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The Journal of Neuroscience, December 24, 2008, 28(52):14230-14244; doi:10.1523/JNEUROSCI.2882-08.2008

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Behavioral/Systems/Cognitive
Distinct Roles for Onset and Sustained Activity in the Neuronal Code for Temporal Periodicity and Acoustic Envelope Shape

Yi Zheng¹ and Monty A. Escabí^1,2

¹Biomedical Engineering and ²Electrical and Computer Engineering, University of Connecticut, Storrs, Connecticut 06269-1157

Correspondence should be addressed to Monty A. Escabí, University of Connecticut, Electrical and Computer Engineering, 371 Fairfield Way, U2157, Storrs, CT 06269. Email: escabi{at}engr.uconn.edu

Auditory neurons are selective for temporal sound information that is important for rhythm, pitch, and timbre perception. Traditional models assume that periodicity information is represented either by the discharge rate of tuned modulation filters or synchrony in the discharge pattern. Compelling evidence for an invariant rate or synchrony code, however, is lacking and neither of these models account for how the sound envelope shape is encoded. We examined the neuronal representation for envelope shape and periodicity in the cat central nucleus of the inferior colliculus (CNIC) with modulated broadband noise that lacks spectral cues and produces a periodicity pitch percept solely based on timing information. The modulation transfer functions of CNIC neurons differed dramatically across stimulus conditions with identical periodicity but different envelope shapes implying that shape contributed significantly to the neuronal response. We therefore devised a shuffled correlation procedure to quantify how periodicity and envelope shape contribute to the temporal discharge pattern. Sustained responses faithfully encode envelope shape at low modulation rates but deteriorate and fail to account for timing and envelope information at high rates. Surprisingly, onset responses accurately entrained to the stimulus and provided a means of encoding repetition information at high rates. Finally, we demonstrate that envelope shape information is accurately reflected in the population discharge pattern such that shape is readily discriminated for repetition frequencies up to 100 Hz. These results argue against conventional rate- or synchrony-based codes and provide two complementary temporal mechanisms by which CNIC neurons can encode envelope shape and repetition information in natural sounds.

Key words: inferior colliculus; periodicity; repetition; amplitude modulation; temporal code; phase locking; phasic; tonic

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Received June 23, 2008; revised Nov. 11, 2008; accepted Nov. 12, 2008.

Correspondence should be addressed to Monty A. Escabí, University of Connecticut, Electrical and Computer Engineering, 371 Fairfield Way, U2157, Storrs, CT 06269. Email: escabi{at}engr.uconn.edu

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