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Processing of frequency-modulated stimuli in the chick auditory cortex analogue: evidence for topographic representations and possible mechanisms of rate and directional sensitivity

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Summary

Responses of units in the auditory forebrain (field L/hyperstriatum ventrale-complex) of awake domestic chicks were studied to frequency-modulated (FM) signals and isointensity tone bursts, presented to the ear contralateral to the recording sites. FM signals, linear frequency sweeps in the range of 50 Hz to 10.25 kHz, differed in the rate of change of frequency (RCF) and in the direction of modulation. The majority of RCF response functions obtained could be classified as predominantly ascending and bell shaped. Best rates of change of frequency (BRCFs), assigned to these functions, covered a range of nearly 3 orders of magnitude. BRCFs of the same units for upward (positive BRCFs) and for downward modulations (negative BRCFs) were correlated. The lowest BRCF encountered among all units for a given isointensity ON-response bandwidth (ΔF on ) increased as a function of ΔF on . ΔF on was derived from the responses to tone bursts of various frequencies at 70 dB SPL. As ΔFON tended to increase with the best frequency (BF) of units the lowest BRCF encountered among all units for a given BF also increased as a function of BF. Positive and negative BRCFs of a unit were also correlated with the slopes of onset latency-frequency relationships below and above BF, respectively. FM responses were optimal, when the frequency-specific latency differences at a given unit were compensated by the direction and rate of frequency change in the signal. FM-directional sensitivity varied with BF. Most units with BFs below about 2 kHz preferred upward modulations, while those with BFs above 2 kHz preferred downward modulations. Directional preference and sensitivity correlated with asymmetric distributions of inhibitory sidebands around BF, as derived from the analysis of OFF-responses. Maximum directional sensitivity for a given BRCF increased with BRCF. BRCF and FM-directional sensitivity were topographically organized on neuronal planes harboring units with similar BFs (“isofrequency planes”). Highest BRCFs were observed in the input-layer L2 of field L. BRCF declined along a rostrocaudal isofrequency axis in all 4 subdivisions of the auditory forebrain. Similarly, response strength shifted from rostral to caudal as a function of RCF. FM-directional sensitivity was organized in a subdivision-specific fashion. Units in the input-layer of field L (L2), and even more so in the hyperstriatum ventrale, were fairly insensitive to the direction of modulation, whereas units in the postsynaptic layers of field L (L1 and L3) exhibited higher degrees of directional sensitivity. Directional sensitivity also declined along the rostrocaudal isofrequency axis of field L. Two simple models of connectivity in the chick auditory forebrain are presented, which could be sufficient to explain these results. One is based on a tonotopic arrangement of afferent synapses on dendrites and somata of units in L2, the other on local lateral inhibition in the postsynaptic layers of field L.

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Abbreviations

BF:

best frequency (kHz)

BRCF:

best rate of change of frequency (kHz/s)

DS:

index of FM-directional sensitivity

ΔF on :

ON-response bandwidth (kHz)

ΔF off :

OFF-response bandwidth (kHz)

FM:

frequency modulation

RCF:

rate of change of frequency (kHz/s)

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Heil, P., Langner, G. & Scheich, H. Processing of frequency-modulated stimuli in the chick auditory cortex analogue: evidence for topographic representations and possible mechanisms of rate and directional sensitivity. J Comp Physiol A 171, 583–600 (1992). https://doi.org/10.1007/BF00194107

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