Recanzone, G. H. | bioRxiv Science

bioRxiv2025

Neural Onset and Offset Responses in Core and Belt Auditory Cortex of Young and Aged Alert Macaque Monkeys

Age-related hearing loss is a ubiquitous malady in the geriatric population, yet the underlying neural mechanisms remain incompletely understood. We compared onset and offset responses of single neurons in the primary (A1), rostral (R), and caudolateral (CL) areas of the auditory cortex using spectral, spatial, and temporal stimuli in a young macaque monkey with normal-hearing and an aged macaque monkey with high frequency hearing loss. In the young monkey, core areas exhibited a significantly higher proportion of neurons responsive to both the onset and the offset of stimuli compared to the belt area CL, indicating functional differentiation. However, this distinction diminished with age, with the proportion of neurons with both onset and offset responses becoming more uniform across cortical areas. Onset firing rates were generally higher in the aged monkey, but with a lower signal-to-noise ratio, suggesting increased neural excitability but reduced response fidelity. Notably, CL neurons in the aged monkey exhibited a significantly greater disparity between the best frequencies for onset and offset responses, suggesting reduced spectral precision. Additionally, spectral tuning bandwidths (BW) were broader in the CL neurons in the aged monkey, while in the young monkey, A1 neurons exhibited significantly narrower onset BWs compared to offset BWs, a distinction that was lost in the aged monkey. These findings highlight a fundamental asymmetry in auditory cortical processing and suggest that belt area CL is particularly susceptible to age-related changes. Understanding these neural mechanisms provides insights into auditory aging and potential strategies for mitigating hearing deficits. New and NoteworthyThis study finds that there are significant differences in the temporal fidelity of auditory cortical neuronal responses as a function of natural aging, particularly in the belt cortical field CL compared to core areas A1 and R. These differences are stimulus dependent and are consistent with known auditory processing deficits in geriatric human subjects.

neuroscience↗

bioRxiv2025

Decoding of frequency modulated sweeps by core and belt neurons in the alert macaque auditory cortex.

Acoustic stimuli where the spectrum is time-varying are ubiquitous in natural sounds, including animal vocalizations, human speech, and music. Early studies of such stimuli involving frequency-modulated sweeps revealed that neurons in the primary auditory cortex of a variety of mammals show differences in firing rates depending on either the direction of the sweep and/or the sweep velocity. Psychophysical studies have also shown that the perception of such time-varying stimulus parameters is quite acute, underscoring the importance of such signals in normal acoustic perception. Surprisingly, the responses of auditory neurons in alert primates has been little studied, and we have limited information relating neural activity to the perception of these signals. In this study, we investigated the neural discriminability of sweep direction and velocity for frequency-modulated sweeps presented to alert rhesus macaque monkeys in both core and belt auditory cortical areas. We quantified how well these information-bearing parameters were encoded using spike train pattern discriminators, and compared decoder performance when neural responses were restricted to temporal patterns or firing rates. Decoding accuracy for firing rate alone exceeded chance, and rate-normalized, spike-timing information was essentially equivalent to the complete firing pattern. Although most belt areas showed small decreases in decoding accuracy relative to the primary field, all fields encoded and represented sweeps similarly. Thus, there was little evidence of hierarchical processing between core and belt fields for these stimuli, indicating that frequency modulation sweep direction and velocity are not specifically extracted in the early auditory cortical hierarchy. Significance StatementFrequency modulated (FM) stimuli are a key feature of many time-varying acoustic stimuli, including speech, vocalizations, music, and environmental sounds. The direction and velocity of FM stimuli are major information-bearing parameters that allow one to discriminate and perceive these sounds. We tested whether single neurons in core and belt auditory cortical fields in alert macaque monkeys preferentially process these features along the cortical hierarchy. We found that the timing of neural activity was much more important than the absolute amount of activity in all cortical areas, and did not observe any evidence of improved discriminability in core or belt fields beyond that seen in the primary auditory cortex (A1).

neuroscience↗