Odor coding properties of frog olfactory cortical neurons

• Published in: Neuroscience Vol. 74; no. 3; pp. 885 - 895
• Main Authors: Duchamp-Viret, P, Palouzier-Paulignan, B, Duchamp, A
• Format: Journal Article
• Language: English
• Published: Oxford Elsevier Ltd 01.10.1996; Elsevier
• Subjects: Animals; Anisoles; Biological and medical sciences; Cerebral Cortex - physiology; Discrimination (Psychology); electrophysiology; Electrophysiology - methods; frog; Fundamental and applied biological sciences. Psychology; Neurons - physiology; odor; Odorants; olfaction; Olfactory Bulb - physiology; olfactory cortex; Olfactory system and olfaction. Gustatory system and gustation; Pentanols; Rana ridibunda; sensory coding; Vertebrates: nervous system and sense organs; olfactory cortex; CAM, dl-camphor; LOT, lateral olfactory tract; olfaction; LIM, dl-limonene; odor; sensory coding; ISO, isoamyl acetate; PIN, pinacolone; ANI, anisole; frog; electrophysiology; ACE, acetophenone; MAK, methylamylketone; Olfactory cortex; Vertebrata; Olfactory pathway; Coding; Frog; Central nervous system; Olfaction; Amphibia; Electrophysiology; Salientia; Odor; Brain (vertebrata)
• DOI: 10.1016/0306-4522(96)00194-7
• ISSN: 0306-4522

Until now, in amphibians, response odor properties of primary cortical neurons had never been investigated. Furthermore, very few data on this subject are available in other species. This prompted us to explore the functional properties of olfactory cortical neurons at rest and in response to odors. To achieve this, our experience with odor coding in the first two stages of the frog olfactory system, the olfactory mucosa and the olfactory bulb, led us to use odor stimuli which were chemical compounds with known stimulating properties, delivered to the mucosa in controlled conditions over a wide concentration range. Most of the cortical neurons were found to be very silent at rest, their average spontaneous activity being significantly lower than that of bulb neurons recorded previously in the same conditions. Cortical cells displayed, with all odors combined, 35% excitatory responses and 8% inhibitory responses. The excitatory response rate was similar to that of the bulb, while the inhibitory response rate was about 4.5-fold lower. Interestingly, two functional groups of cortical cells emerged based both on differences in response temporal patterning to odors delivered at increasing concentrations and in qualitative discrimination power. Regarding intensity coding, group 1 cells (53%) displayed “classical” temporal pattern evolution, increase of discharge frequencies and decrease of latency and burst duration, over the concentration range. The responses of group 2 cells (47%) were clearly original, since they consisted of a single spike (or more rarely two spikes) occurring with a strictly reproducible latency at a given concentration and a decreased latency as a function of increasing concentration. The dynamics of cell recruitment in the cortex showed that group 1 cell recruitment mimicked that of mitral cells, group 2 cells being recruited at higher concentrations. The analysis of qualitative discrimination properties of cortical cells regarding the eight-odor set revealed that the discrimination power of group 2 cells was similar to that of mitral cells. By contrast, the qualitative discrimination power of group 1 cells was found to be similar to that of neuroreceptor cells. In conclusion, this pioneer approach leads us to report that olfactory cortical neurons of the frog are responsive to odors and can be clearly divided into two groups based on functional criteria. Group 1 cells, which were relatively selective, poorly discriminating but sensitive, may be mainly devoted to intensity coding. By contrast, group 2 cells, which were not very sensitive but were selective and discriminating, were hypothesized to provide minimal intensity coding and thus to be mainly devoted to qualitative discrimination tasks.