Odorant-induced olfactory receptor neural oscillations and their modulation of olfactory bulbar responses in the channel catfish

Abstract

Peripheral waves (PWs) in the channel catfish are odorant-induced neural oscillations of synchronized populations of olfactory receptor neurons (ORNs) that appear after the initial approximately 500 msec of the response. The mean dominant frequency during the initial 2 sec of PW activity is approximately 28 Hz, declining to approximately 20 Hz in the last sec of a 5 sec stimulus. Recordings of PWs from different regions of a single olfactory lamella and simultaneously from widely separated lamellae within the olfactory organ suggest that PWs are initiated in the sensory epithelium within each olfactory lamella. Simultaneous recordings in vivo from the olfactory organ [electro-olfactogram (EOG) or integrated neural activity], local field potentials (LFPs) from the olfactory bulb (OB), and single and few-unit activity from OB neurons were performed. Cross-correlation analysis of simultaneously recorded odor-induced OB LFPs and either EOG or ORN neural activity showed that oscillations occurring within the OB were lower (<20 Hz) than those of PWs; however, during PW activity, OB LFPs increased both their magnitude and dominant frequencies and became correlated with the PWs. Also during odorant-induced PW activity, the responses of different OB neurons with similar odorant specificity became phase locked to each other and to both the PWs and OB LFPs. PWs are hypothesized to function to strengthen the synaptic transfer of olfactory information at specific glomeruli within the OB.

Fig. 1.

Different PW patterns were observed in response to 3 sec applications of a binary mixture of an amino acid and citrate.1, Continuous oscillations with similar magnitude in response to 0.1 mml-Met + 1 mmNa₃ citrate; 2, discontinuous oscillations with similar magnitude in response to 0.1 mml-Ala + 1 mm Na₃ citrate;3, continuous oscillations with declining magnitude in response to 0.1 mml-Met + 0.5 mmNa₃ citrate; 4, discontinuous oscillations with varying magnitude in response to 0.1 mml-Met + 1 mm Na₃ citrate;5, abbreviated response to 0.1 mml-Ala + 0.5 mm Na₃ citrate.

Fig. 2.

PWs are generated by stimulus mixtures containing an amino acid not present in the adapting solution. The olfactory epithelium was adapted to the ternary mixture l-Arg,l-Ala, and l-Na⁺ glutamate (each at 3 mm) for 5 min before the presentation of the stimulus mixture containing 1 mml-Met + 1 mm Na₃ citrate (A1) (Table 2), which was not present in the adaptation mixture. The stimulus mixture containing 1 mml-Ala + 1 mmNa₃ citrate (A2) (Table 2), consisting of an amino acid present in the adaptation mixture, did not trigger PWs.

Fig. 3.

Peripheral waves are generated within the olfactory sensory epithelium. A, Dorsal view of the olfactory organ of the channel catfish. M, Medial;C, caudal; L, lateral; R, rostral. B, Expanded view of a single olfactory lamella comprising sensory (filled medial portion of lamella) and nonsensory (NS) epithelia. PWs are recorded in response to a binary mixture of 1 mml-Met and 1 mm Na₃ citrate only within the sensory (1, 5) and not the NS (2–4) epithelia.Numbers represent the sequence of the recording electrode positions in a single preparation. All recordings shown were obtained in the same fish.

Fig. 4.

Cross-correlation analysis (0.5 sec) of olfactory receptor responses to 1 mml-Met + 1 mm Na₃ citrate recorded simultaneously with microelectrodes positioned within the sensory region of lamellae located at opposite ends (rostral and caudal) of the olfactory organ. No correlation was detected between the electrodes 0.5 sec before (A) and 0.5 sec after (B) stimulus onset. Correlation (time lag, ∼5 msec) between the odor responses recorded at the two electrodes was observed during PW activity 1 sec after stimulus onset (C). No correlation occurred after termination of the stimulus (D). All recordings were obtained in the same fish.

Fig. 5.

Distribution of the dominant frequency components of PWs in response to a 5 sec application of 1 mml-Met + 1 mm Na₃ citrate (n = 25 fish, 283 trials).

Fig. 6.

Olfactory receptor recordings and power spectral density analyses of neural oscillations in the olfactory epithelium. Actual recordings (A1–D1) from the same fish and their respective PSD analyses (percentage power of the frequencies between 0 and 50 Hz) (A2–D2). A, Prestimulus, 0.5 sec; B, 1.0–1.5 sec after stimulus onset;C, 1.5–2.0 sec after stimulus onset; D, the first 0.5 sec after termination of the 5 sec odor.

Fig. 7.

PSD analysis (0.5 sec; percentage power of frequencies between 0 and 50 Hz) of olfactory receptor neural recording (ORNR) (A, C) and olfactory bulbar local field potentials (OBLFP) (B, D) activity in the absence of (A, B) and during (C,D) PW activity. Left column, Analysis of spontaneous activity 0.5 sec before stimulus onset;middle column, analysis of the response 3.5 sec after stimulus onset; right column, analysis of the response 4 sec after stimulus onset. The stimulus in A andB is 1 mml-Met. The stimulus inC and D is 1 mml-Met and 1 mm Na₃ citrate. All recordings were obtained in the same fish.

Fig. 8.

Simultaneous recordings of OB LFP (Aa) and DC-recorded EOG (Ab) before (A1) and during (A2,3) PW response to 0.1 mml-Met + 0.5 mmNa₃ citrate. Delay between the start of PWs and the enhancement of OB LFP activity is shown (A2,3, arrows withdashed lines); PWs increase and decrease (portion of record between arrows with solid lines) in magnitude during response (A,b3). B, Cross-correlation analysis (0.5 sec) indicates correlation between EOG recorded PWs and OB LFPs before (B1) and during (B2, 3a,c) response to 0.1 mml-Met + 0.5 mm Na₃citrate; correlation declines during the decrease in PW magnitude (B,3b). There is no correlation between EOG and OB LFP activity 0.5 sec before stimulus presentation (B1).

Fig. 9.

Cross-correlation analysis between PWs and OB LFP. Simultaneously AC-recorded EOG (A) and OB LFP (B). Decrease in time lag during PW/OB LFP synchrony between initial (Aa, C) and later (Ab, D) portions of the PW response.

Fig. 10.

Simultaneous recordings of action potentials from three different OB neurons (A1–3) and the EOG (AC recorded) (A4) to 0.1 mml-Met + 0.5 mm Na₃ citrate in the same preparation as in Figure 9. Cross-correlation (1.5 sec) between EOG and the three OB units (B,C1–3) during initial (A,4a, B) and later (A,4b,C) portions of PW activity. Dashed linesin C indicate phase locking between PWs and three OB units.