How auditory neurons count temporal intervals and decode information

• 成果类型: Article
• 署名作者: Alluri, Rishi K.; Rose, Gary J.; McDowell, Jamie; Mukhopadhyay, Anwesha; Leary, Christopher J.; Graham, Jalina A.; Vasquez-Opazo, Gustavo A.
• 署名单位: Utah System of Higher Education; University of Utah; University of California System; University of California Los Angeles; University of Mississippi; Dartmouth College; Utah System of Higher Education; University of Utah
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-9072
• DOI: 10.1073/pnas.2404157121
• 发表日期: 2024-08-27
• 关键词: whole-cell patch; voltage-clamp; cns neurons; inhibition; selectivity; excitation; treefrog; signals; errors; frog

摘要

The numerical sense of animals includes identifying the numerosity of a sequence of events that occur with specific intervals, e.g., notes in a call or bar of music. Across nervous systems, the temporal patterning of spikes can code these events, but how this information is decoded (counted) remains elusive. In the anuran auditory system, temporal information of this type is decoded in the midbrain, where interval- counting neurons spike only after at least a threshold number of sound pulses have occurred with specific timing. We show that this decoding process, i.e., interval counting, arises from integrating phasic, onset- type and offset inhibition with excitation that augments across successive intervals, possibly due to a progressive decrease in shunting effects of inhibition. Because these physiological properties are ubiquitous within and across central nervous systems, interval counting may be a general mechanism for decoding diverse information coded/encoded in temporal patterns of spikes, including bursts, and estimating elapsed time. Significance Numerical abilities are widespread across taxa, but the underlying neural basis is poorly understood. The anuran auditory system, which has neurons that count temporal intervals, is particularly well suited for investigating the numerosity sense. Here, we combined whole-cell recordings, in vivo, with focal pharmacological manipulations and estimation of excitatory and inhibitory conductances to show that counting is achieved when excitation, augmented over successive pulses, occurs within the temporal interval between the onset and offset phases of inhibition. Further, nonlinear shunting inhibition shaped the amplitude and selectivity of excitation, thereby contributing to interval counting. This work advances our mechanistic understanding of counting and sheds light on the origins of interval-based numerical abilities in animals.