Temporal selectivity of identified auditory neurons in the cricket brain

Abstract

1. The responses of fifty-eight neurons in the cricket brain to auditory stimuli were studied by intracellular recording, after which the cells were marked with Lucifer Yellow. These auditory interneurons could be assigned to three classes on the basis of anatomical criteria: (i) neurons (AN1 and AN2) ascending from the prothoracic ganglion into the brain, (ii) brain neurons (BNC 1) with arborizations overlapping those of ascending cells, and (iii) brain neurons (BNC 2) with arborizations that had no overlap with those of ascending cells. 2. All the ascending neurons had one projection field in common, an area in the anterior dorsal region of the diffuse neuropil lateral to the alphalobe. This field overlaps one of the projection fields of the BNC 1 neurons. Other projection fields of the BNC 1 neurons are frequently found in the posterior ventral region, at the boundary between the proto and deutocerebrum; the latter overlap projection fields of the BNC 2 cells, the arborizations of which are often not clearly distributed in more than one distinct region (Figs. 1–4). 3. The threshold curves and suprathreshold responses revealed that all three classes (AN, BNC 1 and BNC 2) include cells with low frequency (5 kHz) and others with broad-band (2–20 kHz) tuning; high-frequency (10–20 kHz) tuning was found only in AN and BNC 1 cells. Within the region to which the cells were tuned, sensitivity decreased in the order AN, BNC 1, BNC 2 (Figs. 2–4). A frequently observed property of BNC 2 neurons was independence of sound intensity in the suprathreshold intensity region. The response latency increased in the order AN, BNC 1, BNC 2 (Figs. 5, 6). 4. The effect of stimulus temporal structure was studied by presenting ‘constant-energy-chirps’, trains of sound pulses (syllables) varying in duration and repetition interval. The low frequency AN1 neurons, like other prothoracic neurons, copy such signals over a broad range of repetition intervals. Copying by the BNC 1 neurons was less accurate, and the responses of BNC 2 neurons were often not detectably synchronized with the syllables of the stimuli (Figs. 7–10). 5. Strikingly, the magnitude of the BNC 2 responses was in some cases (7 out of 15) found to vary with repetition interval; curves for the BNC 2 responses vs. repetition interval match closely those for the behavioral tracking response of females given an identical stimulus paradigm, and are independent of intensity at intensities 10 dB or more above threshold. By contrast, the responses of AN and most BNC 1 neurons are uniform, regardless of stimulus intensity, over the entire range of repetition intervals studied (Fig. 11). 6. Some BNC 2 neurons responded to constantenergy chirps only with short and intermediate or with intermediate and long repetition intervals, resembling the high-pass and low-pass neurons found in frogs (Fig. 12). This finding, the systematic latency differences, and the anatomical relationships among the AN, BNC 1 and BNC 2 cells all point to a rather specific picture of the way that the male calling song is recognized.