data. The results suggest that N.I‐related neural circuits from the periphery to the subpallium functionally mature earlier than those to the pallium during ontogenesis.
We applied voltage‐sensitive dye recording to the embryonic chick olfactory system and examined functional development of olfactory nerve‐related neural circuits in the forebrain. We functionally identified two neural circuits projecting from the olfactory bulb to the forebrain—the ventral circuit that spread in the dorso‐caudal direction, and the dorsal circuit that passed dorsally to the ventral circuit—and found that the ventral circuit was generated earlier than the dorsal circuit. In comparison with previously reported anatomical data, we suggest that the olfactory nerve‐related neural circuit from the periphery to the subpallium functionally matures earlier than that to the pallium during ontogenesis.